[REVIEW]: Unusual fungal niches

Unusual fungal niches

S.A. Cantrell1

School of Science and Technology, Universidad delTurabo, P.O. Box 3030, Gurabo, Puerto Rico 00778

J.C. DianeseInstituto de Ciencias Biologicas, Universidade deBrasılia, Campus Darcy Ribeiro, 70910-900, Brasılia,DF, Brazi

J. FellRosenstiel School of Marine and Atmospheric Science,4600 Rickenbacker Causeway, Miami, Florida 33149

N. Gunde-CimermanP. Zalar

Biotechnical Faculty, Department Biology, University ofLjubljana, Vecna pot 111, 1000 Ljubljana, Slovenia

Abstract: Fungi are found in all aerobic ecosystems,colonizing a diversity of substrates and performing awide diversity of functions, some of which are not wellunderstood. Many species of fungi are cosmopolitanand generalists but others are specialists found only inrestricted substrates or habitats. Unusual fungalniches are habitats where extreme conditions wouldbe expected to prevent the development of amycobiota. In this review we describe five unusualfungal habitats in which fungi occupy poorly under-stood niches: Antarctic dry valleys, high Arcticglaciers, salt flats and salterns, hypersaline microbialmats and plant trichomes. Yeasts, black yeast-likefungi, melanized filamentous species as well asrepresentatives of Aspergillus and Penicillium seemto be dominant among the mycobiota adapted to coldand saline niches. Plant trichomes appear to be aunique niche, harboring many previously unknowntaxa. The advent of new sequencing technologies ishelping to elucidate the microbial diversity in manyecosystems, but more studies are needed to documentthe functional role of fungi in the microbialcommunities thriving in these unusual environments.

Key words: dry valleys, glaciers, microbial mats,plant trichomes, salt flats, salterns

INTRODUCTION

One paradigm in microbial ecology is the idea that‘‘microbes are everywhere but the environmentselects.’’ We know now that some microbial species

exhibit biogeographical patterns at both macroscales(across regions and habitats) and microscales (withinone location, habitat, ecosystem) (Fierer 2008). Thestudy of microbial biogeography is relatively recent.The advent of molecular tools has provided newinsight on the diversity of the microbial world,particularly for species that we have not been ableto culture in the laboratory. Microbial communities indifferent ecosystems show high diversity and func-tional redundancy (Maier et al. 2009, Torsvik andØvreas 2002), which favors the formation of consortiathat comprise many microorganisms sharing niches innatural ecosystems. Redundancy in function allowsecosystems to be resilient and to recover from naturaland anthropogenic disturbances.

The niche concept integrates two important eco-logical terms, the habitat and the role of a species inthe ecosystem. The habitat encompasses the physicaland biological conditions that allow optimal growthand reproduction of a species. The role is theecological function this species has in the ecosystem.Both abiotic and biotic factors control niche occupa-tion by a particular species. Depending on thesefactors, some species can occupy a diversity ofecological niches as mesophilic generalists whileother species are specialists that occupy a particularniche. Microorganisms because of their size canoccupy habitats separated only by one to a fewmillimeters and perform different roles in theecosystem. Microbial biological processes define theniche and to some extent also affect the surroundingenvironment. Therefore the term microenvironmentis commonly used to describe the physical, chemicaland biological factors of a microbial niche.

Fungi are ubiquitous parts of global microbialcommunities and ecosystems. They occupy diverseniches and provide important ecosystem services,such as decomposition of organic matter, mineraliza-tion and nutrient immobilization. In general, fungiare members of mutualistic symbioses and mediatorsof primary production (Dighton 2003). For a fungusto occupy a niche spore germination must befollowed by production of mycelium or in the caseof yeast populations increased numbers of yeast cells.Most fungi are able to use resources by theproduction of extracellular enzymes for the decom-position of the organic matter. Sometimes species canoccur adjacent to each other in their preferredprimary niche, even in unusual habitats because ofthe generalist ability to adapt to wide variation inabiotic factors. Species that primarily occupy natural

Submitted 31 Mar 2011; accepted for publication 20 Apr 2011.1 Corresponding author. E-mail: [email protected]

Mycologia, 103(6), 2011, pp. 1161–1174. DOI: 10.3852/11-108# 2011 by The Mycological Society of America, Lawrence, KS 66044-8897Issued 17 November 2011

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environments can enter domestic, man-made envi-ronments if appropriate conditions are present. Abias in microbial ecology is that the niche of a speciesis mainly understood through biodiversity surveys.Due to biased approach, we do not know thecomplete distribution and diversity of possible nichesof most species. Because global climate change isexpected to alter water and surface temperatures,precipitation patterns, and wind directions andvelocity new niches for many fungal species will becreated and eventually will be exploited. The subjectof this review is unusual fungal niches, which can bedefined as habitats where we think a species will notbe present (outside what it is thought to be itsprimary niche) or a habitat where we normally donot investigate for the presence of fungi. We presenta list of possible unusual niches for fungi (TABLE I).Many of these unusual niches are consideredextreme environments, and they have been exten-sively studied for bacteria and archaea. Howeverrecent discoveries have revealed also the presence offungi and other eukaryotic species. Zak and Wild-man (2004) defined an extreme environment as

