By Max Aravena-Román BScAppSci FASM This thesis is presented for the degree of Doctor of Philosophy School of Pathology and Laboratory Medicine of Western Australia 2015 Classification, antimicrobial susceptibility and virulence factors of Aeromonas species in Western Australia
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Phylogeny, antimicrobial susceptibility and
virulence factors of Western Australian
By
Max Aravena-Román BScAppSci FASM
This thesis is presented for the degree of Doctor of
Philosophy
School of Pathology and Laboratory Medicine of
Western Australia
2015
Classification, antimicrobial susceptibility and virulence factors of Aeromonas species in
Western Australia
-i-
TABLE OF CONTENTS TABLE OF CONTENTS.................................................................................................i
Members of the genus Aeromonas are Gram-negative rods globally distributed in
aquatic and soil environments. For over one hundred years they have been associated
with infections in humans, other mammals and cold-blooded species. Infections in fish
and snails have resulted in serious financial losses to the aquaculture and French snail
farming industry.
Before the advent of molecular techniques, classification of Aeromonas was based
solely on the different phenotypic characteristics associated with each individual
species. However, the heterogeneous nature of motile and mesophilic Aeromonas
species has led to an unreliable and unstable taxonomy and schemes designed for the
identification of this group have not always been suitable for the identification of non-
motile, psychrophilic species.
The aims of this research were:
1. To characterize a collection of clinical and environmental Aeromonas isolates
from the state of Western Australia using phenotypic and genotypic methods in
order to determine the prevalence of species in this region.
2. To investigate the taxonomic position of isolates as determined by phylogenetic
trees.
3. To determine the antimicrobial susceptibility patterns of clinical and
environmental Aeromonas spp. to antibacterial agents currently in use in clinical
practice.
4. To assess the presence of virulence factors of Aeromonas species in order to
determine the presence of pathogenic strains currently circulating within the WA
community and its environment.
Aeromonas isolates were collected from rural and metropolitan areas of Western
Australia, the largest state in Australia covering an area of 2.5 million km2, for a period
of over 20 years. Phenotypic characterization of isolates was performed by a
conventional biochemical method that included more than 35 tests and by which
approximately 93% of the isolates were identified to the species level. Aeromonas
hydrophila was by far the most predominant aeromonad isolated from clinical and
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environmental samples and represented more than 50% of the species. These results
suggested that phenotypic identification was inadequate since 7% of the strains could
not be assigned to any known taxa.
Genotypic identification was based on the molecular sequences of the gyrB and rpoD
housekeeping genes by a PCR-based method. Phylogenetic trees generated from the
nucleotide sequences of the isolates tested indicated that A. dhakensis and not A.
hydrophila was the most frequently isolated aeromonad. Genotypic classification
resulted in the assignation of 99% of the strains to a species suggesting that accurate
identification of Aeromonas must involve a molecular method.
The antimicrobial susceptibility pattern of each isolate was assessed against 26
antimicrobials representing all classes currently in-use in clinical practice. Susceptibility
of each isolate was determined by the agar dilution and E-strip methods. Antibiotic
profiles indicated that the level of antimicrobial resistance in Western Australian
aeromonads is generally very low although antimicrobial susceptibility testing should
be performed in all strains isolated from human clinical material.
Phylogenetic trees derived from the nucleotide sequences of the gyrB and rpoD
housekeeping genes showed that the position of strain 266 isolated from irrigation water
in rural Western Australia did not cluster with any of the current validated Aeromonas
species. Extensive polyphasic testing that included multilocus phylogenetic analysis,
cellular fatty acid, protein profiles and DNA-DNA hybridization confirmed that strain
266 represented a novel Aeromonas species for which the name A. australiensis species
novo was proposed.
The distribution and prevalence of 13 virulence genes and the activity of four
extracellular enzymes was examined among 130 Aeromonas strains comprising 11
different species. Detection of virulence genes was performed by a PCR-based method
while enzyme activity was evaluated by biological assays. Results indicated that clinical
and environmental strains of A. hydrophila and A. dhakensis are more likely to carry
multiple virulence genes compared to strains of A. veronii and A. caviae. However, the
pathogenic potential of Aeromonas may be strain rather than species dependent, thus
under certain conditions which include host predisposition, a range of aeromonads may
be able to cause infection.
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DECLARATION
_______________________________________
All work presented in this thesis was performed by me and contributions made by
others are duly stated. Identification of Aeromonas by phenotypic methods and
antimicrobial susceptibility testing was performed entirely by me. Identification by
molecular methods and detection of virulence genes was performed by me except for
the preparation of gels and sequencing that was performed by staff from the PCR
Laboratory at PathWest, Nedlands. Polyphasic identification of Aeromonas
australiensis was 50% performed by me and 50% by Dr. R. Beaz-Hidalgo, Facultat de
Cience i Medicina de la Salut, University Rovira i Virgili, Reus, Spain.
Electronmicrograph of bacterial cells of A. australiensis was performed by Prof. Maria
Jose Figueras, Facultat de Cience i Medicina de la Salut, University Rovira i Virgili,
Reus, Spain.
This thesis contains a series of published work that has been co-authored. The following
journal articles constitute the individual chapters of this thesis:
Aravena-Román, M., B. J. Chang, T. R. Riley, and T. J. J. Inglis (2011a). Phenotypic
characteristics of human clinical and environmental Aeromonas in Western Australia.
Pathology 43: 350-356 (Chapter 3).
Aravena-Román, M., G. B. Harnett, T. V. Riley, T. J. J. Inglis and B. J. Chang (2011b).
Aeromonas aquariorum is widely distributed in clinical and environmental specimens
and can be misidentified as Aeromonas hydrophila. Journal of Clinical Microbiology
49: 3006-3008 (Chapter 4).
Aravena-Román, M., T. J. J. Inglis, B. Henderson, T. V. Riley, and B. J. Chang (2012).
Antimicrobial susceptibilities of Aeromonas strains isolated from clinical and
environmental sources to 26 antimicrobial agents. Antimicrobial Agents and
Chemotherapy 56: 1110-1112 (Chapter 5).
Aravena-Román, M., R. Beaz-Hidalgo, T. J. J. Inglis, T. V. Riley, A. J. Martínez-
Murcia, B. J. Chang and M. J. Figueras (2013). Aeromonas australiensis sp. nov.
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isolated from irrigation water in Western Australia. International Journal of
Evolutionary and Systematic Microbiology 63: 2270-2276 (Chapter 6)
Aravena-Román, M., T. J. J. Inglis, T. V. Riley and B. J. Chang (2014). Distribution of
13 virulence genes among clinical and environmental Aeromonas species in Western
Australia European Journal of Clinical Microbiology and Infectious Diseases 33: 1889-
1895 (Chapter 7).
Except for the work performed in the description of the new species A. australiensis
(50% of experimental work), all experimental work (100%) and initial manuscripts
preparation (100%) was performed by me. Editorial advice and guidance for the
manuscripts’ submissions and final corrected versions were provided by my supervisors
Professor Barbara Chang (40% editorial), Professor Timothy Inglis (30% editorial) and
Professor Thomas Riley (30% editorial). Other co-authors provided access to laboratory
equipment and facilities.
Max Aravena-Román
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ACKNOWLEDGEMENTS
I am indebted to my supervisors B. Chang, T. Inglis and T. Riley for their continuous
support, encouragement and guidance.
I would like to thank the staff of the Microbiology Division at PathWest, Nedlands
campus who provided bacterial isolates and access to equipment and reagents. To Rod
Bowman for making the necessary funds available to finance this project.
Thanks to Dr. Nicky Buller, Bacteriology Laboratory, Agriculture Department of
Western Australia, South Perth; Mr. Steve Munyard, Division of Microbiology and
Infectious Diseases, PathWest, Nedlands campus; Mr. Neil Stingemore, Department of
Microbiology, Fremantle Hospital, PathWest, Fremantle campus; Mr. Peter Campbell,
Department of Microbiology, Princess Margaret Hospital, Subiaco, Perth; Professor
Peter Käempfer, Institut für Angewandte Mikrobiologie, Justus-Liebig Universität,
Giessen, Germany; Professor Silvia Kirov, Department of Pathology, University of
Tasmania, Hobart, Tasmania, Australia; Dr. J. Michael Janda, Microbial Diseases
Laboratory, State of California, USA; and Dr. David Miñana-Galbis, Facultat de
Farmacia, Unitat de Microbiologia, Universitat de Barcelona, Barcelona, Spain for
kindly providing bacterial isolates.
To my colleagues, Glenys Chidlow, Gerry Harnett, Adam Merritt, Nikki Foster, Avram
Levy, and Barbara Henderson for their advice, guidance and support. A special thanks
to Diane Bleasdale for her excellent librarian services, to John Boehm from Excel,
PathWest, for providing me with special media and reagents and to my Spanish
colleagues, Professor María Jose Figueras and Dr. Roxana Beaz-Hidalgo from the
Facultat de Cience and Medicina de la Salut, University of Rovira i Virgili, Reus, Spain
and Dr. Antonio Martínez-Murcia from the Departamento de Produccion Vegetal y
Microbiología, EPSO, Universidad Miguel Hernández, Orihuela Alicante, Spain for
their invaluable training, advice and for their generosity in sharing bacterial isolates.
Thank you to Dr. Eduardo Alvarez from ICBM, Programa de Microbiología y
Micología, Facultad de Medicina, University of Chile, Santiago, Chile who provided
much training in sequence analysis and other computer issues and to Cati Nuñez from
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the Facultat de Cience and Medicina de la Salut, University of Rovira i Virgili, Reus,
Spain for her invaluable technical support.
Finally, thanks to my wonderful wife Naomi for her unconditional love and support.
To my beloved Mum Carmen Román Díaz (RIP)
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THESIS STRUCTURE
The body of this research is preceded by an extensive review of the literature in Chapter
1 in which historical, taxonomical issues, antimicrobial susceptibility and the relation of
Aeromonas to human disease are presented. All materials and methods described in
Chapters 3 to 7 are outlined in Chapter 2. Chapters 3 to 7 of this thesis are based on
material published by the candidate and peer reviewed.
Chapter 3 describes the characterization of isolates by phenotypic methods followed by
classification by genotypic methods as presented in Chapter 4. The antimicrobial
susceptibility pattern of 193 strains constitutes Chapter 5. The discovery and proposal
of a novel Aeromonas species is described in Chapter 6. In Chapter 7, the virulence
potential based on the detection and distribution of virulence genes and enzyme activity
is examined in a selected group of strains. Final discussion addressing the results and
conclusions obtained from all other chapters is presented in Chapter 8.
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ABBREVIATIONS ACN acetonitrile ADA ampicillin dextrin agar ADWA Agriculture Department of Western Australia AFLP amplified fragment length polymorphism AMX amoxicillin AMC amoxicillin-clavulanate AMK amikacin AMP ampicillin AnO2 anaerobic APW alkaline peptone water Aq. soln. aqueous solution ATCC American Type Culture Collection ATM aztreonam BAA blood ampicillin agar bv biovar BOC British Oxygen Company bp base pair(s) BSA bovine serum albumin cm centimetre C degrees Celsius CCUG Culture Collection of the University of Göteborg CFA cellular fatty acid CFU colony forming unit(s) CAMP Christie-Atkins-Munch-Peterson CAPD continuous ambulatory peritoneal dialysis CAZ ceftazidime CDC Center for Disease Control CECT Coleccion Española de Cultivos Tipo CEF cephalothin CFZ cefazolin CHO Chinese hamster ovary CIN cefsulodin irgasan novobiocin CIP Collection Bactérienne de l’Institute Pasteur CIP ciprofloxacin CLED cysteine lactose electrolyte deficient CLSI Clinical Laboratory Standard Institute CNA colistin nalidixic acid COL colistin CRO ceftriaxone CSF cerebral spinal fluid d day(s) Da Dalton DAA Difco ampicillin agar DEF deferoxamine DepC diethyl procarbonate DDH DNA-DNA hybridization DNA deoxyribonucleic acid DNAT deoxyribonucleic acid agar plus toluidine blue
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DNase deoxyribonuclease dNTP deoxyribonuclease triphosphate(s) DOX doxycycline DSM Deutsche Sammlung von Mikroorganismen und Zelkuturen ERIC enterobacterial repetitive intergenic consensus ESBL extended-spectrum -lactamase FA formic acid FAME fatty acid methyl ester(s) FEP cefepime FH Fremantle hospital FOX cefoxitin g gram(s) g relative centrifugal force G + C guanine plus cytosine GC gas chromatograph GCAT glycerophospholipid-cholesterol acyltransferase GCF gelatine-cysteine-thiosulfate GEN gentamicin GMP guanosine monophosphate GSP glutamate starch phenol h hour(s) HBA horse blood agar HCCA -cyano-4-hydroxycinnamic acid HG hybridization group HIA heart infusion agar HIB heart infusion broth HPLC high performance liquid chromatography HUS haemolytic uraemic syndrome I intermediate IM intramuscular IP intraperitoneal IBB inositol bile salts brilliant green kb kilobases(s) Km2 square kilometre L litre LBA Luria Bertoni agar LDC lysine decarboxylase LMG Culture Collection of the Laboratorium voor Microbiologie Gent LPS lipopolysaccharide LT labile toxin M molar M mole(s) MALDI-TOF matrix assistedlaser-desorption/ionization mass spectrometry time-of
flight MEM meropenem mg milligram(s) MHA Mueller-Hinton agar MIC minimum inhibitory concentration MIC50 MIC required to inhibit the growth of 50% of organisms MIC90 MIC required to inhibit the growth of 90% of organisms min minute(s) ml millilitre(s)
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MLCK myosin light chain kinase MLPA multilocus phylogenetic analysis MLST multilocus sequence analysis mm millimetre(s) mM millimole(s) MTCC Microbial Type Culture Collection and GeneBank MWA Metropolitan Water Authority MW molecular weight MXF moxifloxacin NaCl sodium chloride NA nutrient agar NAL nalidixic acid N/A not applicable NaOH sodium hydroxide NCIMB National Collection of Industrial and Marine Bacteria NCTC National Collection of Type Cultures ND not detected NIT nitrofurantoin nm nanometre(s) No. number NOR norfloxacin NSW New South Wales nt nucleotide(s) O2 oxygen O/129 2,4-diamino-6,7-diisopropylpteridine ONPG o-nitrophenyl--D-galactopyranoside O/F oxidation/fermentation o/v overnight PCR polymerase chain reaction PFGE pulse field gel electrophoresis pH concentration of hydrogen ions PMH Princess Margaret Hospital PPA phenylalanine deaminase psi pounds per square inch PYR pyrrolidonyl--naphthylamide PYZ pyrazinamidase QE II Queen Elizabeth II R resistant RAPD randomly amplified polymorphic DNA RBC red blood cells RILs rabbit ileal loops RNA ribonucleic acid rpm revolutions per minute s second(s) S susceptible SAA starch ampicillin agar SBA sheep blood agar SCGH Sir Charles Gairdner Hospital SDS sodium dodecyl sulphate SDH Swan District Hospital SF summed feature SI similarity index
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spp. species sp. nov. species novo ssp. subspecies SSSD Salmonella Shigella agar plus sodium desoxycholate ST stable toxin SXT trimethoprim-sulfamethoxazole TCBS thiosulfate citrate bile sucrose TFA trifluoroacetic acid TGC tigecycline TIM ticarcillin-clavulanate TMP trimethoprim TOB tobramycin TSA trypticase soy agar TSB trypticase soy broth TSBA trypticase soy broth agar TZP pipercillin-tazobactam U unit(s) micron(s) g microgram(s) l microlitre(s) m micrometre(s) M micromole(s) UPW ultrapure water w/v weight to volume WA Western Australia XLDA xylose lysine desoxycholate agar XDCA sylose desoxycholate citrate agar + positive negative
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LIST OF TABLETS Table 1.1 Current Aeromonas species p. 5
Table 1.2 Examples of media used in the isolation of Aeromonas
from different sources
p. 14
Table 1.3 Distribution of Aeromonas in water sourcesfrom different locations
p. 26
Table 1.4 Enumeration of Aeromonas in different foodstuffs
p. 29
Table 1.5 Characteristics of pili described in Aeromonas species
p. 37
Table 1.6 Selected effector proteins associated with different secretion systems
p. 47
Table 1.7 Toxins secreted by Aeromonas p. 57
Table 1.8 Clinical characteristics of patients with HUS-associated Aeromonas
p. 70
Table 1.9 Major categories of Aeromonas septicaemia disease presentation
p. 75
Table 1.10 -lactamases produced by Aeromonas species p. 84
Table 1.11 ESBL-producing Aeromonas species p. 87
Table 2.1 Chemicals and reagents used in this project p. 97
Table 2.2 Bacteriological media used in this project p. 99
Table 2.3 Antimicrobial agents used in this project p. 101
Table 2.4 Type and reference strains used in this project p. 102
Table 2.5 Type strains used as positive and negative controls p. 105
Table 2.6 Clinical strains used in this project p. 106
Table 2.7 Environmental strains used in this project p. 109
Table 2.8 Primers used in this project p. 111
Table 2.9 Aeromonas strains used in virulence studies p. 113
Table 2.10 Interpretation of disk diffusion results p. 134
Table 2.11 Interpretation of E-strip MIC values p. 135
Table 3.1 Biochemical characteristics of type and reference Aeromonas strains
p. 139
Table 3.2 Biochemical characteristics of Aeromonas isolated from human clinical material
p. 145
Table 3.3 Biochemical characteristics of Aeromonas isolated from environmental sources
p. 149
Table 3.4 Distribution of Aeromonas spp. among clinical and p. 153
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environmental samples after phenotypic characterization
Table 4.1 Type and reference strains GenBank accession numbers p. 160
Table 4.2 GenBank accession numbers of wild strains for rpoD and gyrB gene sequences
p. 162
Table 4.3 Distribution of Aeromonas spp. among clinical and environmental samples following genotypic characterization
p. 173
Table 4.4 Biochemical characteristics of Aeromonas after genotypic identification
p. 175
Table 4.5 Evolutionary distances based on the percentage sequence dissimilarities of all current Aeromonas spp. and 60 isolates identified as A. aquariorum using Clustal_W and Mega 5 software
CD-ROM
Table 5.1 Antimicrobial susceptibilities determined for different Aeromonas spp.
p. 182
Table 5.2 Antibiotic susceptibilities of Aeromonas spp. by source of isolation
p. 184
Table 6.1 Key tests for the phenotypic identification of strain 266T
from other Aeromonas spp.
p. 192
Table 6.2 Key tests used to differentiate strain 266T from other D-mannitol non-fermentative Aeromonas
p. 197
Table 6.3 Cellular fatty acid profiles of strain 266T and current Aeromonas spp.
p. 198
Table 6.4 Evolutionary distances based on the percentage sequence dissimilarities of current Aeromonas and strain 266T using Clustal_W and Mega 4 software
CD-ROM
Table 6.5 DNA-DNA hybridization values between strain 266T and closely related Aeromonas spp.
