Myxobolus myleus n. sp. infecting the bile of the Amazonian freshwater fish Myleus rubripinnis (Teleostei: Serrasalmidae): morphology and pathology

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Systematic ParasitologyAn International Journal ISSN 0165-5752Volume 82Number 3 Syst Parasitol (2012) 82:241-247DOI 10.1007/s11230-012-9360-0

Myxobolus myleus n. sp. infecting the bileof the Amazonian freshwater fish Myleusrubripinnis (Teleostei: Serrasalmidae):morphology and pathology

Carlos Azevedo, Sérgio Carmona SãoClemente, Graça Casal, Patrícia Matos,Ângela Alves, Saleh Al-Quraishy &Edilson Matos

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Myxobolus myleus n. sp. infecting the bile of the Amazonianfreshwater fish Myleus rubripinnis (Teleostei:Serrasalmidae): morphology and pathology

Carlos Azevedo • Sergio Carmona Sao Clemente •

Graca Casal • Patrıcia Matos • Angela Alves •

Saleh Al-Quraishy • Edilson Matos

Received: 29 December 2011 / Accepted: 8 March 2012

� Springer Science+Business Media B.V. 2012

Abstract Myxobolus myleus n. sp. is described from

the gall-bladder of the freshwater fish Myleus rubri-

pinnis collected near the city of Oriximina in the

Amazon System, Brazil. The spores obtained from the

bile contained two equal symmetrical and smooth

valves, each forming the spore wall. The spores were

large, with a cone-like form, a semi spherical basal

contour and measured (in lm) 19.3 ± 0.5 (n = 25) 9

8.3 ± 0.5 (n = 25) 9 4.0 ± 0.3 (n = 15). The apical

end of the spores contained two elongate, equal and

pointed conical polar capsules measuring 13.2 ± 0.4

lm (n = 25) in length and 3.0 ± 0.3 lm (n = 15) in

width, each having a slightly tapering polar filament

with 19 to 21 turns. The polar capsules were extended

below at about 4/5 of the total length of the spores. The

sporoplasm was binucleate and contained some sporo-

plasmosomes. All infected fish presented hypertrophy

of the gall-bladder due to presence of the brownish

parasite floating in the bile. In this paper we describe

this new species of myxosporean based on light and

ultrastructural observations, together with its associ-

ated pathology.

Introduction

Myxozoans infecting freshwater and marine fishes

represent an important pathogenic group with a

C. Azevedo (&) � G. Casal � A. Alves

Department of Cell Biology, Institute of Biomedical

Sciences (ICBAS/UP), Rua Jorge Viterbo Ferreira, 228,

4050-313 Porto, Portugal

e-mail: [email protected]

C. Azevedo � G. Casal � A. Alves

Laboratory of Pathology, Centre for Marine

Environmental Research (CIIMAR/UP), Rua Jorge

Viterbo Ferreira, 228, 4050-313 Porto, Portugal

S. C. Sao Clemente

Laboratory of Inspection and Technology of Food,

Faculty of Veterinary, Fluminense Federal University,

Niteroi, Rio de Janeiro, Brazil

G. Casal

Department of Sciences, High Institute of Health

Sciences-North (CESPU), Gandra, Portugal

P. Matos

Edilson Matos Research Laboratory, Federal University of

Amazonia, Belem, Brazil

S. Al-Quraishy

Zoology Department, College of Science, King Saud

University, Riyadh, Saudi Arabia

E. Matos

Carlos Azevedo Research Laboratory, Federal Rural

University, Belem, Brazil

123

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DOI 10.1007/s11230-012-9360-0

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worldwide distribution (Eiras et al., 2005b; Lom &

Dykova, 2006). Among the myxosporidians, species

of Myxobolus Butschli, 1882, one of the largest genera

in the family Myxobolidae Thelohan, 1892 (Lom &

Dykova, 2006), have been reported as important

pathogens of freshwater and marine fishes (Kent

et al., 2001).

Two synopses listed the different Myxobolus spp.,

one reporting 744 species parasitising fishes (Eiras

et al., 2005b) and, more recently, another reporting

792 nominal species of this genus, including seven

infecting amphibians (Lom & Dykova, 2006). At

about the same time, Adriano et al. (2006) described

M. cuneus Adriano, Arana & Cordeiro, 2006 infecting

several organs (among them the gall-bladder) from the

Brazilian fauna. More recently, Eiras et al. (2010)

described M. franciscoi Eiras, Monteiro & Brasil-

Sato, 2010 infecting the connective tissues of the fins

and included a revision of Myxobolus species from

South America, listing a further eight new species.