‘‘one that differs considerably from the range ofculture conditions that we believe is normal, eitherin natural settings or in the laboratory.’’ Instead ofcalling these environments extreme they preferredto call them ‘‘stressful’’ where certain abiotic factor(s)imposed a condition that restricts or prevents growthof most organisms. The first definition fits with what wepropose to call unusual fungal niches, however ourdefinition also includes niches normally not investi-gated for fungi. In this review we discuss five unusualfungal niches.

ANTARCTIC DRY VALLEYS

‘‘Where there is water, there is life’’ is an axiom(McKnight et al. 1999) that is accepted for all rangesof life forms and environments. This concept isdemonstrated clearly in the Antarctic dry valleys(FIG. 1), where environmental factors would appearto challenge most biota. The soils are considered tobe the oldest (thousands to millions of years), coldest(220 C av) and driest (, 10 cm precipitation y21)with the lowest organic carbon content (0.03 wt%)

TABLE I. Unusual fungal niches with reference to some published studies

Niche Reference

Hydrothermal vents Edgcomb et al. 2002Microbial mats Cantrell and Baez-Felix 2010, Feazel et al. 2008Deep sea sediments Raghukumar and Raghukumar 1998Acidic geothermal soils Bunn and Zabinski 2003, Redman et al. 1999Acidic mine drainage Baker et al. 2004Hot springs Ellis 1980Mud pools Wilson et al. 2008Acidic hot springs Jones et al. 2000Glaciers Gunde-Cimerman et al. 2003Antarctic dry valleys Fell et al. 2006Alpine tundra Freeman et al. 2000, Cripps and Horak 2008Methane seepage environments Takishita et al. 2006Tidal flat sediments Wilms et al. 2006Surface fumaroles Broady et al. 1987Underwater fumaroles Takishita et al. 2005Rocks Ruibal et al. 2009

Animal environments

Rumen Bauchop 1979, Orpin 1984Guts Heath 1988, Suh et al. 2005Exoskeletons Weir and Hammond 1997, Pagnocca et al. 2008Coral Bentis et al. 2000, Golubic et al. 2005Sponges Holler et al. 2000

Plant environments

Trichomes Dornelo-Silva and Dianese 2004, Pereira-Carvalho et al. 2009Thorns Flournoy et al. 2000Bryophytes fungi Kauserud et al. 2008, Huhtinen et al. 2010, U’ren et al. 2010,

Thormann et al. 2001Marine algae Zuccaro et al. 2003

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and biological activity on earth (Burkins et al. 2000),to the extent that 35% of the soils are reported tohave no animals present (Freckman and Virginia1998). The effect of the presence of water is apparentin soils adjacent to streams and glacial melts, whichteem with life including cyanobacterial mats, proto-zoans, fungi, chlorophytes, diatoms, nematodes,tardigrades, rotifers and springtails (for a review seeAdams et al. 2006).

In contrast to these high moisture soils, the dryvalleys include a region of 105 km2 of soils (Burkins etal. 2000) where moisture is often below 5%, thethreshold between wet and dry soils. The potential ofactive microbial communities in these dry soils wasdemonstrated by Burkins et al. (2000). The authorsreported soil CO2-efflux, which was interpreted asrepresentative of micro- and mesobiotic respiration.Microbial studies to assess this concept of microbesresponsible for respiration in dry soils appear to berare.

Fell et al. (2006) used molecular techniques, toexamine micro-eukaryotes in soils from 15 sites inthe Taylor and Wright valleys. Their results indicat-ed a community structure that is dependent on themoisture content of the soils. Micro-eukaryotes insoils with 0.2–1.3% moisture content were limited tothe yeast genus Trichosporon, whereas soils withmoisture of 3.1–4.9% contained complex food websincluding primary producers (chlorophytes andstamenophiles), symbionts (lichen associated fungi),

saprobes (fungi), predators (alveolates and cercozo-ans) and fungal nematode parasite/pathogens. Earlystudies suggested that the energy for dry valley soilfood webs was dependent on ancient organicreserves from past climate regimes or importedorganics (Doran et al. 1994, Moorhead and Priscu1998). In contrast, a self-contained food web,including algal derived carbon was theorized byFreckman and Virginia (1998). The presence of aprimary producer-based food web (Fell et al. 2006)would appear to corroborate the hypothesis (Bur-kins et al. 2000) of the importance of microbialcontributions to carbon input and turnover in dryvalley soils.