p. 204
Table 7.1 Distribution of virulence genes among Western Australian Aeromonas species
p. 221
Table 7.2 Distribution of virulence genes in Aeromonas spp. isolated from stools
p. 223
Table 7.3 Distribution of virulence genes in Aeromonas spp. isolated from blood
p. 225
Table 7.4 Distribution of virulence genes in Aeromonas spp. isolated from wounds
p. 227
Table 7.5 Distribution of virulence genes in Aeromonas spp. isolated p. 230
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from miscellaneous specimens
Table 7.6 Distribution of virulence genes in Aeromonas spp. isolated from environmental sources
p. 232
Table 7.7 Additional features p. 234
Table 7.8 Percentage identity of gene product sequences from this study compared with sequences deposited in GenBank
p. 235
Table 7.9 Accession numbers of sequences derived from virulence genes and deposited in GenBank
p. 237
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LIST OF FIGURES
Figure 1.1 Unrooted neighbour-joining phylogenetic tree derived from gyrB sequences showing subspecies and biovars
p. 7
Figure 1.2 Unrooted neighbour-joining phylogenetic tree derived from gyrB sequences showing current Aeromonas species
p. 10
Figure 1.3 Unrooted neighbour-joining phylogenetic tree derived from rpoD sequences showing current Aeromonas species
p. 11
Figure 4.1 Concatenated neighbour-joining phylogenetic tree showing the position of A. dhakensis strains derived from the rpoD and gyrB sequences
p. 169
Figure 4.2 Concatenated neighbour-joining phylogenetic tree showing the position of A. caviae strains derived from the rpoD and gyrB genes sequences
p. 170
Figure 4.3 Concatenated neighbour-joining phylogenetic tree showing the position of A. hydrophila strains derived from the rpoD and gyrB genes sequences
p. 171
Figure 4.4 Concatenated neighbour-joining phylogenetic tree derived from the rpoD and gyrB genes sequences showing the position of A. veronii bv. sobria and other species including strain 266
p. 172
Figure 6.1 Electron microscopy images of strain 266T p. 191
Figure 6.2 Protein spectrum of strain 266T p. 203
Figure 6.3 Unrooted neighbour-joining phylogenetic tree derived from the 16S rRNA gene sequences showing the relationships of strain 266T with all other Aeromonas species
p. 205
Figure 6.4 Unrooted neighbour-joining phylogenetic tree derived from dnaJ sequences showing the relationships of strain 266T with the type strains of all other Aeromonas species
p. 206
Figure 6.5 Unrooted neighbour-joining phylogenetic tree derived from dnaX sequences showing the relationships of strain 266T with the type strains of all other Aeromonas species
p. 207
Figure 6.6 Unrooted neighbour-joining phylogenetic tree derived from gyrA sequences showing the relationships of strain 266T with the type strains of all other Aeromonas species
p. 208
Figure 6.7 Unrooted neighbour-joining phylogenetic tree derived from gyrB sequences showing the relationships of strain 266T with the type strains of all other Aeromonas species
p. 209
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Figure 6.8 Unrooted neighbour-joining phylogenetic tree derived from recA sequences showing the relationships of strain 266T with the type strains of all other Aeromonas species
p. 210
Figure 6.9 Unrooted neighbour-joining phylogenetic tree derived from rpoD sequences showing the relationships of strain 266T with the type strains of all other Aeromonas species
p. 211
Figure 6.10 Unrooted neighbour-joining phylogenetic tree derived from the MLPA of concatenated sequences of six housekeeping genes sequences showing the relationships of strain 266T with several strains of all other Aeromonas species
p. 212
-- 1 --
CHAPTER 1: LITERATURE REVIEW
1.1. GENERAL INTRODUCTION
Aeromonas species are authoctonous inhabitants of aquatic environments that can be
frequently isolated from human clinical material, environmental and food sources
(Janda and Abbott 2010). Infections due to Aeromonas occur in amphibians, reptiles
and snails, where the latter infections are a significant problem for the snail industry in
France (Kodjo et al. 1997). In humans, aeromonads have been associated with serious
infections in both immunocompromised and healthy individuals while infections in fish
represent a serious threat to the aquaculture industry resulting in significant financial
loss.
Once considered organisms of doubtful clinical significance the interest in Aeromonas
has grown considerably over the past three decades as reflected by a sixfold increase in
research publications (Janda and Abbott 2010). In the tsunami that devastated parts of
Asia in 2004 Aeromonas species were the predominant (22.6%) Gram-negative isolated
from wounds of victims (Hiransuthikul et al. 2005). This led to the recommendation
that assessment of wound infections in tsunami survivors, empirical antimicrobial
therapy should always include agents with activity against Aeromonas (Lim 2005).
Similarly, Aeromonas was present in high concentration in water samples following the
hurricane Katrina disaster that affected New Orleans (Presley et al. 2006). This review
discusses current taxonomic classification and identification methods. Secondly,
description of putative virulence factors and their association with Aeromonas
infections is examined. Finally, the response of Aeromonas to antimicrobial agents is
reviewed.
1.2. HISTORY
Infections due to Aeromonas species have been described for more than a hundred years
and several reviews have credited the first reports to the work of Zimmerman and
Sanarelli in the late 1880s (Abeyta et al. 1988; Altwegg and Geiss 1989; Joseph and
Carnahan 1994). These cases were followed by other reports of Aeromonas-like bacteria
including the water-borne bacterium, Bacillus hydrophilus, isolated from water and
diseased frogs (Chester 1901) and Proteus melanovogenes implicated as the cause of
black rot in eggs and also isolated from human faeces (Miles and Halnan 1937).
-- 2 --
According to Joseph and Carnahan (1994), the first report of human infection caused by
aeromonads was by Hill et al. (1954) who described a case of fulminant septicaemia
and metastatic myositis caused by an unknown bacterium. The microorganism that was
recovered from multiple organs and in pure form from cerebral spinal fluid was
considered an undescribed member of the family Pseudomonadaceae, tribe Spirilleae
and genus Vibrio.
The genus Aeromonas was first proposed by Kluyver and van Niel (1936) who
recommended that the species Acetobacter liquefaciens be renamed Aeromonas
liquefaciens, then the only species and type species of the genus. The newly proposed
genus was formally accepted in the seventh edition of Bergey’s Manual of
Determinative Bacteriology (Snieszko 1957). The type species of the genus, A.
hydrophila, was later proposed by Stanier (1943) based on the phenotypic
characteristics of Proteus hydrophilus, a fermentative, polar flagellated bacterium. Since
their discovery, Aeromonas or Aeromonas-like bacteria have been assigned to several
genera including Aerobacter, Bacillus, Pseudomonas, Proteus and Vibrio (Joseph and
Carnahan 1994).
1.3. TAXONOMY
Due to the heterogeneous nature of the genus the taxonomy of Aeromonas has been
considered complex and confusing (Schubert 1974; Popoff and Veron 1976; Joseph and
Carnahan 1994; Wahli et al. 2005). The inability to separate genospecies using
biochemical methods (Altwegg et al. 1990) and the poor correlation that existed
between genotypic and phenotypic methods (Austin et al. 1998; Martínez-Murcia et al.
2000) led to an unstable nomenclature (Popoff and Veron 1976; Abbot et al. 1992; Vila
et al. 2002; Ørmen et al. 2005) resulting in conflicting data (de la Morena et al. 1993;
Huys et al. 1997a; Valera and Esteve 2002; Huys et al. 2005).
1.3.1. Early taxonomy
Prior to the 1980s, classification of Aeromonas was based solely on differential
phenotypic characteristics such as growth temperature and motility (Popoff and Veron
1976). Thus, Aeromonas was classified into two major groups: a large group that
comprised the motile, mesophilic and heterogenous species that also included potential
human pathogens; and a second smaller group of homogenous species represented by A.
salmonicida, a non-motile, psychrophilic species primarily considered fish pathogens
-- 3 --
(McNicol et al. 1980; Janda et al. 1984; Kasai et al. 1998; Pidiyar et al. 2002; Martin-
Carnahan and Joseph 2005).
In 1981, Popoff and colleagues used DNA-DNA hybridization (DDH) to classify 55
motile aeromonads. Results revealed that A. hydrophila, A. caviae and A. sobria were
well differentiated but each species contained more than one hybridization group (HG),
a term used to refer to DNA groups that could not be differentiated phenotypically. As a
consequence, investigators began to use DDH values to determine hybridization groups
(HGs), which were defined as having at least 70% DNA homology with the designated
type strain (Wayne et al. 1987). The use of the term “hybridization group” dropped out
of use over the last decade. The last hybridization group was DNA HG 18 assigned to
A. culicicola (Pidiyar et al. 2002). Instead, the term “genomic species” or “genospecies”
followed by a reference number has been recommended to describe unnamed groups
(Janda and Abbott 2010).
1.3.2. Current taxonomy
The genus Aeromonas resides in the family Aeromonadaceae (Colwell et al. 1986)
within the subclass Gammaproteobacteria (Saavedra et al. 2007). There are currently
27 recognized species and six subspecies (Table 1.1), and two biovars (Fig. 1.1). The
complete genome of all type strains representing all species and selected reference
strains have now been sequenced (Seshadri et al. 2006; Colston et al. 2014).
In recent years, the classification of Aeromonas has been based on the nucleotide
sequences of housekeeping genes which have the ability to reliably discriminate
between all species in the genus (Yañez et al. 2003; Soler et al. 2004; Thompson et al.
2004; Nhung et al. 2007; Adekambi et al. 2008; Miñana-Galbis et al. 2009). As a
consequence, 15 new Aeromonas species have been described since 2000, with the
majority recovered from environmental sources.
1.3.3. Controversial taxonomic issues
Controversial taxonomic issues discussed in previous reviews (Janda and Abbott 2010)
can now be considered partly or completely resolved. Extensive genotypic and
phenotypic evidence confirmed that: A. trota was identical to A. enteropelogenes
(Schubert et al. 1990a; Carnahan et al. 1991a; Carnahan 1993; Collins et al. 1993; Huys
et al. 1996b; 2002b) and A. ichthiosmia should be considered a junior synonym of A.
-- 4 --
veronii (Fanning et al. 1985; Schubert et al. 1990b; Collins et al. 1993; Huys et al.
1996a; 2001). The unnamed Aeromonas group 501 (Hickman-Brenner et al. 1988) has
been reclassified as A. diversa sp. nov. (Miñana-Galbis et al. 2010) and A. hydrophila
ssp. anaerogenes has been included in the species A. caviae (Miñana-Galbis et al.
2013).
Phylogenetic evidence indicated that strains of A. hydrophila ssp. dhakensis belonged to
the species A. aquariorum (Martínez-Murcia et al. 2008; 2009). Previously, the species
A. hydrophila consisted of three subspecies including ssp. hydrophila and ssp. ranae
(Huys et al. 2003). Recently, Beaz-Hidalgo et al. (2013) combined A. hydrophila ssp.
dhakensis (Huys et al. 2002a) and A. aquariorum (Martínez-Murcia et al. 2008) and
proposed the creation of A. dhakensis sp. nov. comb. nov. Due to inconsistent genotypic
and phenotypic feature, “A. sharmana” (Saha and Chakrabarti 2006) has not been
included in the genus (Martínez-Murcia et al. 2007; Lamy et al. 2010).
1.3.3.1. Aeromonas allosaccharophila
This species was proposed by Martínez-Murcia et al. (1992a) based on two strains
recovered from diseased elvers (Anguilla anguilla) and one from human stools.
Evidence against A. allosaccharophila representing a separate species derived from
discrepancies reported in the biochemical profiles of the original strains (Martínez-
Murcia et al. 1992a; Esteve et al. 1995b; Huys et al. 1996a; 2001); amplified fragment
length polymorphism (AFLP) and fluorescent amplified fragment length polymorphism
(FAFLP) patterns identical to those of A. veronii (Huys et al. 1996b; Huys and Swings
1999); the nucleotide sequences of several housekeeping genes showed A.
allosaccharophila in close proximity to A. veronii and not sufficiently distant to
confidently separate the two species (Nhung et al. 2007; Miñana-Galbis et al. 2009;
Lamy et al. 2010). Evidence supporting A. allosaccharophila as a separate species
derived from i) its unique 16S rDNA sequence composition that clearly differentiated
this species from most other members of the genus including A. veronii (Martínez-
Murcia et al. 1992a); ii) the nucleotide sequences of the rpoD and gyrB housekeeping
genes (Yañez et al. 2003; Soler et al. 2004; Saavedra et al. 2006) (Figs. 1.2 and 1.3); iii)
multilocus sequence analysis showed that A. allosaccharophila and A. veronii were
-- 5
--
Tab
le 1
.1
Cur
rent
Aer
omon
as sp
ecie
s
Spec
ies
HG
So
urce
of t
ype
stra
in
Ref
eren
ce
A. h
ydro
phila
ssp.
hyd
roph
ila
1 Ti
n of
milk
with
fish
y od
our
Stan
ier (
1943
)
A. sa
lmon
icid
a ss
p. a
chro
mog
enes
3
Fish
(Sal
mo
trut
ta)
Smith
(196
3)
A. sa
lmon
icid
a ss
p. sa
lmon
icid
a
Salm
on (S
alm
o sa
lar)
Sc
hube
rt (1
967b
)
A. sa
lmon
icid
a ss
p. m
asou
cida
Fish
blo
od (O
ncor
hync
hus m
asou
) K
imur
a (1
969)
A. so
bria
7
Fish
Po
poff
and
Ver
on (1
976)
A. m
edia
5
Riv
er w
ater
A
llen
et a
l. (1
983)
A. c
avia
e 4
Gui
nea-
pig
Popo
ff (1
984)
A. v
eron
ii
8/10
Fr
og re
d le
g/sp
utum
H
ickm
an-B
renn
er e
t al.
(198
7)
Aero
mon
as ss
p.
11
Ank
le su
ture
H
ickm
an-B
renn
er e
t al.
(198
7)
A. sc
hube
rtii
12
Fore
head
abs
cess
H
ickm
an-B
renn
er e
t al.
(198
8)
A. e
ucre
noph
ila
6 C
arp
Schu
bert
and
Heg
azi (
1988
)
A. sa
lmon
icid
a ss
p. sm
ithia
Fish
A
ustin
et a
l. (1
989)
A. tr
ota
14
Hum
an fa
eces
C
arna
han
et a
l. (1
991a
)
A. ja
ndae
i 9
Faec
es
Car
naha
n et
al.
(199
1c)
A. a
llosa
ccha
roph
ila
15
Dis
ease
d el
vers
/hum
an fa
eces
M
artín
ez-M
urci
a et
al.
(199
2a)
A. e
nche
leia
16
Eu
rope
an e
els
Este
ve e
t al.
(199
5a)
A. b
estia
rum
2
Infe
cted
fish
A
li et
al.
(199
6)
-- 6
--
Tab
le 1
.1
Con
tinue
d.
Spec
ies
HG
So
urce
of t
ype
stra
in
Ref
eren
ce
A. p
opof
fii
17
Drin
king
wat
er p
rodu
ctio
n pl
ant
Huy
s et a
l. (1
997b
)
A. sa
lmon
icid
a ss
p. p
ectin
olyt
ica
W
ater
from
cis
tern
Pa
van
et a
l. (2
000)
A. h
ydro
phila
ssp.
rana
e
Farm
ed fr
og
Huy
s et a
l. (2
003)
A. si
mia
e
Mon
key
faec
es
Har
f-M
onte
il et
al.
(200
4)
A. m
ollu
scor
um
W
edge
-she
lls (D
onax
trun
culu
s)
Miñ
ana-
Gal
bis e
t al.
(200
4a)
A. b
ival
vium
Coc
kles
(Car
dium
spp.
) M
iñan
a-G
albi
s et a
l. (2
007)
A. te
cta
St
ool o
f a c
hild
with
dia
rrho
ea
Dem
arta
et a
l. (2
008)
A. p
isci
cola
Dis
ease
d fis
h B
eaz-
Hid
algo
et a
l. (2
009)
A. fl
uvia
lis
R
iver
wat
er
Alp
eri e
t al.
(201
0a)
A. d
iver
saa
13
Hum
an le
g w
ound
M
iñan
a-G
albi
s et a
l. (2
010)
A. sa
nare
llii
H
uman
wou
nd
Alp
eri e
t al.
(201
0b)
A. ta
iwan
enes
is
B
urn
wou
nd
Alp
eri e
t al.
(201
0b)
A. ri
vuli
Fr
eshw
ater
Fi
guer
as e
t al.
(201
1a)
A. a
ustr
alie
nsis
Trea
ted
efflu
ent w
ater
A
rave
na-R
omán
et a
l. (2
013)
A. d
hake
nsis
b
Chi
ldre
n w
ith d
iarr
hoea
B
eaz-
Hid
algo
et a
l. (2
013)
A. c
aver
nico
la
Is
olat
ed fr
om w
ater
bro
ok
Mar
tínez
-Mur
cia
et a
l. (2
013)
a p
revi
ousl
y cl
assi
fied
as A
erom
onas
gro
up 5
01 (H
ickm
an-B
renn
er e
t al.
1988
); b co
mbi
ned
from
A. h
ydro
phila
ssp.
dha
kens
is (H
uys e
t al.
2002
a) a
nd A
. aqu
ario
rum
(Mar
tínez
-Mur
cia
et a
l. 20
08)
-7-
Figure 1.1 Unrooted neighbour-joining phylogenetic tree derived from gyrB nucleotide
sequences showing subspecies and biovars. The phylogenetic tree was constructed with
530 nt. Numbers at the nodes indicate bootstrap values. Bar, 0.005 estimated
substitutions per site.
A. salmonicida spp. salmonicida (CECT 894T)
A. salmonicida ssp. smithia (CIP 104757)
A. salmonicida spp. masoucida (CECT 896)
A. salmonicida spp. pectinolytica (34mel)
A. salmonicida ssp. achromogenes (CECT 895)
A. veronii bv. sobria (ATCC 9071)
A. veronii bv. veronii (DSM 7386T)
A. hydrophila spp. dhakensis (LMG 19562T)
A. hydrophila ssp. hydrophila (ATCC 7966T)
A. hydrophila spp. ranae (LMG 19707T)
97
84
100
0.005
-8-
located in different phylogenetic lines and exhibited a high degree of nucleotide
diversity (Martino et al. 2011).
1.3.3.2. Aeromonas spp. HG 11
This unnamed Aeromonas derived from two strains that could not be included in the
original description of A. veronii (Hickman-Brenner et al. 1987). Evidence that
supported the inclusion of Aeromonas HG11 into A. encheleia was based on AFLP
(Huys et al. 1996b) and 16S-23S rDNA-RFLP patterns (Laganowska and Kaznowski
2004); high DDH values (84-87%) between Aeromonas HG11 strains and the type
strain of A. encheleia LMG 16330T (Huys et al. 1997a); and divergent values for gyrB
(2.1-2.2%), rpoD (1.4-1.7%), dnaJ (1.3%), cpn60UT (0.7%) and rpoB (0.9%) (Yañez et
al. 2003; Soler et al. 2004; Nhung et al. 2007; Miñana-Galbis et al. 2009; Lamy et al.
2010). In contrast, phenotypic profiles (Valera and Esteve 2002) and different tRNA
patterns suggested that these two species represent distinct taxa (Laganowska and
Kaznowski 2005). Moreover, the 16S rRNA sequence of A. encheleia and Aeromonas
sp. HG11 differed by eight nucleotides at hypervariable positions 457 to 476 (Martínez-
Murcia 1999), a significant feature considering that in Aeromonas the 16S rRNA gene
similarities range from 96.9 to 100% (Martínez-Murcia 1992a).
