Table 7.1 shows that the overwhelming majority of fungi isolated from permafrost strata form small unicellular conidia (e.g., Aspergillus spp., Chrysosporium spp., Penicillium spp., Phialophora spp.). Experience of successful cryopreservation of collection cultures demonstrates that fungi with small spores are better adapted to long-time preservation than fungi with other types of spores. Representatives of genera of which a characteristic is the ability to form large multicellular spores (Alternaria, Bispora, Monodictys, Ulocladium, etc.) contain melanin within cell wall components; this compound is widely known as a protectant against the impact of extreme temperatures (contrary to prior belief that it attenuates adverse effects of exposure to UV radiation) (Sterflinger 1998; Robinson 2001; Rosas and Casadevall 2001). Note that more than 60% melanin-containing strains were isolated at 4°C (Ivanushkina et al. 2007).
Of considerable importance for the preservation of fungi in permafrost are both the presence of natural cryoprotectants in these ecotopes and the ability of the fungi to make use of their inherent mechanisms of protection. For example, species belonging to the genera Arthrinium, Aureobasidium, Botrytis, Fusarium, Geotrichum, and Oidiodendron, as well as many others, are usually isolated from plant material and/or appear as phytopathogens. It is conceivable that plant substrates or derivatives thereof are natural cryoprotectants, which enables them to provide advantageous conditions to microorganisms when the sediments freeze. Stakhov et al. (2008) demonstrated that ancient seeds of higher plants constitute a specific habitat for microorganisms in frozen ground, which favors their preservation for millennia. The presence of such natural protectants made it possible to preserve certain microbial species specific for these plants, e.g., representatives of the genus Phoma.
Fungi with a broad adaptive potential, such as species of the genera Penicillium, Aspergillus, Cladosporium, and Geomyces, occur in permafrost most frequently. Lowering the ambient temperature may trigger protector mechanisms inherent in fungal cells. These mechanisms include elevation of intracellular trehalose, polyols, and unsaturated fatty acids, as well as the synthesis of enzymes operating at low temperatures (Robinson 2001). In particular, there is evidence that the temperature of cultivation affects both the content and the composition of intracellular carbohydrates and lipids in mycelial fungi. The changes increase the amount of compounds with cryoprotectant properties (e.g., unsaturated fatty acids are elevated, and the sterol to phospholipid ratio becomes lower) (Weinstein et al. 2000; Turk et al. 2004). Fungi exposed to osmotic stressors are capable of synthesizing glycerol for maintaining their intracellular water potential at low levels (Förster et al. 1998; Teixido et al. 1998), and glycerol is known to protect cells under conditions of extreme temperatures.
The features indicated above not only facilitate survival of fungi exposed to stressors, they also favor the development of individual strains of certain species in extreme habitats. The observation that representatives of certain species, isolated from permafrost, are characterized by growth optima shifted towards lower temperatures provides indirect evidence of the ability of microbial strains to develop at extremely low temperatures. Such species are, according to our data and reports of researchers working with Antarctic strains, representatives of the genera Penicillium, Cladosporium and Geomyces, most frequently occurring in permafrost (Tosi et al. 2002). Moreover, a strain of Geomyces pannorum, isolated from liverwort in Antarctica, was reported to grow at a rate of 0.05 mm per day when the temperature of the environment was -2°C (Hughes et al. 2003). The cultures of this species are capable of switching cellular metabolism in response to temperature decreases (Finotti et al. 1996). The ability of these fungi to grow at subzero temperatures is in accordance with the results of studies of Arctic strains (Kochkina et al. 2007). The experiments demonstrated that the optimum growth temperature of G. panno-rum strains, isolated from overcooled water brines (cryopegs) and frozen marine deposits, is lower than those of representatives of this species isolated from other habitats. In addition, these strains exhibited active growth at subzero temperatures (-2°C), surpassing control cultures from the temperate zone by two orders of magnitude in the growth rate.
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