The structure of the fungal communities in the dryvalley soils increased with moisture content in concertwith the general microeukaryote populations. Speciesof Trichosporon, T. domesticum, T loubieri, T. ovoidesand Trichosporon sp. were the dominant mycobiota onsites with soil moisture of 0.2–1.3% in the dry valleys(Fell et al. 2006). The members of this genus areinhabitants of soils worldwide and are associated withhuman diseases. Trichosporon species were less prev-alent in soils with higher (3.1–4.9%) moisture contentthat had a more complex fungal community structure(Fell et al. 2006). Two major groups of fungi weredetected: ascomycetes and basidiomycetes. Ascomyce-tes included the generalist saprobes Phaeosphaeria sp.,Coniochaeta lignaria and Cochiobolus heliconiae andspecies in the lichen-forming genus Caloplaca inaddition to several unidentified species that appear tobe lichen associated fungi. All of these species arefilamentous fungi; yeast-like ascomycetes were notfound.

Basidiomycetes included the yeast Malassezia glo-bosa, which is known from healthy and diseasedhuman and animal skin. The species also been hasreported from nematodes in soils and in associationwith nematodes as the causative agent of bovineparasitic otitis (Duarte et al. 2001). Other basidiomy-cetes include Hohenbuehelia sp., known to includewood decomposers and nematophagus fungi, and thegeneralist saprobes Acanthobasidium sp., Cryptococcuscurvatus and C. arrabidensis.

Bridge and Newsham (2009) explored the speciesdiversity/moisture relationship at Mars Oasis inAntarctica. Their results, also obtained throughmolecular methods, corroborated the influence ofsoil moisture on the composition of Antarctic fungalcommunities. The Mars Oasis, at some distance fromthe dry valleys, has higher soil moisture (2.48–8.07%)and consequently a greater diversity of fungi. Generain common between the two Antarctic regionsincluded Trichosporon and Malassezia. The speciesof Malassezia found by Bridge and Newsham (2009),

FIG. 1. Sampling site in the Antarctic dry valley. Photocourtesy of Laurie Connell.

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M. restricta, is closely related to M. globosa and has thesimilar capacity for human and animal diseases andalso is known to be associated with nematodes(Renker et al. 2003).

Molecular sequence-based studies demonstrated anextensive diversity of fungi in Antarctic soils (Lawleyet al. 2004, Fell et al. 2006, Bridge and Newsham2009). However classical and molecular identifica-tions are not always congruent, a seemingly universalproblem as viewed for soil animals (Wu et al. 2009) tomicrobes (Bridge and Spooner 2001). This conclu-sion is enhanced by culture-based fungal studies inthe dry valleys. Connell et al. (2006, 2008, 2010)studied multiple sites, including the same sampled byFell et al. (2006), and they found Trichosporon andCryptococcus in common, but numerous other generawere found in both studies that did not overlap. Theproblems associated with classical culture methodsare well known (viz. media composition, environmen-tal growth conditions, rapid vs. slow growing colonies,etc.). Similarly variations in results by molecularmethods are attributed to nucleic acid extractionmethods, PCR inhibitors, primer design and geneselection (Anderson and Cairney 2004). As a conse-quence, combined classical and molecular studieswould provide more extensive, although still imper-fect, views of fungal community structures.

Despite the preliminary aspect of micro-eukaryoteresearch in Antarctic dry valleys, these snapshot viewsindicate the presence of complex food webs in drysoils with moisture content of 3.1–4.9% (content of1.3 and 3.1% were not examined). These food websinclude the range from primary micro-algal producersto fungal carbon recyclers. This suggests that the foodweb might contribute to the soil carbon pool, whichBurkins et al. (2000) estimated accounts for 72% ofthe biologically available carbon, whereas lakes andstreams account respectively for 27% and 0.5%. Thealternate hypothesis to the presence of an active foodweb is that these micro-eukaryotes are inactive wind-dispersed transients. Indeed the dry valleys have aharsh environment with low temperatures and strongwinds. Soil surfaces during the summer can vary from215 C to +27 C in 3 h (Cameron and Morelli 1974)and many freeze-thaw cycles can be experienced in amatter of minutes when clouds pass by (Friedmann etal. 1987). While the presence of some of theseorganisms may be the result of wind activity (Pearceet al. 2009), if all the species found in the dry valleysare wind dispersed, a more random distribution ofspecies would be expected, in contrast to themoisture-related distributions that have been report-ed. In addition species such as yeasts, which lackresistant spores, might have considerable difficultysurviving the daily and yearly environmental ex-

tremes. Because genera such as Trichosporon andMalassezia appear to have extensive distribution inthe Antarctic it is reasonable to infer that these yeastshave adapted to this environment and are capable ofmetabolic and reproductive activities. Neverthelessconsiderable study must be undertaken to understandthe structure and function of dry valley micro-eukaryotic communities. The simplicity of the dryvalley soil system, which lacks the complex organics,plants and animals of temperate and tropical regions,offers a unique opportunity to follow the environ-mental effects of climate change on this uniqueecosystem.