1.3.3.3. Aeromonas culicicola
This species originated from strains isolated from the midgut of the mosquito species
Culex quinquefasciatus and Aedes aegyptii (Pidiyar et al. 2002). Evidence that A.
culicicola represents a heterotypic synonym of A. veronii derived from the low
interspecies nucleotide substitution rates for several housekeeping genes (Soler et al.
2004; Nhung et al. 2007; Miñana-Galbis et al. 2009; Lamy et al. 2010); similar
phenotypic and cellular fatty acid profiles (Huys et al. 2005); DDH values well above
70% between A. culicicola MTCC 3249T and A. veronii ATCC 35624T (Huys et al.
2005; Nhung et al. 2007) compared to 44% by the initial report (Pidiyar et al. 2002);
16S rRNA RFLP profiles similar to those of A. veronii (Lamy et al. 2010). In contrast,
16S DNA-RFLP patterns reported by two studies showed that A. culicicola differed
sufficiently from all other members of the genus (Figueras et al. 2005; Kaznowski and
Konecka 2005). Moreover, gyrB gene sequence placed A. culicicola in a separate line of
descent where it differed from A. jandaei by 56 nucleotides (Yañez et al. 2003)
compared to a single nucleotide difference using 16S rDNA (Pidiyar et al. 2003).
-9-
1.4. LABORATORY IDENTIFICATION
Aeromonas species are non-fastidious, catalase and oxidase positive, facultatively
anaerobic Gram-negative fermentative bacilli (Janda 1985). The majority of the species
produce -haemolysis on horse and sheep blood agar and most can produce indole from
tryptophan. Although the optimal temperature for growth is 28C, aeromonads can grow
at temperatures ranging from 1 to 42C (Mateos et al. 1993; Hänninen et al. 1995c) and
can adapt and survive in highly acidic (pH 3.5) environments (Karem et al. 1994).
Traditionally, susceptibility to the vibriostatic agent 2, 4-diamino-6, 7-
diisopropylpteridine (O/129; 150 g disk) and the inability of aeromonads to grow on
thiosulfate citrate bile salts sucrose agar (TCBS) and on 6% NaCl have been used as
preliminary tests to differentiate Aeromonas from closely related Vibrios and
Plesiomonas species. In general, the close phenotypic similarity of aeromonads and
poorly equipped laboratories hampers the identification of aeromonads to species level.
Thus, small laboratories should confine identification to the genus level and significant
clinical or environmental strains should be sent to reference centres for further work
(Abbott et al. 1992).
1.4.1. Isolation
Aeromonas species can grow on most solid media including MacConkey, Hektoen
enteric and xylose lysine desoxycholate (XLDA) agars, although colony size and
plating efficiency differences have been observed (Desmond and Janda 1986; Janda and
Abbott 1999). Plating efficiency appeared to be strain rather than species dependent
(Desmond and Janda 1986). The concentration of salt is critical since Aeromonas do not
usually grow in media containing greater than 3% NaCl (Abbott et al. 2003).
Occasionally, strains of A. trota have been reported to withstand concentrations close to
4% (0.68 M) NaCl (Delamare et al. 2000). An optimal Aeromonas-medium should
contain substrates that do not interfere with the oxidase test (Moulsdale 1983) or include
lactose in its composition as this carbohydrate is highly unsatisfactory for primary
isolation (Millership et al. 1983). The number of Aeromonas species recovered from
different samples has been attributed to variations in technique and media employed to
isolate these organisms (Nazer et al. 1986). A variety of media or variations of well-
established formulae have been developed to isolate and quantify aeromonads from
food, water and human faecal specimens based on biological properties such as
production of amylase and starch activity or the natural tolerance of the majority of
these organisms to ampicillin (Table 1.2).
-10-
Figure 1.2 Unrooted neighbour-joining phylogenetic tree derived from gyrB sequences
showing current Aeromonas species. The phylogenetic tree was constructed with 530 nt.
Numbers at the nodes indicate bootstrap values. Bar, 0.01 estimated substitutions per
site.
A. popoffii (CIP 105493T)
A. bestiarum (ATCC 51108T)
A. piscicola (CECT 7443T)
A. salmonicida (CECT 894T)
A. molluscorum (DSM 17090T)
A. eucrenophila (ATCC 23309T)
A. encheleia (DSM 11577T)
A. tecta (CECT 7083T)
A. rivuli (CECT 7518T)
A. caviae (ATCC 23212)
A. media (ATCC 33907T)
A. bivalvium (CECT 7113T)
A. sanarellii (CECT 7402T)
A. cavernicola (CECT 7862T)
A. dhakensis (LMG 19562T)
A. hydrophila (ATCC 7966T)
A. jandaei (CECT 4228T)
A. fluvialis (CECT 7401T)
A. sobria (CIP 7433T)
A. veronii (ATCC 9071)
A. australiensis (CECT 8023T)
A. allosaccharophila (DSM 11576T)
A. trota (ATCC 49657T)
A. taiwanensis (CECT 7403T)
A. simiae (DSM 16559T)
A. schubertii (ATCC 43700T)
A. diversa (CECT 4254T) 100
99
96
90
85
79
73
0.01
-11-
Figure 1.3 Unrooted neighbour-joining phylogenetic tree derived from rpoD sequences
showing all Aeromonas species. The phylogenetic tree was constructed with 653 nt.
Numbers at the nodes indicate bootstrap values. Bar, 0.02 estimated substitutions per
site.
A. taiwanensis (CECT 7403T)
A. sanarellii (CECT 7402T)
A. caviae (ATCC 13136T)
A. dhakensis (LMG 7862T)
A. hydrophila (ATCC 7966T)
A. eucrenophila (ATCC 23309T)
A. tecta (CECT 7082T)
A. media (ATCC 33907T)
A. encheleia (DSM 11577T)
A. diversa (CECT 4254T)
A. simiae (DSM 16559T)
A. schubertii (CECT 4240T)
A. bivalvium (CECT 7113T)
A. molluscorum (DSM 17090T)
A. rivuli (CECT 7518T)
A. jandaei (ATCC 49568T)
A. trota (ATCC 49657T)
A. australiensis (CECT 8023T)
A. fluvialis (CECT 7401T)
A. veronii (ATCC 9071)
A. allosaccharophila (DSM 11576T)
A. sobria (CIP 7433T)
A. cavernicola (CECT 7862T)
A. salmonicida (CECT 894T)
A. popoffii (CIP 105493T)
A. bestiarum (ATCC 51108T)
A. piscicola (CECT 7443T)
100
100
100
98
92
99
90
97
93
86
93
93
0.02
-12-
Huddleston et al. (2007) recommended that ampicillin should not be used as a selective
agent in isolation medium for Aeromonas when a complete analysis of Aeromonas
diversity and density is desired. These authors argued that media containing ampicillin
was likely to inhibit the growth of ampicillin-susceptible strains resulting in an
underestimation of densities and species diversity.
1.4.2. Identification by phenotypic methods
Identification of Aeromonas by phenotypic methods has been based on the ability of
these bacteria to ferment carbohydrates with vigorous gas production (Kluyver and van
Neil 1936; Stanier 1943; Schubert 1968). However, identification based on biochemical
tests is often unable to accurately identify Aeromonas beyond genus level as phenotypic
features are unstable and vary within the species (Davin-Regli et al. 1998; Martínez-
Murcia et al. 2000; Figueras et al. 2005; Wahli et al. 2005). Moreover, biochemical
analyses depend on the transcription and translation of proteins which in turn are
influenced by environmental factors such as temperature or carbohydrate repression
potentially affecting production of proteins (Knochel 1989; 1990).
Phenotypic identification is also influenced by the number and type of tests and testing
conditions (Valera and Esteve 2002; Esteve et al. 2003; Demarta et al. 2004),
geographical source (Kaznowski et al. 1989) and interpretation of data and
reproducibility of results (Abbott et al. 2003; Ørmen et al. 2005). Inaccurate
identification is further compromised by those species in which only a handful of strains
have been described (Abbott et al. 1992), by the application of schemes designed to
identify clinical isolates to classify strains isolated from environmental and fish sources
(Wakabayashi et al. 1981; Kaznowski et al. 1989; Ashbolt et al. 1995; Borrell et al.
1998; Ørmen et al. 2005). Furthermore, many of the biochemical schemes used in
clinical laboratories predate the description of new taxa leading some authors to
question whether the efficiency of older biochemical schemes are suitable to identify
more recently described species (Edberg et al. 2007).
An identification scheme, the Aerokey II (Carnahan et al. 1991b; Joseph and Carnahan
1994) based on a small subset of highly discriminatory biochemical tests and the
AeroMat-1/AsalMat-1 designed exclusively for the identification of A. salmonicida to
species and subspecies levels, respectively, were developed (Higgins et al. 2007).
-13-
However, Aerokey II has not been generally adopted by laboratories due to the
inconsistent biochemical profiles expressed by some species, costs and long incubation
times required (Abbott et al. 1992; Janda and Abbott 1998). Furthermore, Aerokey II
may be unsuitable for those regions harbouring strains with unique phenotypic profiles
or due to the heterogeneous character of some species (Altwegg et al. 1990) while a
lack of congruence between Aerokey II and genotypic identification has been reported
(Noterdaeme et al. 1996).
Other potential identifying markers proposed to differentiate Aeromonas species
included susceptibility to cephalexin (Janda and Motyl 1985), induced colistin
resistance (Fosse et al. 2003b), production of a CAMP-like factor (Figura and
Guglielmetti 1987) and maximum growth temperature determined with a temperature-
gradient incubator (Havelaar et al. 1992; Hӓnninen 1994). The production of acetic acid
in glucose-containing media is a peculiar characteristic displayed by certain species
whereby some aeromonads become unviable (“the suicide phenomenon”). This test was
designed as an identification marker to separate A. caviae (Namdari and Cabelli 1989).
1.4.3. Identification by commercial systems
A plethora of commercial systems such as Vitek, API, MicroScan Walk/Away, BBL
Crystal Enteric/Non-fermenter, Biolog and the Phoenix 100 ID/AST contain selected
Aeromonas species in their databases (Hӓnninen 1994; Park et al. 2003; Soler et al.
2003b; Huddleston et al. 2006; O’Hara 2006). Unfortunately, identification of
Aeromonas by these systems is inadequate resulting in major errors (Janda and Abbott
2010). Among the major identification problems encountered with these systems are:
misidentification of Aeromonas species as V. cholerae and V. damsela (Abbott et al.
1998), partly attributed to the lower salt concentration (0.45% NaCl) recommended by
the manufacturer in the preparation of the inoculum in the Vitek identification system
(Park et al. 2003); production of acid by the API 20E is temperature-dependent
resulting in false-negative results if the strip is incubated at 37C (Hӓnninen 1994); the
percentage of correct identifications for MicroScan Walk/Away (14.5%) and BBL
Crystal Enteric/Non-fermenter (20.3%) systems is low (Soler et al. 2003b) while the
Phoenix 100 ID/AST identified only 60% of Aeromonas (O’Hara 2006).
-14-
Tab
le 1
.2
Exam
ples
of m
edia
use
d in
the
isol
atio
n of
Aer
omon
as fr
om d
iffer
ent s
ourc
es
Med
ia
So
urce
/pur
pose
R
efer
ence
Glu
tam
ate
star
ch p
heno
l (G
SP);
Red
aga
r (Ps
eudo
mon
as-
Aero
mon
as-s
elec
tive
agar
) Fo
ods o
f ani
mal
or
igin
/env
ironm
enta
l sou
rces
U
llman
et a
l. (2
005)
; Yuc
el a
nd
Erdo
gan
(201
0)
Blo
od a
mpi
cilli
n ag
ar (B
AA
); O
xoid
Aer
omon
as a
gar;
Star
ch
amip
icill
in a
gar (
SAA
) Se
afoo
d R
obin
son
et a
l. (1
984)
; Pal
umbo
et
al. (
1985
); Pi
n et
al.
(199
4); T
sai
and
Che
n (1
996)
B
lood
aga
r con
tain
ing
p-ni
troph
enol
gly
cerin
e Fa
ecal
sam
ples
B
urke
et a
l. (1
983)
; Rob
inso
n et
al.
(198
6)
Car
y-B
lair
med
ium
Tr
ansp
ort m
ediu
m
Moy
er (1
987)
Difc
o Ae
rom
onas
aga
r (D
AA
); am
pici
llin
bloo
d ag
ar (A
BA
); xy
lose
des
oxyc
hola
te c
itrat
e ag
ar (X
DC
A) a
nd a
lkal
ine
pept
one
wat
er (A
PW)
Chi
ldre
n st
ools
/ car
riage
rate
W
ilcox
et a
l. (1
992)
Am
pici
llin-
Dex
trin
Aga
r (A
DA
) R
aw, p
roce
ssed
and
read
y-to
-ea
t foo
ds sa
mpl
es
Kin
gom
e et
al.
(200
4)
XD
CA
, DN
A to
luid
ine
agar
(DN
AT)
; Sal
mon
ella
-Shi
gella
so
dium
des
oxyc
hola
te (S
SSD
) aga
r Fa
ecal
car
riage
rate
M
iller
ship
et a
l. (1
983)
; von
G
raev
enitz
and
Zin
terh
ofer
(197
0);
Wau
ters
(197
3); F
igur
a (1
985)
in
osito
l-bile
-sal
ts-b
rillia
nt g
reen
(IB
B) a
nd c
efsu
lodi
n-irg
asan
-no
vobi
ocin
aga
r (C
IN);
BA
A
Fa
ecal
/abi
lity
to g
row
on
thes
e m
edia
A
ltorf
er e
t al.
(198
5); M
oyer
et a
l. (1
991)
-15-
1.4.4. Additional phenotypic methods
Many non-biochemical methods have been employed as alternatives to biochemical
identification for typing or identification purposes, or both. Some, such as the use of
core oligosaccharides from the endotoxins have not been readily adopted as routine
identification methods (Shaw and Hodder 1978). Isoenzyme analysis has been used as
both a screening method to investigate the epidemiology of hospital infections and as an
identification tool (Picard and Goullet 1987; Altwegg et al. 1988). Multi-loccus enzyme
electrophoresis (MLEE) has been considered useful as a sole method for species
identification and shows good correlation with taxonomic groupings as determined by
DDH (Altwegg et al. 1991c; Miñana-Galbis et al. 2004b). In contrast, phage typing,
although specific to the genus Aeromonas, may be over-sensitive (Altwegg et al. 1988).
The use of outer membrane protein (OMP) composition as a typing method is
cumbersome and time consuming and OMP profiles are influenced by temperature and
the air-supply available to the bacterial cultures (Küijper et al. 1989a). Methods such as
radiolabelled cell proteins (radioPAGE) profiles are difficult to interpret and prone to
subjective bias (Stephenson et al. 1987) while conflicting data have been reported with
whole-protein fingerprinting (Millership and Want 1993; Alavandi et al. 2001; Szczuka
and Kaznowski 2007).
1.4.5. Semiautomated systems
Two semi-automated systems based on the analysis of cellular fatty acid methyl esters
by gas-liquid chromatography (GLC-FAMEs) and by measuring the differences in
protein mass generated by the matrix-assisted laser-desorption/ionization mass
spectrometry time-of flight (MALDI-MS-TOF) are widely used in identification of
Aeromonas. Both methods are expensive and in the case of GLC-FAME require highly
trained personnel. The systems can be used for the rapid identification of bacteria
(Rahman et al. 2002) or as a typing tool (Osterhout et al. 1991; von Graevenitz et al.
1991; Huys et al. 1994, 1995; Donohue et al. 2006, 2007).
The reproducibility of the GLC-FAMEs system depends greatly on media, temperature
of incubation, sets of strains, GC model used to analyse cellular fatty acid patterns and
previous exposure to antibiotics (Canonica and Pisano 1988; Huys et al. 1994;
Kӓempfer et al. 1994). A high identification rate of Aeromonas to species level has been
reported by MALDI-TOF users making this system the most accurate for identification
-16-
of these bacteria (Lamy et al. 2011). For those laboratories that can afford it, the
MALDI-TOF has largely superseded most automated identification systems. Although
the instrument is expensive, consumables and operational costs are lower than those
incurred by the MIDI system, the most commonly used system used to detect FAME. It
also requires less laboratory space than the MIDI system.
1.4.6. Identification by molecular methods
Practically every known molecular technique, each with its own strengths and
weaknesess, has been used in the classification and typing of aeromonads since Popoff
et al. (1981) placed them into DNA hybridization groups. In Aeromonas, the use of a
single typing method to determine interrelationship between species may not be
adequate as the potential for discrimination increases by combining different molecular
methods (Altwegg et al. 1988; Davin-Regli et al. 1998; Soler et al. 2003a; Morandi et
al. 2005). The application of these methods has been useful in establishing the
epidemiological relationships between aeromonads recovered from very different
sources (Villari et al. 2003). However, a situation similar to phenotypic identification
exists where a lack of congruence between different molecular methods has been
recognized (Hӓnninen and Siitonen 1995; Graf 1999a; Martínez-Murcia 1999; Figueras
et al. 2000b; Yañez et al. 2003; Laganowska and Kasnowski 2005; Saavedra et al.
2006). Methods employed in the characterization and typing of aeromonads included
those based on restriction enzymes used to digest genomic DNA [ribotyping, amplified
fragment length polymorphism (AFLP), fluorescence amplified fragment length
polymorphism (FAFLP), restriction fragment length polymorphism (RFLP)]; PCR-
based methods [randomly amplified polymorphic DNA (RAPD), enterobacterial
repetitive intergenic consensus (ERIC), repetitive extragenic palindromic (REP)] and
PCR followed by DNA sequencing targeting single or multiple genes (MLST/MLSA).
In the case of AFLP and FAFLP, digestion of DNA with restriction enzymes was
followed by PCR. Other methods used included pulse field gel-electrophoresis (PFGE)
and plasmid profiles.
1.4.6.1 Typing methods
Although some of the methods mentioned in the previous section can be used for both
identification and typing purposes some are more suitable as typing methods for the
determination of strain relatedness. The use of plasmid profiles was reported to be
relatively unstable and not useful in genomic typing (Altwegg et al. 1988) while others
-17-
are more suitable for fingerprinting at strain level (Chang and Janda 2005). The poor
discriminatory patterns precluded PFGE to be used as an identification method. Instead,
PFGE offers an effective alternative as a typing method (Bonadonna et al. 2001;
Abdullah et al. 2003). The most satisfactory methods used in Aeromonas typing include
RFLP, RAPD, ERIC and AFLP and can be applied to determine the relatedness of
isolates in recurrent infections, the linkage of infections to environmental sources and
pseudo-outbreaks of disease (Janda and Abbott 2010).