This number has continued to increase over the years

due to the description of new species in different South

American countries, especially Brazil (Adriano et al.,

2009a,b; Azevedo et al., 2010, 2011). The little that is

known about these parasites from South American

freshwater fishes comes mainly from studies of

Brazilian fishes (Molnar & Bekesi, 1993; Casal

et al., 1996, 2002, 2006; Eiras et al., 2005a, 2010;

Adriano et al., 2006, 2009a,b; Martins & Onaka, 2006;

Azevedo et al., 2009, 2011, 2012).

The present paper describes a new myxosporidian

species belonging to Myxobolus which infects the

gall-bladder of the Amazonian fish Myleus rubri-

pinnis (Muller & Troschel), including some light and

ultrastructural observations of the spores and its

histopathology.

Materials and methods

Twenty five specimens (10 males and 15 females) of

the freshwater fish Myleus rubripinnis, which is of

great regional commercial importance, were collected

in the Sapurua Lagoon (01�240S, 55�590W). This

lagoon is in the Amazonian system near the city of

Oriximina (Para State), Brazil and located c.770 km

upstream from the mouth of the Amazon and c.550 km

downstream from the city of Manaus. The specimens

were maintained in an aquarium under good

ecological conditions for 3–5 days. Small fragments

of infected gall-bladder and bile were examined in

squash preparations. These fragments of the infected

organ and isolated spores were examined using

differential interference contrast optics and transmis-

sion electron microscopy (TEM). For TEM, small

fragments of gall-bladder wall and free spores

obtained from bile were fixed in 5% glutaraldehyde

in 0.2 M sodium cacodylate buffer (pH 7.2) for

10–12 h at 4�C, washed in the same buffer for 10 h

at 4�C, and post-fixed in 2% OsO4 buffered with 0.2 M

sodium cacodylate for 3 h at the same temperature.

The material was dehydrated in an ascending ethanol

series, followed by propylene oxide, before embed-

ding in Epon. Semithin sections were stained with

methylene blue, and the ultrathin sections, double

contrasted with uranyl acetate and lead citrate, were

observed in a JEOL 100CXII TEM operated at 60 kv.

Results

Gall-bladders and the bile of nine specimens of the

freshwater fish Myleus rubripinnis were infected by a

myxosporean identified as belonging to Myxobolus

Butschli, 1882, because the spores presented the

characteristics of this genus and lacked projections.

The spores are conical in form, comprise two equal

valves and have a hemispherical basal aspect in

valvular view and are biconvex in sutural view. They

contain two elongate, pyriform polar capsules (PCs)

and a binucleate sporoplasm (Lom & Dykova, 2006).

Based on the morphological and ultrastructural

aspects of the spores and their host-specificity, we

propose the establishment of a new species classified,

according to Lom & Dykova (2006), as follows:

Phylum Myxozoa Butschli, 1882; Class Myxosporea

Butschli, 1881; Order Bivalvulida Shulman, 1959;

Family Myxobolidae Thelohan, 1892; Genus Myxo-

bolus Butschli, 1882.

Myxobolus myleus n. sp.

Type-host: Myleus rubripinnis Muller & Troschel

(Teleostei, Serrasalmidae) (the ‘redhook silverdollar’;

Brazilian common name ‘pacu-anhanga’).

Type-material: A microscope slide with the hapanto-

type was deposited in the International Myxozoa

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Collection of the Instituto Nacional de Pesquisa da

Amazonia - INPA, Manaus, Brazil (INPA no. 011/12).

Type-locality: Sapurua Lagoon (01�240S, 55�590W) in

the Amazon System located near the city of Oriximina

(Para State), c.770 km upstream from the mouth of the

Amazon and c.550 km downstream from the city of

Manaus, Brazil.

Site: The spores were floating in the bile. No other

organs or tissues were infected by this species.

Prevalence: In 9 of 25 fishes (36%) [3/10 (30%) for

males, 6/15 (40%) for females].

Etymology: The specific epithet ‘myleus’ is derived

from the generic name of the host species. It is to be

treated as a noun.

