Antarctic fungi

The Antarctic fungal biodiversity has been investigated from floristic (Del Frate and Caretta 1990; Montemartini Corte 1991; Onofri et al. 1991, 1994; Onofri and Tosi 1992; Mercantini et al. 1993; Montemartini Corte et al. 1993) ecophysiological (Caretta et al. 1994; Zucconi et al. 1996; Fenice et al. 1997; Onofri et al. 2000; Tosi et al. 2002), molecular (Vishniac and Onofri 2002) and, most recently, phylogenetic points of view (Selbmann et al. 2005), by isolating and identifying fungal strains from samples collected in different areas of the Antarctic continent (Onofri et al. 2005a). The distribution of fungi in Antarctica is related to the distribution of different substrata such as soils, rocks, bird feathers and dung, vegetation, which consists of plants (largely limited to maritime Antarctica), bryophytes, and lichens (Bridge and Worland 2004; Jumpponen et al. 2003; Leotta et al. 2002; Tosi et al. 2002), and to the distribution of scientific research stations, mainly scattered along the coast of the continent, whose environs have been most extensively investigated. There is a long list of fungal species, including yeasts, colonizing nearly all terrestrial environments occurring in Antarctica (Onofri 1999; Onofri et al. 2006). Most of the filamentous fungi and yeasts are cosmopolitan species; some fungi are psychro-philic, even more are psychrotolerant; whilst the arid conditions on the Antarctic rock surface, usually lead to the dominance of xerotolerant organisms.

Regarding continental Antarctica, Onofri et al. (2005b, 2006) report that a small percentage (0.6%) of known "fungi" species is represented by water moulds (kingdom Chromista), while the major proportion (99.4%) is composed of true fungi, including yeasts and filamentous fungi, which together comprise species belonging to phyla of Chytridiomycota, Zygomycota, Ascomycota and Basidiomycota. Among these, some species are possibly endemic and some others are indigenous, being able to show active growth and to reproduce in Antarctica; these include psychrophilic or, more commonly, cold-tolerant mesophilic strains, or strains adopting other forms of adaptations. For some species, indigenicity is indicated by the high number of isolations over the years, as in Cryptococcus vishniacii, Geomyces pannorum and Thelebolus microsporus, frequently recorded in Antarctica from different sites and substrata (Onofri et al. 2006). Many microfungal strains, having meristematic growth, mainly found associated with rocks, have also been recorded. Some of them, isolated from the ice-free areas of the Victoria Land, have been described as endemic genera and species (Onofri et al. 1999; Selbmann et al. 2005).

Most of the fungi recorded in the Antarctic continent are anamorphic forms. It seems that fungi gaveup sexual reproduction as this simplification means that life cycles can be concluded in a shorter time and without high metabolic costs. A few exceptions have been reported, such as Thelebolus spp. (Ascomycota) frequently collected in continental Antarctica. Thelebolus species have been reported to reproduce sexually, but the endemic species T. globosus Brumm. & de Hoog and T. ellipsoideus Brumm. & de Hoog, living in the microbial mat of some Antarctic lakes, show a strong reduction of the ascomata compared with the species living in more permissive conditions and produce anamorphs as adaptations to the extreme conditions of sealed Antarctic lakes (de Hoog et al. 2005).

Cryptoendolithic black fungi living in the prohibitive conditions of the ice-free zones in Victoria Land show an even more extreme simplification of their life-cycles: most of them are unable even to produce anamorphic reproductive structures but propagules are generated directly from disarticulation of toruloid pre-existing hyphae, as observed in Friedmanniomyces endolithicus Onofri. Some strains of Cryomyces are mostly yeast-like organized and can formally conclude their life-cycles with the production of a single cell being itself a resistant propagule. These high levels of simplification match very well with the prohibitive environment they colonize where the climatic conditions for active life occur just few days a year. Similar situations, recently reported by Kis-Papo et al. (2003) for fungi living in hypersaline environments, support this hypothesis. In fact they found a positive association among ecological stress, genomic diversity and sexual reproduction, and assumed that even if higher levels of genomic diversity provide a higher potential for genetic adaptation, when environmental conditions become closer to the limits for life, and the niche becomes narrower, homogeneous, and extremely stressful, then genomic diversity declines. Thus the harsh conditions experienced by cryptoendolithic black fungi promote a natural selection, which turns from diversification to a selective regime leading to a few highly adapted homozygous clones.

A completely different behaviour has however been discussed by Seymour et al. (2005) for lichens (lichen-forming fungi), which produce abundant sexual structures even in the hostile environments of Antarctica ensuring genetic recombination within populations. In these cases reproductive ascomata require just an initial high metabolic cost, because they persist for several years during which time large numbers of ascosp-ores can be released. But even these organisms, in the very extreme environments of the McMurdo Dry Valleys, give up their typical thallus morphology, epilithic sexual structures disappear and they shift to the cryptoendolithic growth form.