1.4.6.2. Identification based on 16S-23S rRNA gene sequence
The most common target used in bacterial identification in laboratories world-wide is
the 16S rRNA gene (Stackebrandt and Goebels 1994; Petti et al. 2005; Boudewijns et
al. 2006; Janda and Abbott 2007). In aeromonads, 16S rRNA gene sequence signature
regions that differentiate some species from all other members in the genus have been
described (Demarta et al. 1999; Figueras et al. 2000b; Martínez-Murcia et al. 2000). As
a consequence, 16S rRNA-based probes designed to identify individual species directly
from samples have been developed (Ash et al. 1993a/b; Dorsch et al. 1994; Khan and
Cerniglia 1997; Demarta et al. 1999). Genus specific primers based on the 16S-23S
rRNA intergenic spacer region (ISR) have been designed to confirm the identity of
aeromonads following initial morphological and biochemical tests (Kong et al. 1999).
Overall, 16S rRNA sequencing has been found unsuitable to accurately differentiate
Aeromonas species (Martínez-Murcia et al. 2000) as the resolution power of the 16S
rRNA gene is limited when used to differentiate organisms that have identical or similar
sequences (Fox et al. 1992; Martínez-Murcia et al. 1992b; Thompson et al. 2004;
Morandi et al. 2005). For example, the DNA relatedness between A. caviae and A. trota
is 30% although their 16S rRNA sequences differ by only three nucleotides. On the
other hand, A. veronii and A. sobria differ by 14 nucleotides while they are 60 to 65%
related in DNA pairing studies (Martínez-Murcia et al. 1992b).
Secondly, the intragenomic heterogeneity of most Aeromonas based on rrn operon
nucleotide polymorphisms showed values ranging from 0.06 to 1.5%. The latter value
reported in A. veronii, a species known to possess up to six copies of the 16S rRNA
gene (Morandi et al. 2005; Alperi et al. 2008). Roger et al. (2012a) showed that
aeromonads harboured 8 to 11 rrn operons with 10 operons being observed in more than
92% of the strains studied. Although the use of the 16S rRNA gene as an identification
-18-
tool for aeromonads has been found useful by some (Figueras et al. 2005; Al-Benwan et
al. 2007), it should not be the only gene used for Aeromonas species identification and
delineation. This method has now been superseded by the use of housekeeping genes
sequencing (Husslein et al. 1992; Cascón et al. 1996; Khan and Cerniglia 1997; Yañez
et al. 2003; Soler et al. 2004; Nhung et al. 2007; Adekambi et al. 2008; Miñana-Galbis
et al. 2009).
1.4.6.3. Identification based on housekeeping gene sequence
Housekeeping genes are universally distributed among bacterial species and are rarely
predisposed to horizontal transfer as may be the case with 16S rRNA (Yañez et al.
2003; Morandi et al. 2005). The sequence divergence of housekeeping genes is usually
greater than that of 16S rRNA and in some cases the mean substitution rate is four to six
times higher (Yamamoto and Harayama 1996; Yañez et al. 2003; Soler et al. 2004;
Küpfer et al. 2006; Saavedra et al. 2006; Nhung et al. 2007; Beaz-Hidalgo et al. 2009;
Figueras et al. 2011b). Housekeeping genes provide better targets for Aeromonas
delineation (Yañez et al. 2003) with the added advantage that these methods are less
laborious to perform than DDH.
The sequences of the housekeeping genes recA, rpoB, dnaJ and cpn60 UT were
comparable with gyrB and rpoD and superior to 16S rRNA for the differentiation of
Aeromonas species (Küpfer et al. 2006; Nhung et al. 2007; Miñana-Galbis et al. 2009;
Lamy et al. 2010). The combined sequence of several housekeeping genes, multiloccus
sequence typing (MLST) also known as multilocus sequence analysis (MLSA) is a
powerful tool that can be used to determine the microbial diversity and classification of
these organisms (Beaz-Hidalgo et al. 2009; Figueras et al. 2011a; Martino et al. 2011).
1.4.6.4. Specific genes used as identification targets
Primers designed to detect virulence genes that allow the direct identification of specific
species included the aerolysin gene of A. trota (Husslein et al. 1992; Khan et al. 1999),
the lip gene of A. hydrophila (Cascón et al. 1996) and a 421 bp sequence from the 3’
region of the surface array protein (vapA) gene of A. salmonicida (Gustafson et al.
1992). The latter assay doubles as a non-invasive method to monitor A. salmonicida in
carrier fish and as a virulence marker (Gustafson et al. 1992). The glycerophospholipid-
cholesterol acyltransferase (GCAT) gene is universally present in Aeromonas (Chacón
et al. 2002) and has been used as a target to identify aeromonads to the genus level
-19-
(Puthucheary et al. 2012). Multiple-PCR (mPCR) assays capable of identifying up to
98% of Aeromonas species by detecting the presence of virulence genes have been
developed (Sen 2005; Chang et al. 2008). The m-PCR assay based on oligonucleotide
primers directed to the AHCYTOENT gene was designed for the rapid and specific
detection of A. hydrophila in diseased fish including viable but non-culturable cells
(Chu and Lu 2005a). Multiple-PCR assays are less expensive to run than RFLP and
almost complete agreement with identification by biochemical methods has been
reported (Sen 2005).
1.4.6.5. Restriction enzyme-based methods
Several enzyme-based methods such as ribotyping, AFLP and restriction endonuclease
analysis have been used alone, or in combination, as identification and typing tools in
the classification of aeromonads. Of these, ribotyping is a useful method for species
identification. It requires minimal DNA for testing and several strains can be tested
simultaneously (Rautelin et al. 1995b; Martínez-Murcia et al. 2000; Soler et al. 2003a).
Ribotyping has been the method of choice to demonstrate familial transmission and
long-term colonization by A. caviae (Moyer et al. 1992; Rautelin et al. 1995b) and to
determine routes of furunculosis in Finnish salmon caused by A. salmonicida ssp.
salmonicida (Hӓnninen et al. 1995b). Ribotyping was found to be more sensitive than
MLEE (Altwegg et al. 1991b) and superior to PFGE in an epidemiological study of A.
salmonicida ssp. salmonicida (Hӓnninen and Hirvela-Koski 1997). PFGE patterns from
mesophilic aeromonads revealed a high level of genetic heterogeneity (Talon et al.
1996; Hӓnninen and Hirvelӓ-Koski 1997; Villari et al. 2000). In contrast, PFGE patterns
for A. salmonicida ssp. salmonicida confirmed the genetic homogeneity of this species
(Hӓnninen and Hirvelӓ-Koski 1997; Miyata et al. 1995).
Bauab et al. (2003) suggested that ribotyping was a useful epidemiological tool suitable
for the study of Aeromonas infections. However, ribotyping was found to be less
discriminatory than ERIC-PCR (Soler et al. 2003a) and due to the genetically
homogeneous nature of A. salmonicida (Hӓnninen et al. 1995b), unsuitable for typing
these species (Altwegg and Luthi-Hottenstein 1991).
As mentioned in section 1.4.6.1 above, one of the most established molecular methods
used as a typing and identification tool for Aeromonas is RFLP (East and Collins 1993;
Borrell et al. 1997; Nagpal et al. 1998; Graf 1999a; Figueras et al. 2000b; Martínez-
Murcia et al. 2000; Soler et al. 2003a; Laganowska and Kaznowski 2004; Kaznowski
-20-
and Konecka 2005; Ghatak et al. 2007a). On the other hand, patterns generated by
AFLP allow clear differentiation of strains within a given species and correlate well
with DDH data suggesting that AFLP can be used for subtyping of aeromonads (Janssen
et al. 1996). Both AFLP and FAFLP have been proposed for epidemiological and
evolutionary studies (Huys et al. 1996b, 1997a, 2001; Janssen et al. 1996; Huys and
Swings 1999).
1.4.6.6. PCR-based methods
PCR-based methods used in the study of aeromonads include RAPD, AFLP and ERIC.
RAPD requires small amounts of genomic DNA (Miyata et al. 1995) while ERIC-PCR
has generally been used in combination with other methods as a typing or differential
tool (Davin-Regli et al. 1998; Sechi et al. 2002; Soler et al. 2003a; Szczuka and
Kaznowski 2004). Both ERIC and RAPD are considered superior to REP-PCR for
distinguishing Aeromonas species clones and for epidemiological investigation (Davin-
Regli et al. 1998; Szczuka and Kaznowski 2004). As a sole testing method, ERIC-PCR
was found more discriminatory for aeromonads than RFLP and REP (Soler et al.
2003a).
1.4.6.7. Disadvantages of molecular methods
In general, most molecular-based methods are time consuming, expensive and labour
intensive and do not always provide reliable and rapid results (Talon et al. 1996; Davin-
Regli et al. 1998; Figueras et al. 2000b; Sen 2005). Some methods are limited in their
applicability because they require materials not readily available in routine laboratories
while others cannot reliably discriminate between strains (Moyer et al. 1992). Other
methods, due to the type of results produced are more suitable for typing purposes than
for species identification (Taçao et al. 2005b). In addition, ribotyping, RFLP and AFLP
patterns can be difficult to interpret (Martínez-Murcia et al. 2000; Morandi et al. 2005;
Sen 2005) while RFLP is highly dependent on the type and number of endonucleases
used (Huys et al. 1996b; Graf 1999a; Figueras et al. 2000b; Kaznowski and Konecka
2005; Ghatak et al. 2007b). Atypical RFLP patterns have been recognized in clinical
strains (Alperi et al. 2008; Puthucheary et al. 2012) more often than in environmental
isolates (p < 0.01) due to microheterogeneities in the 16S rRNA gene (Alperi et al.
2008). The presence of microheterogeneities compromises accurate identification
(Morandi et al. 2005). The taxonomic value of AFLP as a reliable identification tool has
not yet been demonstrated (Martínez-Murcia 1999). Variations in DNA concentrations
-21-
can affect reproducibility of RAPD (Davin-Regli et al. 1995). This method is also
primer dependent (Oakey et al. 1995; 1996a) while interpretation of RAPD-PCR
fingerprints may be affected by co-migration of DNA fragments due to electrophoretic
resolution (Oakey et al. 1998). Due to a lack of standardization and with the exception
of AFLP and ribotyping, results obtained from most methods are often difficult to
compare (Tindall et al. 2010).
1.5. SEROTYPING
Serotyping was considered a promising tool to rapidly differentiate Aeromonas from
other oxidase-positive bacteria (Joseph and Carnahan 1994; Korbsrisate et al. 2002).
However, the variable typability rate of Aeromonas and antisera availability has
hampered the use of serology as a routine identification method in clinical laboratories
(Havelaar et al. 1992; Millership and Want 1993; Bonadonna et al. 2001). As a
consequence, serotyping of Aeromonas has been confined to a few specialized
laboratories.
No absolute association has been described between serotypes and certain phenotypes
as Aeromonas species are serologically heterogeneous, and no serogroup has been
uniquely associated with a single species (Havelaar et al. 1992; Millership and Want
1993; Bauab et al. 2003). The most dominant serogroups O:11, O:16, O:18, O:34 and
O:83 have been associated with gastroenteritis and septicaemia (Kokka et al. 1991;
Merino et al. 1993; Bauab et al. 2003). These serotypes can be present in up to 50% of
the typable strains isolated from human clinical material (Korbsrisate et al. 2002). The
loss of the O:34 antigen lipopolysaccharide due to mutation of the gne gene can affect
motility despite complete flagellar biogenesis as the absence of O:34 antigen affects
both swarming and swimming motilities (Canals et al. 2006a). Strains with the O:34
antigen have been found to have a high level of adhesion when grown at 20 but not at
37C. Thus, the O:34 antigen acts as an adhesion (Merino et al. 1996a).
Serotypes O:11 and O:34 have the capacity to produce a capsule when grown in
glucose-rich medium (Martínez et al. 1995). Group IIA capsules have been found in A.
hydrophila serotypes O:18 and O:34, while group IIB capsules are found in the O:21
and O:27 serogroups (Zhang et al. 2003). Serotype O:11 strains are known to possess an
S-layer that can confer resistance to the bactericidal activity of normal serum (Kokka et
al. 1991) in addition to being associated with invasive infections in an animal model
-22-
system (Paula et al. 1988). S-layers have also been described in serogroups O:14 and
O:81 of A. hydrophila which possessed S-layer proteins different from A. hydrophila
TF7 and A. salmonicida A450 (Esteve et al. 2004). Clinical strains have been found to
be less amenable to serotyping than environmental isolates (Millership and Want 1993).
A differential serological test that determines the presence of A. salmonicida while
ruling out A. hydrophila as the cause of furunculosis in Californian trout (Oncorhynchus
Mykiss, Walbaum, 1792) was developed by Markovic et al. (2007).
1.6. ECOLOGY
The ubiquitous nature of Aeromonas is reflected by the isolation of these organisms
from every environmental niche capable of sustaining bacterial growth. Although,
compared to other aquatic organisms like Pseudomonas species, Aeromonas are less
able to degrade simple compounds to be used as carbon sources (Schubert 1987). In
earlier ecological studies, laboratory personnel were confronted with isolation
procedures and identification schemes which, at the time, were based on phenotypic
testing only (Schubert 1987).
1.6.1. Aquatic environments
Aeromonas species have been recovered from surface water, fish ponds, brooks, sewage
in various stages of treatment, untreated and treated drinking water, rivers, lakes,
groundwater, wastewater, activated sludge, seawater (estuaries), spring, and stagnant
water (Freij 1984; Ørmen and Østensvik 2001). Despite the ubiquitous nature of these
micro-organisms in aquatic environments, their natural reservoir is still unknown.
Several possible niches have been proposed including the flora of plankton and seawater
(Simidu et al. 1971); as natural inhabitans of chironomid egg masses, a feature also
shared by V. cholerae (Senderovich et al. 2008); as inhabitans of duckweed, a potential
reservoir for infections of humans consuming contaminated fish (Rahman et al. 2007a);
and the ability to survive inside Acanthamoeba and remained viable during the
encystment process while exhibiting high levels of recovery from mature cysts (Yousuf
et al. 2013).
1.6.1.1. Distribution in water
The distribution of Aeromonas in water supplies varies depending on the levels of
pollution, geographical region, methods and media used in the identification of
aeromonads and the type of sample analysed (Araujo et al. 1991; Huys et al. 1995;
-23-
Kühn et al. 1997a/b; Sechi et al. 2002; Pablos et al. 2011). Furthermore, the diversity,
density and overall composition of aeromonads vary depending on the time of the year
(Kühn et al. 1997b; Rahman et al. 2007a). Aeromonads have been found to persist for
prolonged periods of time in different water systems (Kühn et al. 1992, 1997c; Rahman
et al. 2007a). Multiple clones have survived and multiplied in raw surface water after
the treatment process (Kühn et al. 1997b) while phenotypically and genotypically stable
clones could persist in treatment systems over long periods of time. As a result, clones
may have spread from hospitalized children with diarrhoea to fish farmed for human
consumption through the sewage water treatment system (Rahman et al. 2007a).
Bacterial populations can increase from 103 to 106 CFU ml after bottling (Hunter 1993)
to 2.7 x 106 CFU/ml and 1.9 x 106 CFU/ml in sediment sewage water and in duckweed
aquaculture-based hospital sewage water treatment plant, respectively (Rahman et al.
2007a).
The distribution of Aeromonas species varies according to the type of water analysed.
Both A. veronii bv. sobria and A. caviae have been predominant in sediment sewage
water and treated sewage effluents (Ashbolt et al. 1995; Rahman et al. 2007a). The high
incidence of A. caviae in sewage and wastewater suggests that this species may have a
role as a potential indicator of water pollution (Araujo et al. 1991; Ramteke et al. 1993).
In general, data from most studies implicate A. hydrophila as the most prominent
species isolated from water samples. Minor species such as A. culicicola and A. popoffii
have also been recovered from raw and treated waste water (Table 1.3) while A.
eucrenophila was isolated from water and infected fish (Singh and Sanyal 1999;
Figueira et al. 2011).
1.6.1.2. Water quality
The presence of Aeromonas in water depends primarily on the organic material content
of the water, water temperature, the length of time in the distribution network and the
presence of chlorine residues (Seidler et al. 1980; Kaper et al. 1981; Hird et al. 1983;
van der Kooij and Hijnen 1988; Borrell et al. 1998; Korzeniewska et al. 2005). The
survival rate of A. hydrophila in mineral water depended largely on the concentrations
of dissolved solid and organic matter and not on temperature of storage (Korzeniewska
et al. 2005). A significant correlation between organic matter content and total numbers
of mesophilic aeromonads in waters has been reported (Araujo et al. 1989;
-24-
Korzeniewska et al. 2005). In polluted water, a correlation also exists between the
numbers of aeromonads, faecal coliforms and the concentration of organic matter as
measured by biological oxygen demand (Araujo et al. 1991). The isolation of
Aeromonas from chlorinated water suggests a high organic loading as a result of
inadequate chlorination (Abbott et al. 1992). Although polluted waters rich in nutrients
readily support the growth of aeromonads, the presence of low molecular weight fatty
acids, amino acids or carbohydrates in low concentrations can also promote growth of
these organisms in less polluted waters (van der Kooij and Hijnen 1988). Indeed, A.
hydrophila could survive for considerable periods of time in filtered-autoclaved fresh
water or in filtered-autoclaved nutrient-poor water in the absence of natural microflora
(Kersters et al. 1996; Korzeniewska et al. 2005). In some regions, aeromonads have
been found to be more numerous than total coliforms in drinking (Schubert 1987) and
fresh water, and their presence may be an indicator of water quality (Knochel and
Jeppesen 1990).
1.6.1.3. Effects of temperature on growth and toxin production
The incidence of Aeromonas is usually low during winter compared to summer
(Millership and Chattopadhyay 1985; Chauret et al. 2001). The ability of aeromonads to
grow at low temperatures (5C) is a serious public health concern (Callister and Agger
1987; Nishikawa and Kishi 1988; Tsai and Chen 1996; Chang et al. 2008).
Environmental isolates are adapted to competitive growth at lower temperatures than
clinical isolates (Callister and Agger 1987). Toxin production is not necessarily
inhibited at low temperatures (Eley et al. 1993) and enterotoxigenic A. hydrophila
strains have been recovered from oysters stored for 18 months at 72C (Abeyta et al.
1986). Maalej et al. (2004) demonstrated that A. hydrophila enter a viable-but-not-
culturable (VBNC) state when exposed to nutritionally-deficient natural seawater at low
temperatures. Changes in temperature from 5 to 23C allowed multiple biological
activities such as adherence and haemolytic activity to be restored. The ability to enter
this VBNC state may explain the persistence of A. hydrophila in water systems during
winter (Maalej et al. 2004).
The ability of bacteria to enter a VBNC state permits the survival of microorganisms
when confronted with adverse environmental conditions. In this state, bacteria fail to
grow on routine microbiological media although they remain viable and retain virulence
(Fakruddin et al. 2013). Ramamurthy et al. (2014) stated that the VBNC had important
-25-
implication in several fields, including environmental monitoring, food technology, and
infectious disease management. These authors suggested that it was important to
investigate the association of bacterial pathogens under VBNC state and the
water/foodborne outbreaks. Studies have shown that A. hydrophila in a VBNC state
may not be as virulent to goldfish compared to normal culturable bacteria (Rahman et
al. 2001). However, from the public health point of view, culture-negative food,
environmental and clinical samples may not necessarily be an indication of a pathogen-
free status. Moreover, low grade infections may be due to the presence of VBNC in
water and food and in some instances incorrectly attributed to viruses when no bacteria
have been detected (Fakkrudin et al. 2013).
