Permafrost

The most inhabited and ancient part of the cryosphere, permafrost, is defined as permanently frozen ground and underlies about a quarter of the Earth's land surface. This considerable frozen mass, up to several hundreds of meters deep, where microorganisms are adsorbed on organic or mineral particles, harbors a high level (up to dozen millions of cells per gram) of various morphological and ecological viable microbial groups that have survived under permafrost conditions since the time of its formation. They have been isolated from frozen cores with permanently constant ground temperatures of -1 to -2°C near the south border of permafrost in Siberia, from lowest temperatures in the Arctic (-17°C on the most northern latitude: 80°N in NWT, Canada; Steven et al. 2007) and Antarctica (-27°C on the most southern latitude: 78°S in Dry Valleys; Gilichinsky et al. 2007a), down to 400 m depth in Mackenzie Delta (Gilichinsky 2002), and up to 4,700 m elevation in Qinghai-Tibet Plateau (Zhang et al. 2007). The age of the isolates corresponds to the longevity of the permanently frozen state of the sediments, and dates back from a few thousand to 2-3 million years in northeastern Arctic, and to 5-8 million years and probably older in Antarctica (Gilichinsky et al. 2007a). This great mass of the only known living communities preserved over a geologically significant time is peculiar to permafrost only, and represents a wide range of possible cryogenic ecosystems for planets without obvious surface ice.

Unfrozen water films play the leading role in the preservation of microorganisms. These films coat the soil particles and protect the viable cells adhered onto their surface from mechanical destruction by growing crystals of intrusive ice, and make possible the mass transfer of microbial metabolic by-products in permafrost, thus preventing the cells from biochemical death (Gilichinsky et al. 1993). Therefore, the unfrozen water might be considered as a main ecological niche where the microorganisms might survive. In fine dispersed Arctic permanently frozen sediments at temperatures of -3 to -12°C, the amount of unfrozen water can be estimated as 3-8% of total water mass.

Because of temperatures below -20°C in the coarse Antarctic Valley's sands, the unfrozen water amounts are so small that the instrumental methods fail to record them. The unfrozen water must therefore only be firmly bound to "liquid" water with binding molecules, and indicates a "biologically dry" environment. Based on experiments, Jakosky et al. (2003) calculated that liquid water can exist as ice grain-dust grain, and ice grain-ice grain contacts above ca. -20°C. Below this temperature, water would not be present in soils in sufficient thickness and amount to physically allow the presence of microorganisms, i.e., this temperature is the lowest at which life can function. Both conclusions are not fully clear at this moment, and not quite correct. Firstly, because for Victoria Valley it was determined that the amount of unfrozen water is 2% at -20°C and 1.5% at -30°C due to the salt content. The same amount of unfrozen water is expected in Beacon Valley, where the soil has a higher salt content (Gilichinsky et al. 2007a). Secondly, numerous studies have shown that microorganisms metabolize at extremely low temperatures in ice and permafrost, i.e., between -10°C and -20°C (Rivkina et al. 2000, 2004; Carpenter et al. 2000; Bakermans et al. 2003; Junge et al. 2004), and down to -28°C and -35°C (Rivkina et al. 2005; Panikov and Sizova 2007).

Annual maximum surface temperatures in Martian permafrost regions may rise above this level and above 0°C (for hours) up to 75° latitude in the south and up to 50° latitude in the north (Tokano 2003). But temperature at the depth of ground ice burial never exceeds -20°C. At the same time, the Gamma Ray Spectrometer onboard the Mars Odyssey spacecraft observed some areas with rather high concentrations of Cl (Keller et al. 2006) in the upper 10-20 cm of ground, which promises the existence of enough unfrozen water at some salt-rich geologic locations to protect viable cells. This makes the near surface past and present permafrost layers potentially favorable sites to search for evidence of life similar to cryptoendolithic microbial communities within Antarctic sandstone (Friedmann 1982). Probably, in such ecological niches, thin brine films might be formed within Martian permafrost, as proposed by Dickinson and Rosen (2003) in their studies of minerals and accumulation of ground ice on Table Mountain, Sirius Group sediments.

