Genomic analysis of the permafrost isolate Psychrobacter arcticus 273-4 has revealed that a variety of adaptations are employed by P. arcticus 273-4 to enable active growth at low temperatures. Many of these low-temperature adaptations are largely similar to adaptations found in other psychrophilic microorganisms isolated from other low-temperature environments. These similarities include: changes in amino acid abundance that favor protein mobility; RNA and protein chaperones; and desaturation of membrane lipids. Unlike other psychrophiles, P. arcticus 273-4 constitutively expressed the major cold-shock protein (cspA, an RNA chaperone) at all growth temperatures to maintain the molecular motion of RNA. The constitutive expression of cspA may be an advantage in permafrost, where cold temperatures reign. In addition, cell-wall elasticity may be affected by low temperatures in P. arcticus 273-4, and could play a major role in growth rate control or maintenance of turgor pressure in the frozen conditions of the permafrost. Low-temperature effects on the cell wall have not been reported in other psychrophiles, and could suggest a unique adaptation to the permafrost environment. Clearly, maintaining molecular motion, and hence function of those molecules, through changes in the basic structures of biomolecules (proteins, lipids, cell wall) and with the assistance of chaperones is important to actively living at low temperatures.

Isozymes can also be used to maintain molecular motion and allow key enzymatic functions to be maintained regardless of growth temperature. Isozymes may be particularly useful to microorganisms that live in the active layer of permafrost, where temperatures fluctuate on a seasonal — and sometimes daily — basis around the freezing point of water. While P. arcticus 273-4 was recovered from deep permafrost where the temperature has been stable at -10°C for 20,000-30,000 years (Vishnivetskaya et al. 2000), its initial habitat was at the surface within the active layer of permafrost. The presence and use of isozymes within P. arcticus 273-4 (and the constitutive expression of cspA) may reflect this ecological history.

Analysis of the transcriptome demonstrated that efficient use of resources was another strategy employed by P. arcticus 273-4 for living at low temperatures. Efficiency of resource utilization may be key to the survival of heterotrophic microbes over thousands to millions of years in permafrost, given that permafrost, due to the frozen state, is an environment characterized by a high degree of spatial isolation and low rates of solute transport. Hence, the introduction of new substrate is likely to be a rare event in the permafrost. Efficient use of resources has only been suggested in psychrophilic methanogens, and has not been noted in studies of other psychrophiles. Therefore, this particular strategy (efficient use of resources) may be an adaptation of these psychrophiles to physically or energetically constrained environments and not an adaptation to low temperatures per se.

Long-term survival strategies in permafrost are thought to fall into two main categories: (i) microbes maintain viability by entering a dormant state in which they can resist damage to cellular insults, or (ii) microbes maintain viability by metabolizing and repairing damage at rates sufficient to equal or exceed the rate of death due to environmentally induced damage. Psychrobacter sp. clearly fall into the latter category, as the observed changes in the genome and in gene expression are primarily directed toward maintenance of molecular motion and resource efficiency for continued growth in frozen conditions. These low-temperature adaptations are consistent with an organism adapted for life under long-term freezing conditions and may be crucial to survival, considering that a recent study of ancient DNA from permafrost concluded that "long-term survival is closely tied to cellular metabolic activity and DNA repair that over time proves to be superior to dormancy as a mechanism in sustaining bacteria viability" (Johnson et al. 2007).

Acknowledgements The authors and their research on permafrost bacteria were supported through membership in the NASA Astrobiology Institute.

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