1.6.1.4. Aeromonas in drinking water
The incidence of Aeromonas in drinking water from distribution systems is generally
low (Le Chevalier et al. 1982). However, the affinity of A. hydrophila for low
molecular weight substrates indicates that this organism can readily grow if these
compounds are available in drinking water supplies (van der Kooij and Hijnen 1988). In
Denmark, Aeromonas species constituted 28% of the bacterial load in drinking water
with A. hydrophila as the dominant species (Knochel and Jeppesen 1990). The presence
of these organisms in drinking water is undesirable because Aeromonas strains have
been associated with a broad spectrum of human diseases (Gracey et al. 1982a; Burke et
al.1984b; Villari et al. 2003). The relatively high presence of Aeromonas in public
water systems in the USA was attributed to the inability of these systems to maintain an
adequate concentration of residual chlorine throughout the distribution system (Egorov
et al. 2011). The association of aeromonads in drinking water supplies with human
infections and ability to grow in distribution system biofilms, led to the inclusion of
Aeromonas in the first and second editions of the Contaminant Candidate List (CCL)
issued by the United States Environmental Protection Agency (USEPA 1998) and also
in the list of opportunistic bacterial pathogens among the major pathogens and parasites
of health concern (Bitton 2014). Moreover, the presence of Aeromonas in food and
water represents a vehicle for Aeromonas infections (Ottaviani et al. 2011).
-26-
Tab
le 1
.3
Dis
tribu
tion
of A
erom
onas
spp.
in w
ater
sour
ces f
rom
diff
eren
t loc
atio
ns
Spec
ies (
%)
Loc
atio
n T
ype
of w
ater
R
efer
ence
A.
cavi
ae
(55%
); A.
hy
drop
hila
(3
4%);
A.
sobr
ia
(6%
); Ae
rom
onas
spp.
(5%
) N
orth
ern
Spai
n
Sew
age,
rive
r, se
a A
rauj
o et
al.
(199
1)
A. h
ydro
phila
(51
%);1 A
. ca
viae
(26
%);1 A
. ve
roni
i (1
1%);
Unk
now
n sp
p. (1
1%)
Finl
and
Fres
h, d
rinki
ng
Hän
nine
n an
d Si
itone
n (1
995)
A. h
ydro
phila
(39%
);1 A. c
avia
e (2
3%);
A. so
bria
(17%
) B
elgi
um
Drin
king
, raw
/trea
ted
surf
ace
and
phre
atic
gr
ound
wat
er
Huy
s et a
l. (1
995)
A. so
bria
(14%
); A.
cav
iae
(11%
); A.
hyd
roph
ila (9
.5%
) In
dia
Met
ropo
litan
wat
er
supp
ly, b
ore,
drin
king
A
lava
ndi e
t al.
(199
9)
A. so
bria
(70%
); A.
pop
offii
(30%
) R
ussi
a D
rinki
ng
Ivan
ova
et a
l. (2
001)
A. h
ydro
phila
(67%
); A.
salm
onic
ida
(26%
); A.
sobr
ia (1
1%)
Sard
inia
, Ita
ly
Coa
stal
mar
ine
wat
ers
Sech
i et a
l. (2
002)
-27-
Tab
le 1
.3
Con
tinue
d.
Spec
ies (
%)
Loc
atio
n
Typ
e of
wat
er
Ref
eren
ce
A. h
ydro
phila
2 ; A. v
eron
ii (b
oth
biov
ars)
2 In
dia
Riv
er
Shar
ma
et a
l. (2
005)
A. c
ulic
icol
a (4
5%);
A. v
eron
ii (3
6%);
A. s
alm
onic
ida
(8%
); A.
hyd
roph
ila (7
%)
Spai
n D
rinki
ng
Figu
eras
et a
l. (2
005)
A. h
ydro
phila
(25%
) In
dia
Su
rfac
e B
how
mik
et a
l. (2
009)
A. m
edia
(~67
%);
A. c
avia
e (3
3%)
Leon
, Spa
in
Drin
king
Pa
blos
et a
l. (2
010)
A. d
hake
nsis
3 (55%
); A.
ver
onii
bv. s
obria
(27%
);
A. h
ydro
phila
(9%
) A
ustra
lia
Irrig
atio
n, re
serv
oir,
tre
ated
, bor
e,
chlo
rinat
ed
Ara
vena
-Rom
án e
t al.
(201
1b)
1 Iden
tifie
d as
com
plex
; 2 Perc
enta
ges n
ot g
iven
; 3 Prev
ious
ly c
lass
ified
as A
. aqu
ario
rum
.
-28-
1.6.2. Aeromonas in foods
Reports of Aeromonas-associated foodborne outbreaks began to appear frequently from
the late-1970s reaching a peak in the 1980s (Abeyta et al. 1986; Isonhood and Drake
2002). Aeromonas species are not unusually resistant to traditional food processing
techniques but are regularly isolated in variable numbers from vegetables, minced beef,
(20/29) and aspA 52% (15/31); A. veronii bv. sobria, aerA/haem 100% (31/31), ascV
32% (10/31) and 26% (8/31) for both alt and aexT.
7. 3.2. Distribution of virulence genes in stool isolates
The prevalence of virulence genes in stool specimens is shown in Table 7.2. The
aerA/haem and lafA genes were equally distributed in 55% (11/20) of the total isolates
followed by ast 45% (9/20) and alt 40% (8/20). The flaA+/lafA+ genotype was present in
20% (4/20) of total isolates while 35% (7/35) had both alt and ast. Ten% (2/20) of the
strains harboured more than five virulence genes.
-219-
7.3.3. Distribution of virulence genes in extra-intestinal isolates
The prevalence of virulence genes in extra-intestinal specimens is shown in Table 7.3
(blood), Table 7.4 (wounds) and Table 7.5 (miscellaneous specimens). Overall,
aerA/haem, lafA and alt were the most prevalent genes in these specimens. The
distribution of these genes in blood was 86% (24/28), 46% (13/28), 46% (13/28); in
wounds 91% (29/32), 69% (22/32) and 56% (18/32), and in miscellaneous specimens
83% (15/18), 67% (12/18) and 56% (10/18), respectively. Five or more virulence genes
were detected in 28% (9/32) wound isolates, 25% (7/28) in blood, and 22% (4/18)
miscellaneous specimens. The flaA+/lafA+ genotype was present in 28% (9/32) wound,
17% (3/18) miscellaneous specimen and 7% (2/28) blood isolates. Both alt and ast were
present in 33% (6/18) miscellaneous specimens, 29% (8/28) blood and 25% (8/32)
wound isolates.
7.3.4. Distribution of virulence genes among environmental isolates
The prevalence of virulence genes in Aeromonas isolated from environmental samples
is shown in Table 7.6. The most prevalent genes were aerA/haem 68% (21/31), alt 61%
(19/31), aspA 61% (19/31) and vasH 48% (15/31). The flaA+/lafA+ genotype was
present in 9.6% (3/31) of total isolates while 29% (9/31) harboured both alt and ast
genes. Individually, flaA was distributed in 39% (12/31); lafA in 29% (9/31), alt in 61%
(19/31) and ast in 39% (12/31) of total isolates.
7.3.5. Additional features
Overall, 27% (35/129) of the total isolates harboured five or more virulence genes
including 22% (22/98) in clinical and 42% (13/31) in environmental isolates. Five or
more virulence genes were detected in 100% (3/3) A. jandaei, 48% (14/29) A.
hydrophila, 42% (13/31), A. dhakensis, 19% (6/31) A. veronii bv. sobria and the single
strains of A. allosaccharophila and A. australiensis but not in A. bestiarum, A. caviae,
A. media, A. salmonicida and A. schubertii. Among the major species, the average
number of virulence genes detected was: A. dhakensis 4.3, A. hydrophila 4.3, A. veronii
bv. sobria 2.7 and A. caviae 1.7. The flaA+lafA+ genotype was present in 39% (12/31) A.
-220-
dhakensis, 21% (6/29) A. hydrophila, 4% (1/25) A. caviae, 3% (1/31) A. veronii bv.
sobria and in both A. media isolates (Tables 7.7).
7.3.6. Percentage identity of nucleotide sequences of positive products from
this study compared to sequences deposited in GenBank
The nucleotide sequences of gene products from selected strains were compared with
sequences deposited in GenBank and shown in Table 7.8. Accesion numbers for these
sequences are shown in Table 7.9. Unspecific amplification products were detected for
the vasH gene. The percentage of nucleotide identity for aerA/haem ranged from 71.2 to
96.5% over a 323 bp length; alt 90.9 to 93.8% over 244 bp; ast 94.7% over 265 bp;
aexT 88.0 to 94.1% over 510 bp; ascV 83.8% over 500 bp; aspA 71.2 to 93.7% over 306
bp; flaA 71.0 to 90.5% over 326 to 328 bp; lafA 69.3 to 83.0% over 555 to 580 bp and
vasH 86.0% over 572 bp. These results were not included in the original publication.
7.4. DISCUSSION
The distribution of 13 virulence genes assayed among 129 Aeromonas isolates was
determined in order to evaluate the pathogenic potential of these bacteria. The majority
(96%; 124/129) of the strains contained at least one virulence gene. The frequency of alt
and ast in stool isolates was 40% and 45%, respectively. In other studies, the frequency
for alt ranged from 16 to 35% and for ast 6 to 97% (Albert et al. 2000; Aguilera-
Arreola et al. 2005, 2007; Senderovich et al. 2012). In A. hydrophila, ast has been
detected between 30 and 91% of the isolates tested while has been absent in A. caviae
and A. veronii (Sen and Rodgers 2004; Aguilera-Arreola et al. 2007). In another study,
alt was almost exclusively detected in diarrhoeic isolates (Aguilera-Arreola et al. 2005).
The wide variations in the distribution of enterotoxin genes lend support to the
observations by Chopra et al. (2009) who stated that the prevalence of virulence genes
may depend on the strains examined at the time of testing.
The aerA/haem gene was detected in 77% of the total isolates consistent with other
reports where the prevalence of this gene ranged from 72 to 89% (Aguilera-Arreola et
al. 2007; Chacón et al. 2003; Puthucheary et al. 2012).
-221
-
Tab
le 7
.1 D
istri
butio
n of
viru
lenc
e ge
nes a
mon
g W
este
rn A
ustra
lian
Aero
mon
as sp
ecie
s
Gen
e fr
eque
ncy
(%)
Spec
ies
No.
test
ed
aerA
/hae
m
aexT
al
t as
cV
aspA
as
t fla
A
lafA
va
sH
A. a
llosa
ccha
roph
ila
1c
+
+
+ +
+
A. a
ustr
alie
nsis
1e
+
+ +
+
A. b
estia
rum
1c
+
+
+
A. c
avia
e 25
c 14
(56)
1(
4)
4 (1
6)
5 (2
0)
3 (1
2)
15 (6
0)
2 (8
)
2
e
1
(50)
1
(50)
T
otal
27
14 (5
2)
1 (4
) 5
(18)
1
(4)
5 (1
8)
3 (1
1)
15 (5
5)
2 (7
)
A. d
hake
nsis
21
c 17
(81)
1
(5)
15 (7
1)
2 (9
) 3
(14)
5
(34)
13
(62)
17
(81)
11
(52)
10
e 6
(60)
5
(50)
10
(100
) 3
(30)
6
(60)
4
(40)
7
(70)
3
(30)
8
(80)
T
otal
31
23 (7
4)
6 (1
9)
25 (8
1)
5 (1
6)
9 (2
9)
9 (2
9)
20 (6
4)
20 (6
4)
19 (6
1)
A. h
ydro
phila
23
c 20
(87)
1
(4)
20 (8
7)
10 (4
3)
21 (9
1)
6 (2
6)
16 (6
9)
3 (1
3)
6
e 3
(50
5 (8
3)
5 (8
3)
6 (1
00)
3 (5
0)
4 (6
7)
2 (3
3)
T
otal
29
23 (7
9)
1 (3
) 25
(86)
15
(52)
27
(93)
9
(31)
20
(69)
5
(17)
A. ja
ndae
i 3e
2
(67
2 (6
7)
2 (6
7)
2 (6
7)
1 (3
3)
2 (6
7)
2 (6
7)
-222
-
Tab
le 7
.1
Con
tinue
d.
Gen
e fr
eque
ncy
(%)
Spec
ies
No.
test
ed
aerA
/hae
m
aexT
al
t as
cV
aspA
as
t fla
A
lafA
va
sH
A. m
edia
2c
1
(50)
1
(50)
1
(50)
1
(50)
2
(100
) 2
(100
)
A. sa
lmon
icid
a 1c
+
+
+
+
1e
+
+ +
+
A. sc
hube
rtii
1c
+
+
A. v
eron
ii bv
. sob
ria
23c
23 (1
00)
5 (2
2)
7 (3
0)
6 (2
6)
3 (1
3)
5 (2
2)
3 (1
3)
6 (2
6)
3 (1
3)
8
e 8
(100
) 3
(37)
1
(12)
4
(50)
2
(25)
1
(12)
1
(12)
3
(37)
T
otal
31
31 (1
00)
8 (2
6)
8 (2
6)
10 (3
2)
5 (1
6)
6 (1
9)
4 (1
3)
6 (1
9)
6 (1
9)
Tota
l clin
ical
98
79
(81)
a 9
(9)b
49 (5
0)c
9 (9
)d 19
(19)
e 38
(39)
f 29
(29)
g 58
(59)
h 19
(19)
i
Tota
l env
ironm
enta
l 31
21
(68)
a 8
(26)
b 20
(64)
c 12
(39)
d 19
(61)
e 12
(39)
f 12
(39)
g 9
(29)
h 15
(48)
i
Gra
nd to
tal
129
100
(77)
17
(13)
69
(53)
21
(16)
38
(29)
50
(39)
41
(32)
67
(51)
34
(26)
, n
ot d
etec
ted;
+, d
etec
ted;
c, c
linic
al; e
, env
ironm
enta
l; a p
= 0.
1453
; b p
= 0.
0295
; c p =
0.21
52; d
p =
0.00
04; e p
< 0.
0001
; f p =
1.00
00; g
p =
0.37
97; h p
= 0
.004
0; i p
= 0
.002
3
-223
-
Tab
le 7
.2
Dis
tribu
tion
of v
irule
nce
gene
s in
Aero
mon
as sp
p. is
olat
ed fr
om st
ools
(n =
20)
Gen
es d
etec
ted
Spec
ies
Stra
in
no.
a/h
alt
ast
lafA
fla
A
ascV
ae
xT
aspA
va
sH
Stool1
Age
Gender
Clin
ical
dat
a
A. a
llosa
ccha
roph
ila
100
+
+ +
+
+
74
F C
ampy
loba
cter
je
juni
als
o is
olat
ed2
A. d
hake
nsis
16
9
+ +
+ +
L 35
M
In
fect
ed C
hron
s2
18
0
+ +
+
+
W
80
F Pe
rsis
tent
di
arrh
oea;
di
verti
culit
is
18
3
+ +
+ +
L 63
F
Dia
rrho
ea
A. c
avia
e 94
+
+
L 74
M
N
/D
10
2 +
W
71
F D
iarr
hoea
pos
t ch
emot
hera
py2
10
3 +
+ +
+
L 57
F
Dia
rrho
ea fo
r 2
wee
ks
15
6
+ +
+
+
L 5
m
F R
ecen
t tra
vel
15
8
+
W
63
M
Rec
ent t
rave
l
187
+
+ L
44
F Pr
em m
enop
ause
216
+ +
+
SF
74
F
N/D
N
/D, n
o da
ta; 1 St
ool c
onsi
sten
cy, A
. allo
sacc
haro
phila
was
isol
ated
from
a c
olos
tom
y sp
ecim
en; L
, loo
se, W
, wat
ery,
SF,
sem
i-for
med
; 2 le
ucoc
ytes
det
ecte
d in
stoo
ls; a
/h, a
erA/
haem
; M, m
ale;
F, f
emal
e.
-224
-
T
able
7.2
Con
tinue
d.
Gen
es d
etec
ted
Spec
ies
Stra
in
no.
a/h
alt
ast
lafA
fla
A
ascV
ae
xT
aspA
va
sH
Stool1
Age
Gender
Clin
ical
dat
a
A. h
ydro
phila
13
3
+ +
+ +
+
31
M
Po
st/m
orte
m
spec
imen
A.
med
ia
179
+
+ +
+
L
74
M
Prol
onge
d in
trave
nous
an
tibio
tics
A. v
eron
ii bv
sobr
ia
99
+
W
78
F
N/D
2
137
+ +
W
33
M
N
/D
16
6 +
+
+
L 70
F
Dia
rrho
ea
18
4 +
W
78
M
N/D
2
189
+
+ W
67
F
Dia
rrho
ea,
mae
lena
, Tr
icho
mon
as
hom
inis
+
21
5 +
+
+
SF
89
F N
/D
21
9 +
W
61
F D
iarr
hoea
for 1
w
eek2
Tota
l no.
11
8
9 11
7
1 1
3 5
%
55
40
45
55
35
5
5 15
25
-225
-
Tab
le 7
.3 D
istri
butio
n of
viru
lenc
e ge
nes i
n Ae
rom
onas
spp.
isol
ated
from
blo
od (n
= 2
8)
Gen
es d
etec
ted
Spec
ies
Stra
in
no.
a/h
alt
ast
flaA
la
fA
aspA
ae
xT
ascV
va
sH
Age
Gender
Clin
ical
dat
a
A. d
hake
nsis
60
+
+
+
75
M
Acu
te re
nal f
ailu
re
70
+
+
70
M
Abd
omin
al se
psis
154
+ +
+
+
+ N
/D
N/D
N
/D
A. b
estia
rum
68
+
+
+
+
46
F N
/D; p
olym
icro
bial
A.
cav
iae
57
+
+
48
M
N
/D
58
83
F N
/D
65
+
82
M
Cho
lang
eo c
arci
nom
a;
poly
mic
robi
al
75
+
53
F H
ickm
an c
athe
ter
colle
cted
blo
od; N
/D
80
+
80
F N
/D
96
+
+
72
M
N/D
106
72
M
Se
ptic
109
+
+
70
F
Epig
astri
c pa
in;
poly
mic
robi
al
11
0 +
+
50
M
N/D
; pol
ymic
robi
al
20
0
+
+
N/D
N
/D
N/D
-226
-
Tab
le 7
.3
Con
tinue
d.
Gen
es d
etec
ted
Sp
ecie
s St
rain
no
. a/
h al
t as
t fla
A
lafA
as
pA
aexT
as
cV
vasH
Age
Gender
Clin
ical
dat
a
A. h
ydro
phila
59
+
+ +
+
+
65
M
Febr
ile n
eutro
peni
c
84
+ +
+
+ +
81
F
N/D
; Sta
phyl
ococ
cus a
ureu
s als
o is
olat
ed
14
9 +
+ +
+
+
68
M
N/D
151
+ +
+ +
73
M
N
/D
15
2 +
+ +
73
M
N/D
A.
med
ia
85
+
+
+
+
17
F
Prol
onge
d vi
ral-l
ike
illne
ss;
poly
mic
robi
al
A. v
eron
ii bv
sobr
ia
72
+
56
M
C
ance
r/pan
crea
s; p
olym
icro
bial
81
+
+
89
F
Sept
ic sh
ock
11
1 +
+
+
88
F Li
ver c
ance
r; po
lym
icro
bial
125
+ +
+ +
+
88
F
Vom
iting
131
+
+ +
69
M
Le
ukae
mia
; On
chem
othe
rapy
218
+ +
+
+ +
<1 5
N/D
N
/D
22
1 +
+
47
F Fe
ver;
brea
st c
ance
r; po
lym
icro
bial
269
+ +
+
+
+ +
81
M
Fe
ver;
AM
L To
tal n
o.