HIGH ARCTIC GLACIERS

Fungi in polar regions have been reported primarilyin connection with sub-Arctic vegetation. Mainlyyeasts were isolated from berries, flowers, vegetationof the littoral zone, soils, forest trees, grasses (Babjevaand Reshetova 1998), Antarctic mosses (Tosi et al.2002) and recently, in unexpected abundance, alsobelow snow-covered tundra (Pennisi 2003, Schadt etal. 2003). Few studies on the biodiversity of fungi inAntarctic soils revealed the prevalence of xerophilicbasidiomycetous yeasts (Atlas et al. 1978, Vishniac andOnofri 2003, Onofri et al. 2004). Viable yeasts andfungi were isolated sporadically also from Siberianpermafrost sediments, firmly fixed by ice (Takano etal. 2004). They were found with the highest frequencyof occurrence in the youngest layers, fewer than10 000 y old, although they also were detected in3 000 000 y old Pliocene samples (Dmitriev et al. 1997;Rivkina et al. 2000, 2004).

The occurrence of fungi in polar aquatic habitatshas been considerably less investigated. Yeasts andfungi were isolated from polar freshwater samples,benthic microbial mats and biofilms on pebblesbeneath the ice of Antarctic lakes ( Jones 1976,Baublis et al. 1991, de Wit et al. 2003). Fungi alsowere found in the hypersaline Antarctic Lake Wanda(Kriss et al. 1976), while sequences belonging toEumycota were detected up to 3000 m deep in polarwaters (Lopez-Garcıa et al. 2001).

Polar glaciers (FIG. 2) represent one of the leastsampled habitats for the presence of fungi. Filamen-tous fungi and yeasts were found in the microbialcryoconite holes (Margesin et al. 2002), in 10 000–13 000 y old Greenland ice (Ma et al. 2000), 12 000 yold Antarctic Vostok ice core sections (Christner2002, Christner et al. 2000) and even from Antarcticice layers up to 38 600 y old (Abyzov 1993). In allthese cases the isolated fungi were filamentous andtheir numbers were low. By PCR amplification offragments of the eukaryotic 18S rRNA gene a diversity

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of fungi was identified in 2000–4000 y old ice coresamples from northern Greenland. However theywere not tested for viability (Price 2000). All thesefindings were interpreted as the result of coincidentalAeolian deposits of spores or mycelium into the iceduring its geological history and preservation of somesturdy fungal propagules in this extremely stable,frigid and static environment.

Recent investigations have shown that ice inglaciers can contain more than only frozen, viablecells and that glaciers in general harbor a much moredynamic microbiota than previously assumed. Ice intemperate glaciers can be permeated by a continuousnetwork of aqueous veins, formed at the linearjunctions of three ice crystals, due to salt-containingaerosols, essentially insoluble in ice crystals (Rohdeand Price 2007). Due to the percolation of water fromthe top of the glacier to its bottom, salts canaccumulate to relatively high ionic concentrations incertain areas of the glacier and also in the bottomparts of polythermal glaciers (Price 2000). Further-more, due to quick seismic shifts (Ekstrom et al. 2003,Fahnestock 2003) and cryokarst phenomena, liquidwater can appear temporarily as ponds or streamletson the surface of the glacier and as caves orinterglacial lakes, artesian fountains and moulinswithin the glaciers (Christner et al. 2000). Supragla-cial waters can reach the glacier bed and mix withgroundwater and basal melt water, interact with rocksand sediments and create subglacial environmentsuntil recently considered abiotic. Initially only pro-karyotic microbial communities were found in north-ern and southern hemispheres beneath high and lowaltitude glaciers (Skidmore et al. 2000, Foght et al.2004). The first report on the presence of fungirevealed large populations of xerotolerant/halotoler-ant fungi in subglacial ice of Arctic coastal glaciers of

Kongsfjorden, Spitsbergen, in the Svalbard Archipel-ago (Gunde-Cimerman et al. 2003). The mainrepresentatives were yeasts (Butinar et al. 2007,2011), which also have been isolated from ice andmelt water from Italian alpine glaciers (Branda et al.2010, Thomas-Hall et al. 2010, Turchetti et al. 2008)and from Patagonian glaciers (de Garcıa et al. 2007).

In addition to yeasts the dominant taxa weremelanized yeast-like fungi, mainly represented bythe genera Cladosporium and Aureobasidium (Zalar etal. 2008) and different species of Penicillium (Sonjaket al. 2006). The fungal counts detected in thesubglacial samples were two orders of magnitudegreater when compared with those recovered fromsupraglacial samples, mainly due to yeasts (withcounts reaching up to 4 3 106 CFU L21).

Most isolated yeasts were basidiomycetes; ascomy-cetous yeasts represented , 15% of all isolates. Theratio of basidiomycetous to ascomycetous yeastschanged with the aw and the solute used to increasethe osmotic pressure of the media. On media withadded NaCl the ratio between ascomycetous andbasidiomycetous yeasts increased above 50% (Butinaret al. 2007, Butinar et al. unpubl).