Pathology: The infection was macroscopically char-

acterised by hypertrophy of the gall-bladder (the only

infected organ), which exhibited bile with a brownish

colour. The more heavily infected gall-bladders gen-

erally presented bile, containing numerous free spores,

which appeared to be under an abnormally high

pressure.

Description (Figs. 1–7)

Mature spores were present floating in the bile

(Fig. 1). These contained 2 equal conical valves which

have a semi-spherical basal aspect in valvular view

and biconvex aspect in sutural view. The spores were

Figs. 1–6 Morphological and ultrastructural aspects of Myxobolus myleus n. sp. infecting the bile of the Amazonian fish Myleusrubripinnus. 1. Free mature spore observed in frontal view with DIC. 2. Ultrastructural view of a longitudinal section of a spore

observed in lateral section, showing the spore wall (W) and the suture line (arrows), one of the two polar capsules (PC), different

sections of the polar filament (arrowheads) and the sporoplasm (Sp). 3. Ultrastructural detail of a longitudinal section of the apical

region of the polar capsule, showing the arrangement of the polar filament (PF). 4, 5. Two ultrastructural views of transverse sections of

the polar capsules (PC) at two different levels: (4) in the apical region (arrows) and (5) in the middle. 6. Ultrastructural details of a

longitudinal section in the middle and basal region of a polar capsule (PC), showing different sections of the polar filament (PF). Scale-

bars are in lm

Syst Parasitol (2012) 82:241–247 243

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19.3 ± 0.5 (19–20) long (n = 25) 9 8.3 ± 0.5

(7.5–9) wide (n = 25) 9 4.0 ± 0.3 (3.5–4.5) lm

thickness (n = 15) (Figs. 1–4). The 2 polar capsules

(PCs) were equal in size, pyriform, elongated, pointed

apically, circular in cross-section and convergent

towards the apex of the spore (Figs. 1–5, 7). The

apical region of the PCs was plugged by a stopper

projecting towards the internal face of the spore wall

(Figs. 2, 3). The PCs, which extend up to about 4/5 of

the total length of the spores, were 13.2 ± 0.4

(12.5–13.5) lm in length (n = 25) and 3.0 ± 0.3

(2.5–3.5) lm in width (n = 15), with the polar

filament (PF) having 19 to 21 coils and orientated

obliquely to the longitudinal axis of the PC at an angle

of 72–76� (Figs. 4–6). The binucleate sporoplasm

contained some sporoplasmosomes. A diagrammatic

illustration of a spore, based on both LM and TEM

observations, is presented in Fig. 7.

Discussion

The morphology of the myxosporidian spores

described in this paper exhibits all the characteristics

of Myxobolus Butschli, 1882 (family Myxobolidae),

the species of which are pathogens of several organs of

freshwater and marine fishes (Eiras et al., 2005b, 2010;

Lom & Dykova, 2006). About 790 species of Myxo-

bolus have been reported; however, only 38 species

were reported to infect the gall-bladder of these fishes

and these were mainly in China and other Asian

countries (Eiras et al., 2005b). Of this number, only a

single species (M. latipinnacola Wold & Iverson,

1978) had been reported to infect the gall-bladder of

the fishes in the Americas (Wold & Iverson, 1978).

However, a new species, M. cuneus, infecting the gall-

bladder of Piaractus mesopotamicus in Brazil has

more recently been described and with ultrastructural

details (Adriano et al., 2006), but the great majority of

the species of this genus have been illustrated only by

light microscopical observations and diagrammatic

representations of the spores, which make comparison

difficult (Molnar et al., 1993; Eiras et al., 2005a, 2007,

2010; Lom & Dykova, 2006; Martins & Onaka, 2006).

The main criteria for comparison between the

different Myxobolus spp. are spore shape and mea-

surements and PC shape, measurements and the

internal arrangements of the PF (i.e. the number of

coils and their position in relation to the PC axis).

Another feature is the location of the parasite;

Myxobolus spp. have been reported as histozoic

parasites infecting various tissues in freshwater fishes

and coelozoic plasmodia are a common developmen-

tal phase of numerous myxoporean species (Lom &

Dykova, 2006; Eiras et al., 2010, 2011; Rocha et al.,

2011).

As indicated above, only M. cuneus has been

described as coelozoic, infecting, among other organs,

the gall-bladder of a Brazilian fish (Adriano et al.,

2006). Several LM and TEM studies of coelozoic

plasmodia of different myxosporean species have

Fig. 7 Diagrammatic illustration of a mature spore of Myxo-bolus myleus n. sp., showing the spore morphology and its

different organelles and structures

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shown them to be attached by some kind of branching

processes and flattened against the epithelial cells of

the host (Canning et al., 1999; Rocha et al., 2011).