24
13
8 7
13
5 5
3 2
%
86
46
29
25
46
18
18
11
7
a/h,
aer
A/ha
em; A
ML,
acu
te m
yelo
blas
tic le
ukae
mia
; N/D
, no
data
; M, m
ale;
F, f
emal
e
-227
-
Tab
le 7
.4
Dis
tribu
tion
of v
irule
nce
gene
s in
Aero
mon
as sp
p. is
olat
ed fr
om w
ound
s (n
= 32
)
Gen
es d
etec
ted
Spec
ies
Stra
in
no.
a/h
alt
ast
flaA
la
fA
aspA
ae
xT
ascV
va
sH
Age
Gender
Clin
ical
dat
a
A. d
hake
nsis
67
+
+
+ +
+
20
M
Cel
lulit
is
71
+
+
+ +
+
+
16
F In
fect
ed la
cera
tion
of fo
ot (r
iver
wat
er)
73
+
+
+ +
28
M
App
endi
citis
79
+
+
+
60
M
Infe
cted
fing
er
91
+
+
+
78
F Le
g w
ound
95
+
+
+ +
+
50
M
Wou
nd in
fect
ed p
ost e
lbow
surg
ery;
on
kefle
x
104
+ +
+
+ 60
F
Non
-hea
ling
shin
; on
flucl
oxic
illin
10
7 +
+
+ +
+
39
M
Sept
ic w
ound
righ
t-han
d; o
n flu
coxi
cilli
n
14
1 +
+ +
+
N/D
U
N
/D
17
6 +
+ +
+
26
M
Puru
lent
wou
nd o
oze
right
-leg
22
0 +
+
+ +
+
+
N/D
U
U
lcer
27
9 +
+
+
14
M
Ost
eom
yelit
is le
ft th
umb;
Sta
phyl
ococ
cus
aure
us a
lso
isol
ated
.
-228
-
Tab
le 7
.4
Con
tinue
d.
Spec
ies
Stra
in
no.
a/h
alt
ast
flaA
la
fA
aspA
ae
xT
ascV
va
sH
Age
Gender
Clin
ical
dat
a
A. c
avia
e 14
3 +
+
+
N/D
U
N
/D
16
3
50
M
Han
d w
ound
27
0 +
+
+
37
F In
fect
ed w
ound
; Sta
phyl
ococ
cus
aure
us a
lso
isol
ated
A.
hyd
roph
ila
23
+
+
N
/D
U
N/D
69
+
+ +
+
+
18
M
Infe
cted
subu
ngua
l hae
mat
oma;
po
lym
icro
bial
90
+ +
+
36
F
Ulc
er; S
taph
yloc
occu
s aur
eus a
nd
anae
robe
s als
o is
olat
ed
98
+
+ +
+
35
M
Infe
cted
left
hand
10
1 +
+ +
+
76
F M
ultip
le u
lcer
s
11
2 +
+ +
+ +
+
66
F Po
st/la
para
tom
y an
d w
ound
br
eakd
own;
pol
ymic
robi
al
11
7
+ +
+
+
+
54
F N
/D; p
olym
icro
bial
12
6
+
22
M
Dirt
y pu
rule
nt a
quat
ic w
ound
12
8 +
+ +
+
13
M
Stap
hylo
cocc
us a
ureu
s als
o is
olat
ed
14
8 +
+
+
73
M
N/D
-229
-
Tab
le 7
.4
Con
tinue
d.
Gen
es d
etec
ted
Spec
ies
Stra
in
no.
a/h
alt
ast
flaA
la
fA
aspA
ae
xT
ascV
va
sH
Age
Gender
Clin
ical
dat
a
A. sa
lmon
icid
a 19
0 +
+
+
+
65
M
Off
ensi
ve sm
elly
pur
ulen
t di
scha
rge
of le
ft-po
int f
inge
r A.
schu
bert
ii 18
6 +
+
42
M
Pus f
rom
infe
cted
wou
nd in
foot
A. v
eron
ii bv
. sob
ria
24
+
<1
5 U
N
/D
66
+
+
+
+
+
47
F R
ight
-low
er le
g
12
9 +
+
+
48
M
Infe
cted
wou
nd ri
ght-a
nkle
14
7 +
+ +
<15
M
N/D
17
4 +
+
71
M
Infe
cted
thum
b na
il; M
ixed
an
aero
bes a
lso
isol
ated
To
tal n
o.
29
18
13
10
22
6 3
3 11
%
91
56
41
31
69
19
9
9 34
N/D
, no
data
; M, m
ale,
F, f
emal
e, U
, unk
now
n; a
/h, a
erA/
haem
.
-230
-
Tab
le 7
.5
Dis
tribu
tion
of v
irule
nce
gene
s in
Aero
mon
as sp
p. is
olat
ed fr
om m
isce
llane
ous s
peci
men
s (n
= 18
)
Gen
es d
etec
ted
Spec
ies
Stra
in
no.
a/h
alt
ast
flaA
la
fA
aspA
as
cV
vasH
A
ge
Gen
der
Sour
ce
C
linic
a da
ta
A. d
hake
nsis
47
+
+
+
81
M
sp
utum
Le
u 3+
;Abu
ndan
t gr
owth
; N/D
56
+
+ +
35
M
bone
chi
ps
Infe
cted
frac
ture
93
+ +
+
35
M
urin
e U
rinar
y tra
ct
infe
ctio
n A.
cav
iae
62
+
+
47
M
cath
eter
s Li
ver t
rans
plan
t; po
lym
icro
bial
78
+
75
M
dial
ysis
flu
id
Perit
oniti
s
14
0
57
F
dial
ysis
flu
id
Perit
onea
l dia
lysi
s;
poly
mic
robi
al
17
8
+ +
34
F
bile
B
iliar
y ob
stru
ctio
n;
poly
mic
robi
al
18
8
+
+
68
F
bile
A
cute
cho
lecy
stiti
s;
poly
mic
robi
al
A. h
ydro
phila
61
+
+ +
+
62
M
ca
thet
ers
Bili
ary
seps
is;
poly
mic
robi
al
83
+
+ +
+
53
F
sput
um
Leu
3+; N
/D;
89
+
+ +
+
46
F
bile
C
hola
ngiti
s;
poly
mic
robi
al
-231
-
T
able
7.5
C
ontin
ued.
Gen
es d
etec
ted
Spec
ies
Stra
in
no.
a/h
alt
ast
flaA
la
fA
aspA
as
cV
vasH
A
ge
Gen
der
Sour
ce
Clin
ical
dat
a
A. h
ydro
phila
92
+
+
+ +
+
66
F
tissu
e Pa
ncre
atic
ne
cros
is;
poly
mic
robi
al
11
3 +
+ +
+ +
+
+ 35
M
dr
ain
fluid
N
/D; p
olym
icro
bial
11
8 +
+ +
+
+
30
F
sput
um
Exac
erba
tion
of
CF;
pol
ymic
robi
al;
15
0 +
+ +
73
M
tis
sue
Foot
infe
ctio
n
A. v
eron
ii bv
sobr
ia
25
+
<15
N/D
ca
thet
ers
N/D
27
+
+
+
+ +
<1
5 N
/D
tissu
e N
/D
17
1 +
83
F
sput
um
Asp
iratio
n pn
eum
onia
; po
lym
icro
bial
To
tal n
o.
15
10
7 3
12
5 2
1
%
83
56
39
17
67
28
11
6
M, m
ale;
F, f
emal
e; N
/D, n
o da
ta; a
/h, a
erA/
haem
; CF,
cyt
isc
fibro
sis;
Leu
3+,
man
y le
ucoc
ytes
seen
on
mic
rosc
opy.
-232
-
Tab
le 7
.6
Dis
tribu
tion
of v
irule
nce
gene
s am
ong
Aero
mon
as sp
p. is
olat
ed fr
om e
nviro
nmen
tal s
ourc
es (n
= 3
1)
Gen
es d
etec
ted
Spec
ies
Stra
in
no.
a/h
alt
ast
flaA
la
fA
aspA
ae
xT
ascV
va
sH
Sour
ce
Loc
atio
n
A. a
ustr
alie
nsis
26
6 +
+
+ +
+
IW
Rur
al
A. d
hake
nsis
31
+
+
+
Fish
A
DW
A
32
+
+
+
+
Fish
A
DW
A
22
3
+ +
+
+ +
+ +
Unk
now
n U
nkno
wn
22
9 +
+
+ +
+
+
TW
Unk
now
n
230
+ +
+
+
W
ater
M
etro
polit
an
23
5 +
+ +
+
+
Wat
er
Unk
now
n
241
+ +
+
+ +
W
ater
U
nkno
wn
24
2
+
+
+
+
Wat
er
Unk
now
n
256
+ +
+ +
+ +
Wat
er
Unk
now
n
257
+ +
+
+ +
+
+ W
ater
U
nkno
wn
A. c
avia
e 30
Fish
A
DW
A
26
4
+
+
IW
Unk
now
n A.
hyd
roph
ila
34
+
+
+ +
Fi
sh
AD
WA
231
+
+ +
+
SW
M
etro
polit
an
24
3 +
+
+
+
+
Wat
er
Unk
now
n
-233
-
Tab
le 7
.6
C
ontin
ued.
Gen
es d
etec
ted
Spec
ies
Stra
in
no.
a/h
alt
ast
flaA
la
fA
aspA
ae
xT
ascV
va
sH
Sour
ce
Loc
atio
n
A. h
ydro
phila
24
5
+ +
+
+
Wat
er
Unk
now
n
260
+
+
+
+ W
ater
U
nkno
wn
26
1 +
+ +
+ +
+
IW
Unk
now
n A.
jand
aei
35
+
+ +
+
+ Fi
sh le
sion
A
DW
A
25
3 +
+
+
+ +
Wat
er
Unk
now
n
262
+
+
+ +
+
W
ater
U
nkno
wn
A. sa
lmon
icid
a 19
9 +
+
+
+
Cra
b R
ural
A.
ver
onii
bv. s
obria
33
+
+
+ +
Fish
A
DW
A
22
4 +
+
BW
M
etro
polit
an
23
7 +
+
+ +
+
Wat
er
Unk
now
n
247
+ +
+
W
ater
U
nkno
wn
25
4 +
Wat
er
Unk
now
n
259
+
+
+
+ W
ater
U
nkno
wn
26
5 +
+
IW
Unk
now
n
268
+
+ IW
U
nkno
wn
Tota
l no.
21
19
12
12
9
19
8 12
15
%
68
61
39
39
29
61
26
39
48
a/h
, aer
A/ha
em; I
W, i
rrig
atio
n w
ater
; TW
, tre
ated
wat
er; B
W, b
ore
wat
er; A
DW
A, A
gric
ultu
re D
epar
tmen
t of W
este
rn A
ustra
lia
-234
-
Tab
le 7
.7
Add
ition
al fe
atur
es
Spec
ies (
no. s
trai
ns)
Ave
rage
no.
gen
es p
er st
rain
fla
A+ la
fA+ g
enot
ype
(%)
>5 v
irul
ence
gen
es (%
)
C
lin
Env
T
otal
C
lin
Env
T
otal
C
lin
Env
T
otal
A. c
avia
e (2
7)
1.8
1.0
1.7
4 0
~4
0 0
0
A. d
hake
nsis
(31)
4.
0 5.
1 4.
3 48
a 20
a 39
33
c 60
c 42
A. h
ydro
phila
(29)
4.
2 4.
6 4.
3 22
b 17
b 21
48
d 50
d 48
A. v
eron
ii bv
. sob
ria (3
1)
2.6
2.8
2.7
3 0
4
22e
12e
19
Tot
al
3.1
3.4
3.2
19
9 17
26
30
27
A. a
llosa
ccha
roph
ila (1
) 5
0
10
0
A. a
ustr
alie
nsis
(1)
4
0
10
0
A. b
estia
rum
(1)
4
0
0
A. ja
ndae
i (3)
5
0
100
A. m
edia
(2)
4
10
0
0
A. sa
lmon
icid
a (2
) 4
4 4
0 0
0 0
0 0
A. sc
hube
rtii
(1)
2
0
0
a Pe
rcen
tage
diff
eren
ces
are
stat
istic
ally
sig
nific
ant
(p <
0.0
001)
; b Pe
rcen
tage
diff
eren
ces
are
not
stat
istic
ally
sig
nific
ant
(p =
0.4
75);
c Perc
enta
ge d
iffer
ence
s ar
e st
atis
tical
ly s
igni
fican
t (p
= 0
.000
2);
d Per
cent
age
diff
eren
ces
are
not
stat
istic
ally
sig
nific
ant
(p =
0.8
87);
e Perc
enta
ge d
iffer
ence
s are
not
stat
istic
ally
sign
ifica
nt (p
= 0
.889
2); C
lin, c
linic
al is
olat
es; E
nv, e
nviro
nmen
tal i
sola
tes.
- 235
-
Tab
le 7
.8 P
erce
ntag
e id
entit
y of
gen
e pr
oduc
t seq
uenc
es fr
om th
is st
udy
com
pare
d w
ith se
quen
ces d
epos
ited
in G
enB
ank
Gen
e Sp
ecie
s/st
rain
no.
%
L
engt
h (b
p)
Spec
ies
Acc
esio
n no
.
aerA
/hae
m
A. d
hake
nsis
60,
73, 2
56, 2
57, 2
79
71.2
32
3 A.
ver
onii
bv. s
obria
A.
hyd
roph
ila
A. h
ydro
phila
AB
1090
93
AY
6110
33
AF4
1046
6
A.
aus
tral
iens
is 2
66
90.4
32
3
A. b
estia
rum
68
78.3
32
3
A. c
avia
e 27
0 96
.5
323
A.
jand
aei 3
5 90
.4
323
A.
ver
onii
bv. s
obria
125
, 215
, 221
, 237
, 259
, 269
93
.4
323
A.
ver
onii
bv. s
obria
125
, 215
, 221
, 237
, 259
, 269
93
.1
323
A. sa
lmon
icid
a
X65
048
alt
A. d
hake
nsis
31,
32,
60,
67,
180
, 183
, 223
, 229
, 235
, 241
, 242
, 256
90
.9
244
A. h
ydro
phila
A.
hyd
roph
ila
A. h
ydro
phila
A.
hyd
roph
ila
JBN
1302
JQ
0031
97
L775
73
JX48
9379
A.
aus
tral
iens
is 2
66
96.3
24
4
A. c
avia
e 10
3, 1
88, 2
00, 2
64
93.0
24
4
A. h
ydro
phila
34,
59,
61
94.2
24
4
A. ja
ndae
i 253
, 262
94
.7
244
A.
ver
onii
bv. s
obria
111
, 218
, 247
, 269
93
.8
244
ast
A. d
hake
nsis
154
, 169
, 183
A. c
avia
e 10
3, 1
43, 1
56
94.7
26
5 A.
hyd
roph
ila
JQ00
3211
A. h
ydro
phila
23,
34,
59,
83,
113
, 117
, 243
, 261
A. m
edia
179
; A. v
eron
ii bv
. sob
ria 2
7, 6
6, 1
25, 2
69
aexT
A.
dha
kens
is 3
1, 3
2, 2
20, 2
30; A
.med
ia 8
5 94
.1
510
A. v
eron
ii EF
0260
79
-- 2
36 --
Tab
le 7
.8
Con
tinue
d.
Gen
e Sp
ecie
s/st
rain
no.
%
L
engt
h (b
p)
Spec
ies
Acc
esio
n no
.
aexT
A.
ver
onii
bv. s
obria
33,
66,
218
, 224
, 269
;
A. d
hake
nsis
31,
32,
220
, 230
; A.m
edia
85
88.0
51
0 A.
salm
onic
ida
AF2
8836
6
A. v
eron
ii bv
. sob
ria 3
3, 6
6, 2
18, 2
24, 2
69;
ascV
A.
allo
sacc
haro
phila
100
; A. d
hake
nsis
47,
220
; 83
.8
500
A. v
eron
ii bv
. ver
onii
HM
5845
87
A.
aus
tral
iens
is 2
66; A
. ver
onii
bv. s
obria
66,
218
, 221
, 269
as
pA
A. a
ustr
alie
nsis
266
85
.6
306
A. h
ydro
phila
A
F126
213
A.
aus
tral
iens
is 2
66
86.2
30
6 A.
sobr
ia
AF2
5347
1
A. h
ydro
phila
34,
69,
84,
92,
149
, 261
71
.2
306
A. h
ydro
phila
A
F126
213
A.
jand
aei 2
62
92.4
30
6 A.
sobr
ia
AF2
5347
1
A. v
eron
iii b
v. so
bria
27
93.7
30
6 A.
sobr
ia
AF2
5347
1
A. sa
lmon
icid
a 19
9 90
.1
306
A. sa
lmon
icid
a
X67
043
flaA
A. d
hake
nsis
60,
67,
176
, 183
, 229
84
.6
326
A. h
ydro
phila
JQ
0032
17
A.
dha
kens
is 6
0, 6
7, 1
76, 1
83, 2
29
90.5
32
7 A.
hyd
roph
ila
AY
4243
58
A.
hyd
roph
ila 9
2, 1
51, 2
61
78.8
32
7 A.
salm
onic
ida
EU
4103
42
A.
bes
tiaru
m 6
8 71
.0
328
A. sa
lmon
icid
a
EU41
0342
la
fA
A. h
ydro
phila
133
83
.0
555
A. h
ydro
phila
D
Q12
4694
A. h
ydro
phila
260
78
.9
580
A. h
ydro
phila
D
Q12
4694
A. m
edia
179
72
.7
580
A. p
unct
ata
A
F348
135
A.
dha
kens
is 9
5 74
.3
580
A. p
unct
ata
A
F348
135
A.
dha
kens
is 9
5 69
.3
580
A. ja
ndae
i A
Y22
8331
va
sH
A. d
hake
nsis
31
86.0
57
2 A.
hyd
roph
ila
GQ
3597
79
-- 2
37 --
Tab
le 7
.9
Acc
essi
on n
umbe
rs o
f seq
uenc
es d
eriv
ed fr
om v
irule
nce
gene
s and
dep
osite
d in
Gen
Ban
k
Gen
e Sp
ecie
s St
rain
no.
A
cces
sion
no.
Sp
ecie
s St
rain
no.