Overall 22 basidiomycetous species of the classesHymenomycetes and Urediniomycetes were found(Butinar et al. 2007). With respect to their abundanceand species diversity, the dominant group corre-sponded to the hymenomycetous, nonpigmentedFilobasidium/Cryptococcus taxa of the Tremellales(Butinar et al. 2007). Cryptococcus liquefaciens, thepredominant species, was isolated primarily fromsediment-free subglacial ice (Butinar et al. 2007).The second most frequent species, Rhodotorulamucilaginosa (Libkind et al. 2004), the prevailingyeast in subglacial ice with sediment inclusions, alwayswas isolated together with C. liquefaciens (Butinar etal. 2007). Of note, both C. liquefaciens and Rh.mucilaginosa were the only microorganisms that havebeen isolated from Antarctic Vostok ice core (D’Eliaet al. 2009) and at various depths of the Greenland icesheet (Starmer et al. 2005). Ascomycetous yeasts havebeen reported rarely from extremely cold naturalenvironments, even though they are known contam-inants of frozen foods. Various yeasts, includingDebaryomyces hansenii and Pichia guillermondii, withcounts up to 104 CFU L21, were isolated using mediawith low water activity (Butinar et al. 2011). Thegroup of ascomycetous black yeasts was dominated byAureobasidum pullulans, a ubiquitous and widespreadoligotroph, which also can be found in osmoticallystressed environments such as hypersaline waters insalterns (Gunde-Cimerman et al. 2000), phyllosphereand recently subglacial ice samples with gypsuminclusions (Zalar et al. 2008). The stable core of the

FIG. 2. Polythermal glacier in Svalbard, Spitzbergen,Norway. Photo by N. Gunde-Cimerman.

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subglacial yeast communities thus was represented byCryptococcus liquefaciens, Rhodotorula mucilaginosa,Debaryomyces hansenii, Pichia guillermondii and Aur-eobasidium pullulans.

Among the isolated filamentous fungi the prevail-ing genus was Penicillium with a surprisingly highbiodiversity of 24 identified species and the newlydescribed P. svalbardense (Sonjak et al. 2007b).Although supraglacial samples contained only up to50 CFU L21 conidia, subglacial debris-rich ice samplesharbored a surprisingly rich diversity and highoccurrence of penicillia (up to 1.3 3 104 CFU L21)(Sonjak et al. 2006). The dominant species, both insediment-rich and in overlying clear glacial ice, wasthe cosmopolitan P. crustosum (Sonjak et al. 2006),which typically is reported as foodborne (Pitt andHocking 2009). This species was isolated from allsampled glaciers, and it also represents one of the twodominant species in the glacier melt water (Sonjak etal. 2006). It is interesting to note that P. crustosumstrains isolated from one glacier differed from allother Arctic strains and also from all tested strainsisolated worldwide (Sonjak et al. 2005, 2007a). AFLPanalysis distinguished a new P. crustosum genotypethat otherwise did not differ in other tested chemical,physiological, and morphological characteristics(Gostincar et al. 2009; Sonjak et al. 2005, 2007a).From all isolated penicillia only P. commune, P.discolor, and P. polonicum were detected at signifi-cantly greater numbers in clear glacial ice than insediment-rich ice (Sonjak et al. 2006). The onlyspecies other than P. crustosum that was detected asabundant in the glacial outflow water was P.bialowiezense (Sonjak et al. 2006).

SALT FLATS AND SALTERNS

Crystalline salt (NaCl) generally is considered to be sohostile to most forms of life that it has been used forcenturies as a food preservative. However foodpreserved with high concentrations of salt, solarsalterns (FIG. 3) and salt lakes worldwide representnatural environments for halophilic and halotolerantmicroorganisms which can adapt to extreme concen-trations of NaCl and also to high concentrations ofother ions, to high ultraviolet (UV) irradiation and insome cases to extremes of pH (Gunde-Cimerman etal. 2000).

Until Gunde-Cimerman et al. (2000) reported thatfungi populate brine in Slovenian salterns fungi wereknown only as contaminants of food that had beenpreserved with high concentrations of salt or sugar.They therefore were considered to have a generalxerophilic phenotype (Northolt et al. 1995), deter-mined primarily by the water potential of the medium

instead of the chemical nature of the solute (Hocking1993, Pitt and Hocking 1997). Subsequent reportsrevealed that fungi are active inhabitants of globalsolar salterns (Gunde-Cimerman et al. 2000, Butinaret al. 2005c) and hypersaline lakes around the world.Fungi were isolated from brine, agar baits, pelliculeson the surface of water and wood immersed in brine.Based on these reports halophilic and halotolerantmycobiota are now recognized as an integral part ofglobal stable indigenous microbial communities,differing to some extent in diversity and abundancealong environmental gradients.

