Life in Dark and Cold Ecosystems

While the mechanisms which protect bacteria against the adverse conditions that include oxidation, cooling, high osmolarity/dehydration and starvation are well studied, our knowledge about adaptive and survival mechanisms of photoautotrophic microorganisms in cold and dark ecosystems such as permafrost remains limited. Obviously the upper soil and permafrost layers prevent photosynthetic activity of any chlorophyll-containing organisms. However, green algae and cyanobacteria do survive in the permafrost (Table 6.2). We have suggested that the permafrost algae survive in the deep dark permafrost sediments below freezing point for thousands and up to millions of years in the dormant or resting state (Vishnivetskaya et al. 2001). Permafrost photoautotrophic microorganisms endure the long-term impact of cold and darkness but they are readily reversible to proliferation and they do not lose the capability for photosynthesis (Vishnivetskaya et al. 2003). We have shown that isolates of the genus Chlorella grew on solid nutrient media at the dark (Vishnivetskaya et al. 2005). Recent studies have shown that contemporary unicellular algae possess the ability for heterotrophic growth as a mechanism for survival. For example, Chlamydomonas exhibited a remarkable resistance to starvation in the dark (Tittel et al. 2005); the marine dinoflagellate Fragilidium subglobosum was capable of phototrophic growth as well as of heterotrophic (phagotrophic) growth in the dark (Skovgaard 1996); unicellular green algae (Oocystis sp.) and cyanobacteria (Xenococcus sp.) were isolated from drinking water systems, and they demonstrated the ability to grow in the dark as a consequence of their heterotrophic metabolism (Codony et al. 2003).

Table 6.2 List of the viable cyanobacteria and green algae discovered in the permafrost



(Kolyma lowland, Northeast Russia)

(Dry Valleys)

Green algae

Chlorella sp.

Chlorella sp.

Chlore vulgaris

Chlorococcum sp.

Chlorella sacchorophilla

Mychonastes sp.

Chlorococcum sp.

Chodatia sp.

Chodatia tetrallontoidea

Mychonastes sp.

Nannochloris sp.

Paradoxia sp.

Pseudococcomyxa sp.

Scotiellopsis sp.

Stichococcus sp.


Anabaena sp.


Leptolyngbya sp.

Microcoleus sp.

Nostoc sp.

Oscillatoria sp.

Phormidium sp.

Our observations have shown that the appearance, morphology and growth rate of ancient permafrost algae did not differ significantly from the findings on contemporary algae from cold regions. The viable permafrost green algae grew at 27, 20 and 4°C, but cyanobacteria had good growth at room temperature only (Vishnivetskaya et al. 2003). Algae had a low growth rate, with a doubling time of 10-14 days. Rise in nitrogen, phosphorus or CO2 concentrations did not affect the growth rate. On the other hand, the growth of the Nostoc sp. was completely inhibited by ammonium chloride or ferric ammonium citrate (Erokhina et al. 1999). The sources of organic ammonium such as Na-glutamine, asparagine or glycine led to the reduction of heterocysts and the development of akinetes (resistant resting cells) (Vishnivetskaya et al. 2003).

The content and composition of photosynthetic pigments in the cells of the ancient cyanobacteria and green algae based on their absorption spectra, the second-derivative absorption spectra, were studied (Erokhina et al. 1998, 2004). Comparative analysis of the absorption spectra of the Siberian permafrost cyanobacteria Oscillatoria sp., Phormidium sp., Nostoc sp., and Anabaena sp. revealed the presence of chlorophyll a, phycobiliproteins, and carotenoids in their cells (Erokhina et al. 1998). Spectral analyses of the Antarctic permafrost green algae Chlorococcum sp. and Chlorella sp. showed the presence of a low content of chlorophyll a, a high relative content of chlorophyll b, and complex composition of carotenoids (Erokhina et al. 2004; Gilichinsky et al. 2007b). The ability of Nostoc sp., and Anabaena sp. to form numerous hetero-cysts when grown on nitrogen-free medium, and the presence of C-phycoerythrin, suggested that they were capable of nitrogen fixation (Erokhina et al. 1999; Vishnivetskaya et al. 2001). The permafrost nitrogen-fixing cyanobacteria were capable of complementary chromatic adaptation, which involves the regulation of the synthesis of the photosynthetic pigments, C-phycoerythrin and phycocyanin, by red or green light (Erokhina et al. 2000; Vishnivetskaya et al. 2005).

In nature, algae inhabiting surface layers of cold regions show high resistance to the temperature fluctuations which are caused by repetitive phase transitions of water through the freezing point. Deep freezing (-40°C, -100°C, -196°C) and desiccation, laboratory-tested on cyanobacterial and algal strains from maritime and continental Antarctica, caused little harm to cyanobacteria, but was fatal for more than 50% of the population of algae (Sabacka and Elster 2006). But how would permafrost microalgae conduct themselves in such a situation? The fact that algae have been recovered from permanently frozen sediments may suggest the resistance of algae to both primary and long-term freezing. The most critical steps where cells may receive injuries are the primary freezing and the thawing. The permafrost samples with relatively high algal biomass and numerous cultivable green algae units were exposed to repeated freeze-thaw cycles. During the experiments, it was shown that permafrost algae themselves could survive the stresses associated with transition through the freezing point. It appears that freezing induces the formation of protective envelopes and resting cells, and as a result the permafrost algae withstand dehydration and long-term inactivity (Vishnivetskaya et al. 2003).

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