A
cces
sion
no.
aerA
/hae
m
A. a
ustr
alie
nsis
26
6 H
G97
7017
A.
bes
tiaru
m
68
HG
9770
18
A.
dha
kens
is
73
HG
9770
19
A. d
hake
nsis
27
9 H
G97
7020
A.
hyd
roph
ila
59
HG
9770
21
A. h
ydro
phila
14
8 H
G97
7022
A.
jand
aei
35
HG
9770
23
A. v
eron
ii bv
. sob
ria
215
HG
9770
24
A.
ver
onii
bv. s
obria
23
7 H
G97
7025
A.
ver
onii
bv. s
obria
12
5 H
G97
7026
A.
ver
onii
bv. s
obria
22
1 H
G97
7027
A.
ver
onii
bv. s
obria
26
9 H
G97
7028
A.
cav
iae
270
HG
9770
29
A. ja
ndae
i 25
3 H
G97
7030
A.
hyd
roph
ila
151
HG
9770
31
A. d
hake
nsis
60
H
G97
7032
A.
dha
kens
is
256
HG
9770
33
A. d
hake
nsis
25
7 H
G97
7034
A.
ver
onii
bv. s
obria
25
9 H
G97
7035
aexT
A.
dha
kens
is
220
HG
9770
36
A. v
eron
ii bv
. sob
ria
269
HG
9770
37
A.
ver
onii
bv. s
obria
33
H
G97
7038
A.
ver
onii
bv. s
obria
66
H
G97
7039
A.
ver
onii
bv. s
obria
13
1 H
G97
7040
A.
ver
onii
bv. s
obria
21
8 H
G97
7041
-- 2
38 --
Tab
le 7
.9
Con
tinue
d.
Gen
e Sp
ecie
s St
rain
no.
A
cces
sion
no.
Sp
ecie
s St
rain
no.
A
cces
sion
no.
aexT
A.
ver
onii
bv. s
obria
22
4 H
G97
7042
A.
dha
kens
is
31
HG
9770
43
A.
dha
kens
is
230
HG
9770
44
A. d
hake
nsis
32
H
G97
7045
A.
med
ia
85
HG
9770
46
A. v
eron
ii bv
. sob
ria
237
HG
9770
47
alt
A. a
ustr
alie
nsis
26
6 H
G97
7048
A.
cav
iae
10
3 H
G97
7049
A.
cav
iae
18
8 H
G97
7050
A.
cav
iae
26
4 H
G97
7051
A.
cav
iae
20
0 H
G97
7052
A.
dha
kens
is
31
HG
9770
53
A.
dha
kens
is
67
HG
9770
54
A. d
hake
nsis
60
H
G97
7055
A.
dha
kens
is
183
HG
9770
56
A. d
hake
nsis
18
0 H
G97
7057
A.
dha
kens
is
32
HG
9770
58
A. d
hake
nsis
25
6 H
G97
7059
A.
dha
kens
is
223
HG
9770
60
A. d
hake
nsis
22
9 H
G97
7061
A.
dha
kens
is
235
HG
9770
62
A. d
hake
nsis
24
1 H
G97
7063
A.
dha
kens
is
242
HG
9770
64
A. h
ydro
phila
34
H
G97
7065
A.
hyd
roph
ila
61
HG
9770
66
A. h
ydro
phila
59
H
G97
7067
-- 2
39 --
Tab
le 7
.9
Con
tinue
d.
Gen
e Sp
ecie
s St
rain
no.
A
cces
sion
no.
Sp
ecie
s St
rain
no.
A
cces
sion
no.
alt
A. ja
ndae
i 25
3 H
G97
7068
A.
jand
aei
262
HG
9770
69
A.
ver
onii
bv. s
obria
26
9 H
G97
7070
A.
ver
onii
bv. s
obria
24
7 H
G97
7071
A.
ver
onii
bv. s
obria
11
1 H
G97
7072
A.
ver
onii
bv. s
obria
21
8 H
G97
7073
ascV
A.
allo
sacc
haro
phila
10
0 H
G97
7074
A.
aus
tral
iens
is
266
HG
9770
75
A.
dha
kens
is
256
HG
9770
76
A. d
hake
nsis
22
3 H
G97
7077
A.
dha
kens
is
220
HG
9770
78
A. v
eron
ii bv
. sob
ria
27
HG
9770
79
A.
ver
onii
bv. s
obria
24
7 H
G97
7080
A.
ver
onii
bv. s
obria
13
1 H
G97
7081
ast
A. h
ydro
phila
23
H
G97
7082
A.
hyd
roph
ila
149
HG
9770
83
A.
hyd
roph
ila
243
HG
9770
84
A. v
eron
ii bv
. sob
ria
27
HG
9770
85
A.
cav
iae
103
HG
9770
86
A. c
avia
e 21
6 H
G97
7087
A.
cav
iae
270
HG
9770
88
A. m
edia
17
9 H
G97
7089
A.
jand
aei
262
HG
9770
90
A. v
eron
ii bv
. sob
ria
269
HG
9770
91
A.
ver
onii
bv. s
obria
12
5 H
G97
7092
-- 2
40 --
Tab
le 7
.9
Con
tinue
d.
Gen
e Sp
ecie
s St
rain
no.
A
cces
sion
no.
Sp
ecie
s St
rain
no.
A
cces
sion
no.
flaA
A. b
estia
rum
68
H
G97
7093
A.
dha
kens
is
60
HG
9770
94
A.
dha
kens
is
67
HG
9770
95
A. d
hake
nsis
18
3 H
G97
7096
A.
dha
kens
is
176
HG
9770
97
A. d
hake
nsis
22
9 H
G97
7098
A.
hyd
roph
ila
92
HG
9770
99
A. h
ydro
phila
69
H
G97
7100
A.
hyd
roph
ila
261
HG
9771
01
A. h
ydro
phila
15
1 H
G97
7102
A.
hyd
roph
ila
231
HG
9771
03
A. c
avia
e 96
H
G97
7104
A.
ver
onii
bv. s
obria
23
7 H
G97
7105
A.
ver
onii
bv. s
obria
21
5 H
G97
7106
lafA
A.
dha
kens
is
95
HG
9771
07
A. d
hake
nsis
10
4 H
G97
7108
A.
dha
kens
is
220
HG
9771
09
A. m
edia
17
9 H
G97
7110
A.
ver
onii
bv. s
obria
26
9 H
G97
7111
A.
ver
onii
bv. s
obria
12
5 H
G97
7112
A.
ver
onii
bv. s
obria
66
H
G97
7113
A.
cav
iae
158
HG
9771
14
A.
cav
iae
109
HG
9771
15
A. c
avia
e 14
3 H
G97
7116
-- 2
41 --
Tab
le 7
.9
Con
tinue
d.
Gen
e Sp
ecie
s St
rain
no.
A
cces
sion
no.
Sp
ecie
s St
rain
no.
A
cces
sion
no.
lafA
A.
hyd
roph
ila
101
HG
9771
17
A. h
ydro
phila
34
H
G97
7118
A.
hyd
roph
ila
260
HG
9771
19
A. h
ydro
phila
13
3 H
G97
7120
aspA
A.
aus
tral
iens
is
266
HG
9771
21
A. d
hake
nsis
56
H
G97
7122
A.
dha
kens
is
230
HG
9771
23
A. d
hake
nsis
10
7 H
G97
7124
A.
hyd
roph
ila
34
HG
9771
25
A. h
ydro
phila
26
1 H
G97
7126
A.
hyd
roph
ila
69
HG
9771
27
A. h
ydro
phila
84
H
G97
7128
A.
hyd
roph
ila
149
HG
9771
29
A. h
ydro
phila
92
H
G97
7130
A.
jand
aei
262
HG
9771
31
A. sa
lmon
icid
a 19
9 H
G97
7132
A.
ver
onii
bv. s
obria
27
H
G97
7133
A.
ver
onii
bv. s
obria
25
9 H
G97
7134
A.
ver
onii
bv. s
obria
21
8 H
G97
7135
vasH
A.
dha
kens
is
31
HG
9771
36
A. d
hake
nsis
15
4 H
G97
7137
A.
dha
kens
is
70
HG
9771
38
A. d
hake
nsis
67
H
G97
7139
A.
jand
aei
35
HG
9771
40
A. ja
ndae
i 25
3 H
G97
7141
- 242 -
The primers used in the detection of aerA/haem can amplify several related genes which
encode toxins with a variety of names including aerolysin, aerolysin-haemolysin,
haemolysin-aerolysin, haemolysin, and cytolytic enterotoxin, hence the generic term
aerolysin-haemolysin genes (Soler et al. 2002). The prevalence of aerA/haem in A.
veronii bv. sobria detected in all (100%) isolates tested was also reported by Aguilera-
Arreola et al. (2007).
The prevalence of the ascV (16%) and aexT (13%) genes was low, consistent with other
reports (Aguilera-Arreola et al. 2005; Puthucheary et al. 2012; Senderovich et al. 2012).
In this study, these genes were more often detected in environmental than in clinical
isolates (ascV (39 vs. 8%; p < 0.0004; aexT 26 vs. 9%; p < 0.0295). Braun et al. (2002),
exclusively detected aexT in A. salmonicida ssp. salmonicida but not in other
Aeromonas spp. while Chacón et al. (2004) detected ascV and aexT in all intestinal and
extra-intestinal A. hydrophila and A. veronii isolates but only in a few extra-intestinal A.
caviae isolates. Based on these results, it appears that the distribution patterns of the
T3SS genes are strain and source dependent. The prevalence of the aspA gene (29%)
was low compared with the high frequency (75 to 77%), reported by Chacón et al.
(2003) and Puthucheary et al. (2012) who evaluated the distribution of virulence genes
and molecular characterization of Aeromonas species from Spain and Malaysia,
respectively. However, the prevalence of aspA in A. hydrophila (52%) isolates was
similar (58%) to the study by Aguilera-Arreola et al. (2005).
Lateral flagella (lafA) play an important role in cell adherence, invasion and biofilm
formation (Gavin et al. 2003). The presence of both genes (the flaA+lafA+ genotype) has
been associated with intense biofilm formation (Santos et al. 2010), a characteristic
feature of persistent infections. The frequency of the lafA gene (51%) was similar to the
overall frequency (60%) reported in mesophilic aeromonads by Gavin et al. (2003). In
other studies (Aguilera-Arreola et al. 2005, 2007; Senderovich et al. 2012), the
frequency of the lafA gene ranged from 37 to 41% although in one study (Aguilera-
Arreola et al. 2005), lafA was detected in 84% of A. hydrophila isolates. On the other
hand, the prevalence of the flaA (32%) gene was low compared to the range 59 to 74%
reported by others (Sen and Rodgers 2004; Puthucheary et al. 2012; Senderovich et al.
2012). In a recent study, flaA (94%) and lafA (71%) were highly prevalent in A. caviae
isolated from water, food and human faeces (Santos et al. 2010).
-- 243 --
No amplification products were detected for the virulence genes BfpA, BfpG, stx-1, and
stx-2. These virulence genes are rarely investigated and their prevalence among
Aeromonas from other locations needs to be evaluated. Sechi et al. (2002) detected the
BfpG gene in four out of 46 A. hydrophila isolates collected from water samples in
Sardinia, Italy. By contrast, BfpA was not detected in any isolate, consistent with results
from this study. There have been few reports of Aeromonas strains producing a Shiga-
like toxin or carrying the encoding genes (Haque et al. 1996; Alperi and Figueras 2010).
One such gene, stx-l, is plasmid-mediated and it is possible that in this study, strains
carrying the stx-1 may have been lost during storage. It is also possible that due to the
fact that primer design is based on the nucleotide sequence of one species, species-
specific variations in the gene sequences of the species evaluated resulted in failure to
amplify providing false negative results.
The vasH (Sigma 54-dependent transcriptional regulator) gene is a relatively recent
addition to the arsenal of virulence factors described in Aeromonas spp. Together with
vasK the gene is a component and/or is essential for expression of the T6SS. These
genes were found in the T6SS of the diarrhoeal isolate A. hydrophila SSU and in A.
hydrophila ATCC 7966T (Suarez et al. 2008). In the present study, vasH was detected
primarily among environmental (48%, 15/31) rather than in clinical (19%, 19/98)
strains.
Results from this study reveal that among the major species, A. hydrophila and A.
dhakensis contain more strains that possess multiple virulence genes compared to other
clinically relevant species like A. caviae and A. veronii bv. sobria. On the other hand,
strains from A. allosaccharophila and A. jandaei also harbour many virulence genes
suggesting that in Aeromonas the pathogenic potential may be strain rather than species
related. In the present study not many virulence genes were detected in A. caviae.
However, other studies suggest that this species should be considered an enteric
pathogen capable of harbouring several virulence determinants including the production
of a cholera-like and a Shiga-like toxin (Haque et al. 1996; Mokracka et al. 2001;
Alperi and Figueras 2010). It is also possible that variations in gene sequences are
responsible for lack of amplification in A. caviae.
This raises the question of how many and what virulence genes are essential for an
Aeromonas strain to cause infection. In general, pathogens should possess the necessary
virulence genes to gain entry, adhere, colonize, causing damage in host tissue while
-- 244 --
evading the host defence mechanisms, and in some cases spread, leading to systemic
infection. In Aeromonas, multiple virulence factors most likely work in concert (Yu et
al. 2005) where the product of one gene may facilitate the action of other genes or act
synergistically (Albert et al. 2000). Some authors observed that combinations or subsets
of virulence factors can be found among different isolates responsible for a wide range
of infections (Sen and Rodgers 2004; Puthucheary et al. 2012). Virulence genes such as
aerA, hlyA, alt, ast, act are thought to contribute to enteritis-related virulence (Janda and
Abbott 2010) while the severity of the diarrhoea has been associated with the number
and type of enterotoxin genes present (Albert et al. 2000; Chopra et al. 2009).
Enterotoxigenic aeromonads possessing both the alt and ast genes may represent true
diarrhoeal pathogens (Albert et al. 2000) although this hypothesis has not been
supported by others (Aguilera-Arreola et al. 2007) who suggested that aerolysin-
haemolysin may be sufficient to cause diarrhoea particularly in patients colonized with
A. caviae or A. veronii. The latter would explain the production of diarrhoea found
among patients from the present study infected with these species and lacking either alt
or ast. Moreover, aerA/haem and lafA are among the most predominant virulence genes
present in isolates from intestinal specimens suggesting that these genes may play an
essential role in the pathogenesis of aeromonads isolated from these sites. In this study,
with the exception of two cases, Aeromonas was the only recognized enteric pathogen
and no parasitic or mixed infections were recorded (Table 7.2).
The variable percentage identity found between the sequences of selected strains
compared to sequences deposited in GenBank for the nine genes has been previously
reported by others. The ASA1 protein secreted by the A. sobria 33, a human isolate and
the ASH3 produced by the fish isolate A. salmonicida 17-2 were found to be 66%
identical with aerolysin (Table 1.8) (Hirono et al. 1992; Hirono & Aoki 1993). On the
other hand, the cytotonic enterotoxin (Alt) produced by the human diarrhoeal isolate A.
hydrophila SSU showed 45 to 51% identity with phospholipase/lipase (Chopra et al.
1996). These results suggest that Aeromonas can produce a variety of extracellular
products that may be unique to specific strains. This is not surprinsing considering that
some Aeromonas strains can produce several enzymes with different biological
properties (Wretlind and Heden 1973; Honda et al. 1985; Howard and Buckley 1985;
Kozaki et al. 1987).
-- 245 --
The virulence genes investigated in this study represent a subset of the many virulence
factors described in Aeromonas, and the roles of only some of these genes have been
defined in the pathogenesis of aeromonads (Chopra et al. 2009). In this study, the only
gene found to be significantly more common in clinical than in environmental isolates
was lafA. Recently, Grim et al. (2013) used a combination of whole genome-sequence
and phenotypic assays to compare the virulence potential between two A. hydrophila
strains isolated from a patient with a polymicrobial wound infection. The more virulent
isolate harboured genes encoding for act, T3SS, flagella, haemolysins, capsule and a
homolog of exotoxin A found in Pseudomonas aeruginosa. The isolate was also lethal
to mice injected with a dose of 1 x 107 CFU. Thus a virulent pathotype of A. hydrophila
has now been identified and further genomic analysis is likely to reveal more distinct
pathotypes within the genus.
In this Chapter, 129 genotypically-characterized WA Aeromonas isolates of clinical and
environmental origin were examined for 13 putative virulence determinants to add to
the current body of knowledge on virulence-associated characteristics of Aeromonas.
This is the first study of this kind in Australia. Results from this study showed that the
distribution of these genes varies from strain to strain irrespective of the species and
source of isolation. Furthermore, this study reinforces the clinical relevance previously
attributed to A. dhakensis (as A. aquariorum or A. hydrophila ssp. dhakensis), a species
known to possess many virulence genes (Figueras et al. 2009; Sedláček, et al. 2012;
Puthucheary et al. 2012). Moreover, although clinical isolates belonging to A.
hydrophila and A. dhakensis can harbour many virulence genes, not all strains do so.
Genomic comparisons combined with phenotypic studies appear to be a suitable and
practical approach for the identification of virulent pathotypes in Aeromonas.
-- 246 --
-- 247 --
CHAPTER 8: GENERAL DISCUSSION
This thesis consists of several peer-reviewed publications in which the phenotypic,
genotypic, antimicrobial susceptibility profiles and the presence of several virulence
factors were investigated in a collection of Aeromonas isolated from human clinical
material, various water sources and fish samples. In addition, the taxonomic position of
an isolate recovered from irrigation water was investigated by extensive phenotypic and
genotypic testing leading to the proposal of a novel Aeromonas species.
Despite the ubiquitous nature of Aeromonas, a genus that has been associated with
infections in warm and cold-blooded animals including humans for more than a hundred
years, the lack of an animal model of infection has undermined the significance of this
genus as a true human pathogen. The failure of aeromonads to fulfil Koch’s postulates
has led bacteriologists to consider these bacteria opportunistic microorganisms rather
than recognized bona fide pathogens. This is highly surprising considering the
devastating impact that infection with these bacteria has caused to the aquaculture and
other related industries resulting in enormous financial loss (Kodjo et al. 1997; Nash et
al. 2006). In the past, the complex taxonomy of the genus undermined an understanding
of the potential pathogenic significance of Aeromonas, and their distribution. However,
the introduction of molecular methods has facilitated a more accurate differentiation of
the species. As a consequence, the real distribution of Aeromonas in all environments is
starting to emerge.
Therefore, the aims of this thesis were:
1. To determine the identity and distribution of local clinical and environmental
Aeromonas isolates by phenotypic and genotypic methods.
2. To introduce novel phenotypic methods and revisit older ones with the aim
to find new biochemical markers.
3. To examine the antimicrobial susceptibilities of local clinical and
environmental isolates.
4. To identify isolates with uncertain taxonomic positions
5. To investigate the presence of selected virulence genes among local clinical
and environmental isolates.
-- 248 --
Classification of Aeromonas isolates
This study began with the phenotypic classification of 199 Aeromonas isolates from
various clinical and environmental sources. Identification was based on a scheme
comprising more than 60 biochemical and physiological assays (Abbott et al. 2003).