Halophilic and halotolerant fungi differ in halo-philic behavior from the majority of halophilicprokaryotes. With few exceptions halophilic fungido not require salt for viability because they can growand adjust to the salinity range from freshwater toalmost saturated NaCl solutions (Plemenitas et al.2008). The most important variables influencing theirpresence and numbers in nature are two mainnutrients (phosphorous and nitrogen), followed bydissolved oxygen, aw, pH and sampling year (Butinaret al. unpubl).

FIG. 3. Solar salterns in Puerto Rico (A, photo by S.A.Cantrell) and Slovenia (B, photo by N. Gunde-Cimerman).

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Tolerance to low aw has been described to date onlyin 10 orders of fungi. In each of these orders growthat decreased aw is limited in most cases to a fewspecies or to a single genus. However in theWallemiales (Basidiomycota), Capnodiales, Dothi-deales and Eurotiales (Ascomycota) halophily isexpressed in several groups within the same orderthat are not the nearest phylogenetic neighbors (deHoog et al. 2005). Most halophilic and halotolerantfungi described to date from natural hypersalineenvironments have been identified either as knownfoodborne species with previously unrecognizednatural niches or as species that were not known toscience and consequently were newly described.

The mycobiota in hypersaline waters around theworld comprises meristematic melanized yeast-likefungi and several species of Cladosporium (Gunde-Cimerman et al. 2000, Butinar et al. 2005c, Zalar et al.2007), non-melanized yeasts (Butinar et al. 2005b),filamentous genera Wallemia, Scopulariopsis andAlternaria (Gunde-Cimerman et al. 2005, Zalar et al.2005) and different species of Aspergillus andPenicillium (i.e. holomorphs in Eurotium, Emericellaand Petromyces) (Butinar et al. 2005a, Butinar et al.unpubl). The dominant halophilic species are repre-sented by Hortaea werneckii, Phaetotheca triangularis,Trimmatostroma salinum and the halotolerant Aur-eobasidium pullulans.

Within Ascomycota the main orders with halophilicand halotolerant representatives are Capnodiales,Dothideales and Eurotiales. Cladosporium isolatesinitially were identified as C. sphaerospermum, howev-er taxonomic and phylogenetic analyses revealed acomplex of eight new species that have either narrowor wide ecological distributions (Zalar et al. 2007).Within Eurotiales, xerotolerant and halotolerantspecies are located in remote clades and arerepresented by A. niger, A. sydowii, E. amstelodamiand P. chrysogenum (Butinar et al. unpubl). Osmoto-lerant yeast taxa belong mainly to the Saccharomyce-taceae and Metschnikowiaceae, however the onlyhalotolerant yeasts that have been isolated fromhypersaline environments belong to the generaCandida, Debaryomyces, Metschnikowia and Pichia(Butinar et al. 2005b).

The Basidiomycota contains three orders withhalophilic and halotolerant representatives, Trichonos-porales with Trichosporon mucoides, Sporidiales withseveral Rhodotorula species and Wallemiales with thesingle genus Wallemia, a phylogenetic maverick in theBasidiomycota (Zalar et al. 2005). Until recentlyWallemia contained only the species W. sebi. Howevertaxonomic analyses of isolates from sweet, salty anddried food (Samson et al. 2002) and from hypersalineevaporation ponds around the world have resolved this

genus into three species, W. sebi, W. muriae and W.ichthyophaga (Zalar et al. 2005). The latter is at presentthe most halophilic eukaryote known to date because itcannot grow without at least 10% NaCl medium.

The most studied eukaryotic microorganism relat-ing to salt tolerance is S. cerevisiae (Serrano 1996).However, S. cerevisiae is salt sensitive and cannotadapt to hypersaline conditions. In contrast speciessuch as D. hansenii (Norkrans 1966, Prista et al.2005), H. werneckii (Gunde-Cimerman et al. 2000)and W. ichthyophaga (Zalar et al. 2005) have beenisolated globally from natural hypersaline environ-ments. These thrive even at extremely low aw andtherefore represent more suitable model organismsthan S. cerevisiae for the study of halotolerance ineukaryotes. Furthermore because they belong todifferent and distant phylogenetic groups presumablythey have evolved different strategies to cope with thesame problems of ion toxicity and loss of water (Oren2002). When comparing these three species with S.cerevisiae, physiological and molecular studies haverevealed substantial differences in their responses tochanges in salt concentrations (Prista et al. 2005).Saccharomyces cerevisiae can grow in up to 1.2 M NaCl,D. hansenii in up to 3.0 M and H. werneckii in up to5.0 M, while W. ichthyophaga requires at least 1.5 Mand can thrive in NaCl saturation (5.2 M).