2.1 Cryptoendolithic communities

Antarctic cryptoendolithic microorganisms constitute very simple communities comprising only a few species (Nienow and Friedmann 1993). The most common and extensively studied is the ''lichen dominated community'' found in sandstone (Friedmann 1982). This community colonizes porous sandstones and appears under the rock crust as a conspicuous zone up to 10 mm deep, formed by parallel and differently coloured bands. Typically it consists of a black zone under the crust followed by a white, a green, and sometimes a blue-green zone (Fig. 1). The black and the white zones are formed by filamentous fungi and chlorophycean algae, which together give rise to a cryptoendolithic lichen association. However, they retain the potential of thallus formation and in protected niches, such as small depressions and crevices, characterized by a favourable microclimate, epilithic sexual structures appear. Lichens are pioneer organisms of extreme terrestrial environments (Kappen 1974) showing diverse and strategic growth and distribution (Kappen 1993; Nienow and Friedmann 1993); the transition from epilithic to endolithic morphotype in Antarctica occurs on a gradient that is mainly based on temperature (Friedmann

Endolithic Microorganism
Fig. 1 Cryptoendolithic lichen dominated community colonizing sandstone in the McMurdo Dry Valleys, Antarctica (bar 10 mm) (Onofri et al. 2006)

et al. 1994). Sandstone outcrops appear to become sterile with increasing distance from the sea (Onofri and Friedmann 1998). The fungal hyphae in the dark zone are melanized, while in the white zone they are colourless; they possibly represent different morphotypes of the same fungal species and the pigmentation in the upper level is supposed to be a response to higher light intensity (Nienow and Friedmann 1993); in fact, a fungal strain isolated from a lichen-dominated community in Southern Victoria Land, producing both pigmented and hyaline hyphae in culture, was demonstrated to be the fungal symbiont by means of laboratory resynthesis experiments (Ahmadjian and Jacobs 1987); later on molecular and microscopy studies demonstrated the ability of a lichen to grow endolitically (de los Rios et al. 2005). In the black zone, thick-walled and dark pigmented non-lichenized fungi, often showing meristematic growth in vitro, grow mixed with the lichen-forming fungi and are isolated as regular members of the lichen dominated cryptoendo-lithic community (Ocampo-Friedmann and Friedmann 1993; Onofri et al. 1999; Selbmann et al. 2005). In the green zone different species of non-lichenized chlorophycean algae grow, including the endemic species Hemichloris antarctica, as well as different extremophilic prokaryotes, such as the cyanobacteria Chroo-coccidiopsis sp. and Gloeocapsa sp. (Friedmann 1982). In some cases a further band is observed whenever Chroococcidiopsis forms a separate band below H. antarctica.

2.2 Rock inhabiting black fungi

Rock-inhabiting fungi can be split in two ecological groups: hyphomycetes of soil and of epiphytic origin, and black (melanized) microscopic fungi (Gorbushina et al. 2005). The black melanized microscopic fungi exhibit meristematic growth and form compact restricted microcolonies into rocks (Gorbushina et al. 1993; Sterflinger et al. 1999; Ruibal et al. 2005); they have been named microcolonial fungi (MCF, Staley et al. 1982; Sterflinger 2005) for their growth habit; their presence is ubiquitous and ranges from rock surfaces in the Mediterranean, middle and northern Europe, desert rocks worldwide, bare alpine rock surfaces, hypersaline environments to the Antarctic or as plant, animal and human pathogens. The meristematic fungi are a group of fungi that show very little and slow expansion growth, cauliflower-like colonies, and reproduce by isodiametric enlargement with subdividing cells. From a phylogenetic point of view they represent a quite heterogeneous group of fungi (Sterflinger et al. 1999). Microcolonial fungi show some typical characteristics that are extremely important for their survival in the challenging lithic environments and make them the most stress-tolerant and persistent inhabitants of sub-aerial rock biofilms on desert rocks (Staley et al. 1982). These fungi express melanized thick cell walls as a stable character, which make them able to withstand dryness, desiccation, and UV exposition. Furthermore, the meristematic growth ensures an optimal surface to volume ratio for the colonies (Wollenzien et al. 1995), a character that was supposed to improve the survival ability under stressful conditions such as high or low temperature, low water availability (Wollenzien et al. 1995), high UV exposition (Urzi et al. 1995), nutrient deficiency (Sterflinger et al. 1999), and high salt concentrations (Zalar et al. 1999c). Interactions between rock inhabiting microorganisms (fungi, algae, cyanobacteria and bacteria) are still poorly understood even if possible contacts between fungi and algal cells in rock crevices penetrated by fungi have been already recognized (Grondona et al. 1997; Turi-an 1977). Furthermore, in a recent study, Gorbushina et al. (2005) showed interactions between xerophilic photoautotrophic (photo-bionts of xerophilic lichens) and chemo-organo-heterotrophic (free-living microcolonial fungi) rock-inhabiting microorganisms, using axenic cultures. They demonstrated that at least some rock-inhabiting microcolonial fungal strains are capable of forming a very specific contact with algae. Rock-inhabiting black fungi in the Antarctic have been isolated from cryptoendo-lithic communities. They are fascinating and scarcely known microorganisms, surviving and even thriving in environments more hostile than those of the remaining rock-inhabiting fungi. Among the fungal species reported from the continent, they seem to be the best adapted ones to the harshest conditions typical of this environment (Selbmann et al. 2005). The typical morphology of the rock inhabiting fungi makes them suitable to withstand harsh environmental conditions; they also show the ability to produce extracellular polymeric substances (EPS), possibly polysaccharides, that are thought to be involved specially in the protection against desiccation and repeated freezing and thawing cycles (Selbmann et al. 2002, 2005).

Recently, two new genera and four new species (Friedmanniomyces endolithicus Onofri, F. simplex Selbmann et al., Cryomyces minteri Selbmann et al., C. antarcticus Selbmann et al.) have been described (Onofri et al. 1999; Selbmann et al. 2005) by means of morphological and molecular analyses (rDNA ITS and SSU). Among the filamentous hyphomycetes present in endolithic habitats, a strain of Verticillium sp. and a non-cultured black pigmented fungus have been recorded from a microbial endolithic community within gypsum crusts at Two Step Cliffs, the closest analogue to continental Dry Valley systems present in the Antarctic Peninsula region (Alexander Island, maritime Antarctica) (Hughes and Lawley 2003).

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