Unfortunately, the present study does not include

morphological aspects of the plasmodia, because this

stage of the development was never observed. This

situation was certainly the result of the fact that only

one fish was studied, possibility in an unfavourable

seasonal period for plasmodial development. The

development of plasmodia is known to occur in

various myxosporean species during different sea-

sonal periods (Canning et al., 1999; Rocha et al.,

2011).

When comparing the present results with those of

other Myxobolus spp. described from the fishes of the

South American fauna, we observed several morpho-

logical differences in the shape and dimensions of the

spores and PCs, as well as in the number, position and

organisation of the PF coils (Molnar & Bekesi, 1993;

Molnar et al., 1998; Adriano et al., 2002; Viozzi &

Flores, 2003; Eiras et al., 2005a, 2007; Tajdari et al.,

2005).

The species M. inaequus Kent & Hoffman, 1984,

M. absonus Cellere, Cordeiro & Adriano, 2002

and M. desaequalis Adriano, Arana, Ceccarelli &

Cordeiro, 2002 were excluded as being conspecific

with the new taxon, because they possess two unequal

PCs (Kent & Hoffman, 1984; Cellere et al., 2002;

Azevedo et al., 2002).

Comparing the morphology and measurements of

the spores and the dimensions and arrangement of the

PCs in different species of Myxobolus with equal-sized

PCs, we observed that M. maculatus Casal, Matos &

Azevedo, 2002 is morphologically most similar to

M. myleus n. sp. (see Casal et al., 2002). However,

there are some specific differences (Table 1). The

spores of M. myleus are smaller in length and

thickness, and have a greater number of PF coils

(19–21 vs 14–15). Furthermore, the PC coils of

M. myleus are orientated obliquely (72–76�) to the

longitudinal axis of the PCs, whereas in M. maculatus

the plane of the coils is perpendicular to the PC axis. In

comparison with M. cuneus, the spores of M. myleus

are larger in all dimensions and have a greater number

of PF coils (19–21 vs 8–9) which are oriented

obliquely rather than perpendicular to the axis of the

capsules. When comparing the spores of the all other

Myxobolus spp. with equal PCs, it was determined that

none of the spore and PC measurements were the same

as those of the new species. Furthermore, M. cuneus

and M. myleus are the only described species of

Myxobolus which infect the gall-bladder and bile of

South American fishes; in fact, the spores of virtually

all other species of this genus infect other organs of the

body (Eiras et al., 2005b, 2010; Lom & Dykova,

2006).

These morphological differences, in addition to the

host species and the site of infections, appear sufficient

arguments to consider Myxobolus myleus as new to

science.

Acknowledgements We thank Joana and Joao Carvalheiro

(ICBAS/UP) for their excellent photographic assistance and

Manoel Newton Souza, a technician from the Campus of the

UFF in Oriximina (Brazil), who provided the access to different

sites on the Amazon River and for help with the collection of fish

samples. This work complies with the current laws of the

countries in which it was performed and was supported by the

Fundacao Eng. Antonio de Almeida (Porto, Portugal), CNPq

and CAPES (Brazil) and a Visiting Professorship at King Saud

University (Riyadh, Saudi Arabia). We would also like to thank

the referees for their comments and suggestions.

Table 1 Comparative measurements (in lm) of the spores of Myxobolus myleus n. sp. and two other similar South American species

of Myxobolus

Myxobolus spp. (Site of

infection)

Host (Family) SL SW ST PCL PCW PFc Reference

M. maculatus (Kidney) Metynnis maculatus (Characidae) 21.0 8.9 7.5 12.7 3.2 14–15 Casal et al. (2002)

M. cuneus (Gall-bladder and

others)

Piaractus mesopotamicus(Characidae)

10.0 5.7 1.7 5.7 1.7 8–9 Adriano et al.

(2006)

M. myleus n. sp. (Bile) Myleus rubripinnis(Serrasalmidae)

19.3 9.1 4.0 13.2 3.0 19–21 Present study

Abbreviations: SL, spore length; SW, spore width; ST, spore thickness; PCL, polar capsule length; PCW, polar capsule width; PFc,

polar filament coils

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