MICROBIAL MATS

Microbial mats are laminated organo-sedimentaryecosystems that often are considered to be relics oflife on early Earth (FIG. 4). They have been foundunder a wide range of environmental conditions (e.g.freshwater to extremely hypersaline, 0–35% salt) andtemperatures ranging from subzero to hyperthermal(van Gemerden 1993, Dupraz and Visscher 2005).Based on their preservation potential in the rockrecord, two major mat types can be distinguished,lithifying and non-lithifying. Lithification, the processof converting sediments into rocks, is influenced byabiotic and biotic conditions affecting the precipita-tion of minerals (Dupraz and Visscher 2005, Duprazet al. 2009). For example, carbonate precipitation inmats, which is microbially mediated, enhances thepotential of fossilization. The production of carbon-ates is influenced by metabolic processes of thevarious microbial groups that thrive in these systems(Visscher and Stolz 2005, Dupraz et al. 2004,Vasconcelos et al. 2006). These metabolically linkedmicrobial groups often are segregated into distinctlayers based on strong fluctuations of physicochemi-cal and biogeochemical gradients, resulting in thetypical laminated mat structure (Dupraz and Visscher2005, Visscher and Stolz 2005).

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Based on general traits, members of microbial matcommunities have been categorized into approxi-mately seven guilds: (i) photolithoautotrophs (i.e.cyanobacteria); (ii) aerobic (chemoorgano-)hetero-trophs; (iii) fermenters; (iv) anaerobic heterotrophs(sulfate-reducing bacteria; SRB); (v) sulfide-oxidizingbacteria (SOB); (vi) anoxyphototrophs (i.e. purpleand green [non]sulfur bacteria); and (vii) methano-gens (van Gemerden 1993, Dupraz and Visscher2005). While this trait-based classification suggeststhat mats are relatively simple ecosystems, molecularstudies show that mats contain an extremely complex,diverse and unique assemblage of microorganismsthat interact to produce a highly productive ecosys-tem that surpasses rain forests in complexity, diversityand net primary production (Visscher and Stolz 2005,Ley et al. 2006, Baumgartner et al. 2006, Burne andMoore 1987).

Molecular studies indicate also that eukaryoticorganisms (i.e. algae, ciliates, flagellates, fungi andnematodes) are present in these ecosystems (Cantrellet al. 2006, Feazel et al. 2008). Cantrell et al. (2006)isolated and characterized fungi in young transientmicrobial mats with traditional and PFLA techniques

and documented for the first time that fungi arepresent in this unusual niche. Some species that havebeen isolated are Aspergillus carneus, A. flavus, A.nidulans, A. niger, A. terreus, Aurebasidium pullulans,Cladosporium cladosporioides, C. sphaerospermum, C.dominicanum, Hortaea werneckii, Penicillium citrinum,P. chrysogenum, P.oxalicum, Pichia guiliermondi, Pre-ussia minima and Rhodosporidum sp.

TRFLP results suggested that the total abundanceand richness of TRFLP phylotypes in older maturemicrobial mats are greater during the wet season thanin the dry season. Diversity decreased from the firstlayer (at a depth of 0–1 mm) to the third layer (at adepth of 2–20 mm) (Cantrell and Baez-Felix 2010).Feazel et al. (2008), using universal 18S rDNAeukaryotic primers, reported that three of 890sequenced clones from the Guerrero Negro microbialmat in Mexico belonged to a single species of fungus,Metschnikowia bicuspidata (Saccharomycotina). Pre-liminary results from 131 sequenced clones from sixlibraries have detected six species from a maturepermanent microbial mat in Puerto Rico (Cantrelland Baez-Felix 2010). The majority of these clonesfrom Puerto Rico belong to Acremonium strictum(41% of all sequenced clones) and Cladosporiumhalotolerans (36%). Additional sequences of Clado-sporium and Acremonium, (5% and 6% respectively)may represent unknown species. Five percent of theclones belong to Aspergillus penicilloides, and 2% areclosely related to other Aspergillus/Penicillium spe-cies. Six clones (5%) did not match any sequence inGenBank and might represent a novel group withinthe ascomycetes. These finding demonstrated theneed of selecting the appropriate molecular marker.The 18S rDNA region is highly conserved in fungi andwill not discriminate among species, while the ITSregion is more variable and in some cases can be usedfor species delimitation.

LEAF TRICHOMES

Trichomes are mostly filamentous, sometimes bul-bous to broadly clavate structures arising from thefoliar epidermis of angiosperms, which can be uni- ormulticellular. They can accumulate essential oils orother substances in their apical cells that function as aglandular head. Trichomes of plants growing on theNeotropical Brazilian savanna, the Cerrado, recentlywere found to be a microhabitat where severalunusual fungal species (Dornelo-Silva and Dianese2004, Pereira-Carvalho et al. 2009) preferably orexclusively proliferate in a superficial interaction withplant trichomes. Thus, three new hyphomycetespecies were found to belong in three new genera(Trichomatomyces, Trichosporodochium and Phaeoidio-

FIG. 4. Nonlythifying microbial mats from Puerto Rico.A. Young transient non-laminated mat. B. Older maturelaminated mat. (Photos by S.A. Cantrell)

