The survival of microorganisms in ancient glacial ice and permafrost has been ascribed to their ability to persist in a dormant, metabolically inert state. An alternative possibility, supported by experimental data, is that microorganisms in frozen matrices are able to sustain a level of metabolic function that is sufficient for cellular repair and maintenance. To examine this experimentally, frozen populations of Psychrobacter arcticus 273-4 were exposed to ionizing radiation (IR) to simulate the damage incurred from natural background IR sources in the permafrost environment from over ϳ225 kiloyears (ky). High-molecularweight DNA was fragmented by exposure to 450 Gy of IR, which introduced an average of 16 double-strand breaks (DSBs) per chromosome. During incubation at ؊15°C for 505 days, P. arcticus repaired DNA DSBs in the absence of net growth. Based on the time frame for the assembly of genomic fragments by P. arcticus, the rate of DNA DSB repair was estimated at 7 to 10 DSBs year ؊1 under the conditions tested. Our results provide direct evidence for the repair of DNA lesions, extending the range of complex biochemical reactions known to occur in bacteria at frozen temperatures. Provided that sufficient energy and nutrient sources are available, a functional DNA repair mechanism would allow cells to maintain genome integrity and augment microbial survival in icy terrestrial or extraterrestrial environments.
The results from decades of studying the stability of DNA in bacteria may be summarized in two uncomplicated axioms. First, genomic DNA is not inert; the genetic material will degrade with time, and damage will accumulate unless that degradation is repaired. And second, if this degradation is not reversed, the cell will die. The repair processes that cope with DNA damage are integral to life, and it is assumed that all species express means of maintaining genetic integrity.The importance of DNA repair to cell viability motivated extensive study of the biochemistry and molecular biology of these repair processes in model organisms such as Escherichia coli (1). Although the advantages of using this species for such studies are well documented, there is a question as to whether detailed knowledge of DNA repair in E. coli as observed under standard laboratory conditions adequately represents the full spectrum of bacterial responses to DNA damage. For instance, DNA repair is an energy-intensive activity (2, 3), but microbial species in nature rarely experience optimal conditions for growth or have access to nutrient excess. Without a generous supply of energy, cells may need to generate a more measured response, rationing available resources in a manner that prioritizes the most important tasks for survival. Moreover, viability in the absence of cellular reproduction is sustained only by cells that do not accumulate a level of damage (e.g., to DNA) that exceeds a threshold beyond which effective repair is no longer possible.Genomic DNA and viable bacteria are preserved in ancient ice and permafrost for hun...