Novel tests were introduced to find additional biochemical markers for an improved
identification. Overall, most isolates (93%) were identified to species level. Among the
clinical isolates, A. hydrophila (52.2%), A. caviae (19.0%) and A. veronii bv. sobria
(14.5%) accounted for 92% of the total isolates. This is in accordance with other studies
where together these species usually account for > 85% of the clinical isolates for this
genus (Altwegg and Geiss 1989; Abbott et al. 2003). Among water isolates, A.
hydrophila (46%) was the most common species followed by A. veronii bv. sobria
(22%). The high frequency of isolation of A. hydrophila supports the notion that the
frequency with which various species occur in clinical and environmental specimens,
are probably due to differences in the virulence potential of the strains (Janda et al.
1984; Barer et al. 1986; Kuijper et al. 1989b). It may also explain the reason why this
species has been the most studied aeromonad (Figueras 2005).
Earlier studies used numerical taxonomic techniques in combination with a large
number of biochemical characters to identify Aeromonas. However, no study was able
to characterize every isolate tested (Bryant et al. 1986a; Renaud et al. 1988; Kaznowski
et al. 1989; Käempfer and Altwegg 1992) reflecting the phenotypic homogeneity within
the genus. Nevertheless, in some studies, phenotypic identification in combination with
numerical taxonomy was able to produce discrete phenotypic clusters allowing the
recognition of two novel species (Miñana-Galbis et al. 2004, 2007). In this study,
identification of Aeromonas to the species level using biochemical methods was fraught
with difficulties including the low positivity rate of some tests, interpretation of end-
points, and the low number of strains representing environmental and infrequently
isolated species. Moreover, the introduction of novel tests in this study failed to provide
useful phenotypic markers further confirming that the identification of Aeromonas by
phenotypic methods is unreliable and some isolates are likely to be misidentified or
cannot be assigned to any definitive taxon (Figueras et al. 2007b; Ghatak et al. 2007b).
Following phenotypic classification, the genetic relationships of all isolates were
determined from gyrB and rpoD gene sequences. As a result, 99.5% of the strains re-
identified were placed in a taxon compared to 93% by the previous method. The new
-- 249 --
distribution indicated that in WA A. caviae, A. dhakensis, A. hydrophila and A. veronii
bv. sobria were the most prevalent species in clinical specimens accounting for 96% of
the total isolates. Moreover, the frequency of these species among human clinical
material was very similar with A. veronii bv. sobria (25%) slightly more prevalent than
A. caviae and A. dhakensis (both at 23.8%) and A. hydrophila (23%), respectively.
Thus, the difference in the frequency of isolation of A. hydrophila from clinical and
environmental specimens fell significantly from 52 to 19% (p < 0.0001) after genotypic
identification. These results provide strong evidence that the distribution of Aeromonas
species largely correlates with the identification method employed. The high prevalence
of A. dhakensis in this study has been reported in recent studies suggesting that this
species is globally distributed in clinical specimens (Figueras 2005; Puthucheary et al.
2012; Wu et al. 2012).
Misidentification of isolates may also explain the phenotypic heterogeneity previously
associated with A. hydrophila, A. caviae and A. veronii (Miyata et al. 1995; Graf 1999a;
Korbsrisate et al. 2002; Abbott et al. 2003). It is also possible that among Aeromonas
species different ecotypes capable of exploiting a specific ecological niche exist.
Ecotypes have been described among strain that exhibit higher than 99% average
nucleotide identity (ANI) although the gene content of strains of the same species can
vary up to 30%. This difference begs the question of whether these strains should
belong to the same species (Konstantinidis and Tiedje 2005). Future studies designed to
compare the gene content between clinical and environmental isolates using ANI as a
tool may be forthcoming. Thus, this study contributes to an important knowledge about
the frequency of Aeromonas species in WA indicating that a more accurate distribution
of the genus is beginning to emerge.
The description of Aeromonas australiensis sp. nov.
In Chapter 4, the position of strain 266 inferred from the gyrB and rpoD gene sequences
showed that this isolate formed a separate line of descent from all other species in the
genus. Furthermore, the inability of the strain to produce acid from D-mannitol was
significant as most species in the genus do so. Subsequent extensive phenotypic and
genotypic testing confirmed that strain 266T indeed represented a novel Aeromonas
species (Aravena-Román et al. 2013). Proposing new species based on a single strain
has been a source of controversy among bacteriologists. This situation has led some
authors to recommend that the Bacteriological Code be revised and that a minimum
-- 250 --
number of standard tests and strains should be included in the description of new
species (Christensen et al. 2001; Janda and Abbott 2002) of which genotypic methods
should be mandatory (Figueras et al. 2006). However, there are a few drawbacks with
these recommendations. Firstly, it may take a very long time to collect the minimum
number of strains recommended from geographically and epidemiologically unrelated
areas. Secondly, strains may be lost in storage or simply forgotten in culture collections.
Thirdly, sequences from nearly every bacterial species have been placed on GenBank
and are readily available for comparison. The latter point is reinforced by the recent
isolation of A. simiae following a survey to determine the prevalence of Aeromonas in
slaughterhouses in northern Portugal. The strain was isolated among 703 isolates and
was identified on the basis of 16S rDNA, gyrB and rpoD sequencing (Fontes et al.
2010). Aeromonas simiae was first described on the basis of two strains isolated from
faeces of healthy monkeys (M. fascicularis) from Mauritius (Harf-Monteil et al. 2004).
A second study recently reported that A. taiwanensis constituted 6% of the Aeromonas
species isolated from diarrhoeal stools in Israel. In this study, identification of the
isolates was based on the sequences of the rpoD gene (Senderovich et al. 2012). The
original description of A. taiwanensis was based in a single strain recovered from an
infected burn wound of a 40 year-old male from Taiwan (Alperi et al. 2010b).
These findings suggest that A. australiensis may be isolated by others in future studies.
Isolation of A. australiensis outside Australia would indicate a global distribution of the
species while isolation within Australia would suggest that the species is indigenous to
this region only. The discovery of A. australiensis from irrigation water is a significant
contribution to the understanding of the global distribution of this genus and adds to the
list of new aeromonads described in the last 14 years. This increasing number of new
Aeromonas species also coincided with the rapid increase of new bacterial species
described over the same period of time (Janda and Abbott 2010). Furthermore, the
recognition of a novel species reinforces the notion that accurate identification of these
bacteria must include a molecular approach.
Antimicrobial susceptibility
The antimicrobial susceptibility patterns of Aeromonas determined in this study indicate
that the number of multi-drug resistance strains found locally is extremely low. In
contrast to other reports, no Aeromonas strain isolated in WA was found to carry
resistance mechanisms such as ESBLs or the presence of MBLs (Rasmussen and Bush
-- 251 --
1997; Neuwirth et al. 2007; Libisch et al. 2008; Wu et al. 2012). All isolates tested in
this study were exquisitely susceptible to the fluoroquinolones ciprofloxacin and
norfloxacin (100%) while resistance to nalidixic acid was very low (3.1%). The latter
result is in sharp contrast with the high rates of resistance to nalidixic acid reported by
Rhodes et al. (2000) who observed resistance to nalidixic acid in 94% of human derived
and 52% of aquaculture aeromonads. Similarly, Figueira et al. (2011) reported
resistance to this antimicrobial agent in 90.6% of waste water and 17.6% of surface
water isolates. In Taiwan, resistant to fluoroquinolones is emerging where up to 14% of
Aeromonas showed tolerance to this antimicrobial class (Wu et al. 2007). On the other
hand, resistance to tetracycline in WA aeromonads is low (<6%) whereas reports from
Asia suggest that up to 49% of the isolates can be resistant to this antimicrobial class
(Chang and Bolton 1987; Ko et al. 1996).
Based on the low antimicrobial resistance exhibited by environmental aeromonads
consisting primarily of strains isolated from water samples it is safe to suggest that
water is not an ecological niche for resistance mechanisms in WA. By contrast, reports
from several locations reveal that multi-resistant Aeromonas strains can be found among
water and foods sources (Goñi-Urriza et al. 2000; Rhodes et al. 2000; Nawaz et al.
2010; Esteve et al. 2012). In one study, consumption of contaminated water was
implicated in serious infections caused by ESBL-producing Aeromonas (Rodríguez et
al. 2005). Furthermore, the high susceptibility nature of environmental strains to most
antimicrobial classes reported in this study suggests that clinical strains may act as a
potential reservoir for resistance mechanisms. This is consistent with previous
observations that suggested that resistant strains isolated from clinical samples may
release compounds into the environment and provide a source of constant selection that
maintains pressure for populations of resistant strains (Davies and Davies 2010). Thus,
results from this and other studies confirm that variations in the antimicrobial profiles
exist in Aeromonas strains isolated from different locations.
From the clinical point of view, the presence of aeromonads in human clinical material
may impact patient management as incorrect empirically therapy has been administered
in a significant number of cases involving Aeromonas (Scott et al. 1978; Vila et al.
2002; Bravo et al. 2003; Figueras 2005). The overall susceptibility profile of
Aeromonas was deemed to be stable during the decade mid-1980s to mid-1990s (Janda
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and Abbott 2010), a trend that appears to continue in this region as indicated by this
study.
There were 11 isolates with a multi-resistant profile. One was isolated from water, two
from diseased fish and the rest from human clinical material. Of these, only one
exhibited resistance to the aminoglycosides, 3rd generation chephalosporins, lower
concentration cefepime but was susceptible to meropenem, fluoroquinolones, amikacin
and high concentration of cefepime. The remaining resistant isolates were invariably
susceptible to the fluoroquinolones while the majority were also susceptible to the
aminoglycosides, meropenem and 3rd and 4th generation cephalosporins. From the
clinical point of view, clinicians still have more than one choice of antimicrobials at
their disposal to treat these resistant isolates. In conclusion, this research provides
significant information about the antimicrobial resistance patterns of local clinical
Aeromonas species and may guide clinicians to implement correct antimicrobial
therapy. That is, if Aeromonas spp. are suspected or proven, then antimicrobials such as
fluoroquinolones, aminoglycosides, carbapenems, 3rd and 4th generation cephalosporins
can be safely administered.
Distribution and significance of virulence genes
In this study, the pathogenic potential of 129 genotypically-characterized isolates
comprising 11 Aeromonas species was evaluated by detecting the presence of 13
virulence genes using a PCR-based method. Of these, 98 isolates were of clinical origin
and 31 derived primarily from water and fish samples. Aeromonas was the sole
aetiological agent in 60% of the cases while the remining 40% were isolated with
another pathogen or as part of a polymicrobial bacterial population. The majority (17,
85%) of the isolates recovered from stools were from symptomatic patients who had
watery diarrhoea or loose faeces and in some cases blood and leucocytes were present in
the specimen. These parameters are usually associated with gastroenteritis. Although no
clinical data was obtained in 31% of the clinical cases, Aeromonas was the only
microorganism isolated in most (26, 84%) while 5 (16%) cases were polymicrobial.
Strains isolated from fish derived mainly from diseased animals.
Overall, the majority of the isolates (96%) harboured at least one virulence gene
compared to 65% of the total isolates from another study (Kingome et al. 1999). The
number of virulence genes found in multidrug resistant isolates ranged from 1 to 4 with
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one isolate not included in the virulence study. These isolates were no more pathogenic,
in terms of virulence genes detected, than others in the study. Therefore, there was not a
relation between the most virulent strains and their antibiotic profile found. Results
from this and other studies from locations as diverse as Mexico, Spain, Bangladesh,
Italy, USA and Israel (Albert et al. 2000; Sechi et al. 2002; Sen and Rodgers 2004;
Aguilera-Arreola et al. 2007; Senderovich et al. 2012) indicate that the distribution of
virulence genes among the species is highly variable. Comparison between studies is
difficult due to the number of isolates tested, source of isolation, identification method
used to characterize isolates and choice of virulence genes (Sechi et al. 2002; Chacón et
al. 2003; Wu et al. 2007). Some studies were designed to evaluate the virulence
potential of different strains of the same species (Soler et al. 2002; Yu et al. 2005) while
others targeted the detection of a single virulence gene from several species (Chacón et
al. 2003; Yu et al. 2004). A recent study from Malaysia evaluated the pathogenic
potential of 94 genotypically-characterized clinical isolates comprising five species by
detecting the prevalence of 10 virulence genes (Puthucheary et al. 2012). Of these, only
six (aerA, alt, ast, flaA, aspA and aexT) virulence genes were common with those used
in this study. The prevalence of aerA and alt within the major species was remarkable
similar with the present study while the prevalence of the remaining four genes differed
significantly depending on the gene and the species.
In this study, aerA/haem was highly prevalent in WA isolates while the remaining
virulence genes were randomly distributed among the species. And although many
isolates harboured multiple virulence genes, not a single strain carried the full
complement of the 13 virulence genes. Several virulence genes including alt, aspA,
vasH, ascV and aexT were more prevalent in environmental rather than in clinical
isolates. These differences were statistically significant and suggested that
environmental isolates may represent a reservoir of potentially pathogenic strains. Any
discernible virulence pattern present is tenuous and evidence from this study does not
support that each species carried distinct sets of genes as reported by others (Kirov et al.
2002; Aguilera-Arreola et al. 2007; Puthucheary et al. 2012). In addition to A.
dhakensis and A. hydrophila, strains from A. allosaccharophila and A. jandaei also
harboured multiple virulence genes. The presence of multiple virulence genes or other
virulence factors in less frequently isolated species suggest that strains from these
species are potentially pathogen (Soler et al. 2002; Chacón et al. 2003; Senderovich et
al. 2012).
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Although no single or combination of virulence factors has been unequivocally
correlated to virulence in Aeromonas (Aguilera-Arreola et al. 2007), the presence of
T3SS and toxin genes in clinical strains would elevate Aeromonas to the same category
as the primary pathogens Y. enterocolitica, Salmonella enterica, enteropathogenic E.
coli and Shigella flexnery (Chacón et al. 2004). The high prevalence of aerA/haem
(81%) in clinical isolates suggests that strains possessing this virulence gene are
potentially pathogenic and may be diarrhoeagenic in vivo (Janda and Abbott 2010) as
both aerA and hlyA are considered virulence markers for Aeromonas (Heuzenroeder et
al. 1999; González-Serrano et al. 2002). Thus, despite the low number of virulence
genes detected among A. veronii bv. sobria isolates, the pathogenic potential previously
attributed to this species (Daily et al. 1981; Janda et al. 1985; Janda and Kokka 1991;
Kirov and Hayward 1993; Lye et al. 2007) should be maintained as every strain (100%)
harboured the aerA/haem gene. It is also possible that the action of this toxin alone may
account for the infectious process associated with strains harbouring aerA/haem in this
study. Similarly, while the frequency of isolation and clinical relevance previously
attributed to A. hydrophila has been overestimated (Figueras et al. 2009), isolation of
this species from serious human infections continuous to grow. In a recent report, A.
hydrophila was recovered from a posttraumatic brain abscess following a head injury
and was described as an aggressive pathogen (Mahabeer et al. 2014). Unfortunately, the
isolate was identified by a commercial system without further confirmation by a
molecular method. Nevertheless, this case reinforces the pathogenic potential attributed
to this species in particular and to Aeromonas in general.
The low number of virulence genes detected in A. caviae was consistent with previous
reports and has been one of the main reasons to consider this species less pathogenic
than A. veronii and A. hydrophila (Honda et al. 1985; Kirov et al. 1986; Majeed et al.
1990; Eley et al 1993; Martins et al. 2002). A lack of virulence genes is contrary to the
notion that the presence of high number of virulence genes is associated with a high
pathogenic potential among Aeromonas strains (Nawaz et al. 2010). However, growing
evidence suggests that A. caviae should be considered a bona fide pathogen. Firstly, A.
caviae strains can possess virulence factors considered to be significant in the
pathogenesis of Aeromonas-associated infections (Callister and Agger 1987; Gray et al.
1990; Namdari and Bottone 1990b; Deodhar et al. 1991; Singh and Sanyal 1992b;
Kirov and Hayward 1993; Shaw et al. 1995; Wang et al. 1996; Mokracka et al. 2001;
Ghatak et al. 2006; Krzymińska et al. 2003, 2011). Secondly, the pathogenic potential
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of A. caviae is enhanced by animal passage suggesting that expression of virulence
genes may be reactivated in genes that were previously repressed (Singh and Sanyal
1992c; Krzymińska et al. 2003). Thirdly, the predominance of A. caviae in diarrhoeal
stools from neonates and children with gastroenteritis is further evidence that A. caviae
should be considered a true enteric pathogen (Altwegg and Geiss 1989; Namdari and
Bottone 1990b; Pazzaglia et al. 1990a; Moyer et al. 1991; Wilcox et al. 1992; Albert et
al. 2000; Rabaan et al. 2001; Bravo et al. 2012; Senderovich et al. 2012). Evidence now
exists for water-to-human transmission by members of the A. caviae-A. media group
(Khajanchi et al. 2010). Fourthly, A. caviae has been implicated in serious human
infections affecting immunocompetent individuals (Kumar et al. 2012). This would also
support the notion that to date, there is no consensus as to which virulence factor(s) is
the most critical for human infections (Chakraborty et al. 1987) and that a hierarchical
classification of virulence factors for Aeromonas does not exist or cannot, at this stage,
be established (Aguilera-Arreola et al. 2007).
Predicting virulence of Aeromonas isolates based on changes in transcription of c-jun
and c-fos in human tissue culture cells has been recently proposed (Hayes et al. 2009)
and although detection of virulence genes can be used to determine the pathogenic
potential of Aeromonas, this method only demonstrates that some virulence genes are
present in some strains but not in others. Instead, the study by Grim et al. (2013)
demonstrated that genotypic differences correlated with functional virulence factor
assays and allowed to identify a virulent pathotype of A. hydrophila capable of causing
wound infections in humans. This study offers several advantages over the detection of
virulence genes or the detection of virulence products by bioassays alone. Taken
together, these observations suggest that the combinations of methods used by Grim et
al. (2013) should be considered the standard method to evaluate the pathogenic
potential of Aeromonas species and that a library of truly pathogenic strains should be
created as previously proposed (Janda and Abbott et al. 2010).
CONCLUSIONS
The characterization of a large collection of clinical and environmental isolates indicate
that in Western Australia the species A. veronii bv. sobria, A. dhakensis, A. caviae and
A. hydrophila are the most prevalent. Characterization of isolates by genotypic methods
is also likely to identify less frequently isolated species including A. allosaccharophila,
-- 256 --
A. salmonicida, A. bestiarum, A. jandaei, A.media, A. schubertii and uncover potentially
novel species. From the clinical point of view, the antimicrobial susceptibilities
determined in this study provide clinicians with several choices of antimicrobials to
empirically initiate therapy if Aeromonas are suspected to be present. The detection of
clinical and environmental isolates harbouring multiple virulence genes among several
Aeromonas species contributes to the current knowledge on the virulence of these
bacteria. Finally, data from this and other studies suggest that the pathogenic potential
in Aeromonas is probably strain- rather than species-dependent.
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Evolutionary distances based on the percentage sequence dissimilarities of all current Aeromonas species and 60 isolates identified as A. dhakensis (A. aquariorum) using Clustal W and Mega 5 software (combined gyrB and rpoD dissimilarities). Numbers in brackets indicate strains with similar nucleotide sequences.
Evolutionary distances based on the percentage sequence dissimilarities of current Aeromonas and strain 266T using Clustal_W and Mega 4 software (combined gyrB and rpoD dissimilarities)