1168 MYCOLOGIA

myces). All are epiphytes growing on trichomeswithout an obvious parasitic relationship. Theirconidiogenous cells are produced mostly on micro-nematous to semimacronematous conidiophoresformed by light brown to brown superficial myceliumthat spreads on the trichome surface. However inmany instances the conidiogenesis occurs mainlytoward the trichome apex, indicating an ecologicaladaptation that apparently leads to an easier conidialdispersal. More recently, also found on native plantson the same ecosystem, eight new monotypic tricho-matous hyphomycete genera were described; they aretype species Trichomatoclava cerradensis Sepulveda-Chavera, Pereira-Carvalho & Dianese, Echinoconidio-phorum cerradense Pereira-Carvalho & Dianese, Globo-conidiopsis cerradensis Sepulveda-Chavera (FIG. 5),Pereira-Carvalho & Dianese, Globoconidium cerradenseSepulveda-Chavera, Pereira-Carvalho & Dianese, Hel-minthosporiomyces cerradensis Sepulveda-Chavera, Per-eira-Carvalho & Dianese, Microtrichosphaera cerraden-sis Pereira-Carvalho, Sepulveda-Chavera & Dianese,Phragmoconidium cerradense Sepulveda-Chavera, Per-eira-Carvalho & Dianese and Vesiculohyphomycescerradensis Armando, Pereira-Carvalho & Dianese)(Pereira-Carvalho et al. 2009). The interaction be-tween the fungus and trichome is predominantlyepiphytic, however in one example, penetration ofthe trichome by the fungus was observed. ThusGloboconidiopsis cerradensis originally was consideredan epiphytic species, however a closer observationrevealed fungal hyphae in the trichome lumen thatemerge to form a compact spore mass on sympodiallyproliferating conidiophores (FIG. 5). Thus, the tri-chomatous hyphomycetes are not mere users ofsuperficial organic residues but may occupy a parasiticor endophytic function.

Plants in regions with a long, dry season tend toshow their leaves with the abaxial face rich intrichomes associated with microfungi that are mostlyhyphomycetes of complex morphology. Thus it isexpected that mycologists interested in fungal diver-sity will start to seriously consider this novel micro-habitat whose richness is just being detected.

CLOSING REMARKS

Many opportunities for fungi to thrive can occur indifferent ecosystems around Earth, and adaptationsto new abiotic conditions and to resist extremeenvironmental conditions will arise. Recent studieshave revealed the diversity of fungi that can occur instressful environments that are hostile to mosteukaryotes. It is possible that the ability of fungi toadapt to low and changing water activities, whetherdue to low temperatures or high salinities, is crucial

for their successful survival in some of the harshestenvironments on Earth. The unusual niches discussedconstitute unique ecosystems that enable occasionalenrichment of selected genotypes of the mostadaptable species that can tolerate a broad range ofenvironmental conditions. Surprisingly, these envi-ronments may result in similar environmental andevolutionary pressures on microorganisms. Freezing,drying and hypersaline stress lead to cellular dehy-dration and therefore can activate common respons-es. Cold-, salt- and drought-tolerant fungi thereforemay belong to a limited group of extremophilicspecies that share more features and inhabit moreextreme environments than we have imagined so far.It appears that traits present in some fungal groups,such as asexuality, synthesis of melanin-like pigmentsand a flexible morphology, are pre-adaptations thatfacilitate persistence and eventual adaptation toconditions on the ecological edge as well as biotopeswitches. Stressful environments thus may represent asignificant, previously unrecognized reservoir notonly of prokaryotic but also of eukaryotic diversity.

Most of the species described from the unusualniches are cosmopolitan and occur in a diversity ofsubstrates; however, they primarily thrive in thedescribed stressful environments. Yeasts, black yeast-like fungi, melanized filamentous species as well asrepresentatives of Aspergillus and Penicillium seem tobe dominant among the mycobiota adapted to coldand salty niches. Plant trichomes seem to be a uniqueniche harboring many previously unknown taxa. Eventhough the advent of new sequencing technologies ishelping elucidate the microbial diversity in manyecosystems and an increasing number of publicationsare dedicated to studies of molecular adaptations ofmodel organisms, more studies are needed todocument the functional role of fungi in themicrobial communities thriving in these unusualenvironments.

FIG. 5. Globoconidiopsis cerrradensis on leaf trichomes(T) with internal mycelium (I), bearing conidia onsympodially proliferate conidiophores. Bar 5 20 mm.(Photos by J.C. Dianese)

CANTRELL ET AL.: UNUSUAL FUNGAL NICHES 1169

ACKNOWLEDGMENTS

The authors thank the Mycological Society of America forfinancially supporting this symposium, held at the MSAannual meeting in 2009. Financial support for Dr Cantrellwas provided by the National Science Foundation (NSFMCB 0718500). Grant from CNpq-Brasil supported J.C.Dianese research.

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