From the astrobiological point of view, it is important that permafrost (where 92-98% of water is in a solid state) and subzero temperatures slack off the cumulative effects of background terrestrial gamma radiation on cells for thousands and millions of years. The lower the water content and the rate of metabolic processes, the less are the radio lesions of biological objects. This is why the irradiation sensitivity of soil microorganisms at temperatures above 0°C differs from the sensitivity of microorganisms preserved in permafrost. The response of permafrost microorganisms to irradiation in non-frozen and frozen state is different. At an irradiation dose of 1 kGy, there is one magnitude difference in the number of viable cells between non-frozen and frozen samples (Gilichinsky et al. 2007b), and the cell survival rate was estimated to be 1% and 10% of the initial cell number in non-frozen and frozen samples, respectively. In the model gamma-irradiation, a dose of 5 kGy was lethal for the microbial community in non-frozen samples.

Direct in situ measurements in boreholes on the Eurasian northeast showed that the dose received by the immured bacteria in frozen sands and loams is about 2 mGy per year. Taking into account the oldest (~3 million years) late Pliocene age of permafrost and bacteria, the total dose received by cells would be 5-6 kGy. Under these conditions, most of the cells survived. This fact shows that freezing increased the cells' resistance to radiation, and demonstrates the uniqueness of permafrost as an environment where microorganisms display a high resistance to radiation. From these data, the dose from radionuclides diffused through permafrost is not fatal, but should be large enough to destroy the DNA of ancient viable cells. Their viability and growth implies the capacity for DNA repair, probably in the frozen environment, i.e., at the stable rate of damage accumulation, a comparable rate of repair also exists (Rivkina et al. 2004). This is why the "biologically dry" (at temperatures below -20°C) Antarctic permafrost, with extremely low and inaccessible organic matter, is nevertheless inhabited by up to 103-105 viable cells g-1, providing an analogue for Martian ecosystems.

Antarctic ice-free areas are the best terrestrial analogues of Martian permafrost for several reasons. The first one is that the temperature conditions in Antarctica are closest to conditions on Mars. For example, the annual surface temperatures on 40° latitude south, which is the warmest place with permafrost on Mars, includes a maximal temperature of 15°C, a mean temperature of -65°C, and a minimal temperature of -130°C (Tokano 2003). In Antarctic Dry Valleys (Beacon Valley), the maximal surface temperature is the same, mean and minimal temperatures are

-23°C and -45°C respectively. Due to extremely low temperatures in Antarctica, phase transfer of H2O occurs without melting, so that sublimation is the main factor controlling the stability of ground ice exactly as on Mars. The second similarity is double-layered ground with a dry layer at the top and an ice-rich layer at the bottom, which together with the absence of vegetation and soils make the Antarctic landscape Mars-like. The third similarity is permafrost age. The development of global ice-rich permafrost is attributed to post-Noachian time (nearly 4 billion years ago). Permafrost in some areas related to Hesperian mega outflow and Amazonian volcano-ice-water geomorphic features may be substantially younger (up to 1 billion years). Mars is known to be a still geologically active planet. Aeolian transport of dust, together with the presence of a global water cycle between atmosphere and ground ice, lead to the permanent development of syncryogenic permafrost. But, as there is no addition of any new possible life-containing material from volcano eruptions or underground water (excluding local spots of possible groundwater seepage in gullies), the material of this modern permafrost still comes only from old Noachian-Hesperian-late Amazonian rocks.

Antarctic desert deposits beneath the frosty active layer are unexpectedly icy, i.e., of the same order as the more humid Arctic area. This means that ground ice instability due to the processes of sublimation at ultra-low humidity and air temperature is in a very thin surface layer only, and revises the earlier thesis of dry Antarctic permafrost. This is why we can also expect the existence of high icy subsurface layers on Mars.

Permafrost on Earth and Mars vary in age, from a few million years found in the north hemisphere on Earth (Sher 1974) to a few billion years on Mars (Carr 2000; Baker 2004; Tokano 2005); such a difference in time scale would have a significant impact on the possibility of preserving life on Mars, because the number and biodiversity of microorganisms decrease with increasing permafrost age. This is why the longevity of life forms preserved within the Arctic permafrost can only work as an approximate model for Mars. The suggested age of Antarctic permafrost (~30 million years) is somewhat closer to that of Mars. A number of studies indicate that the Antarctic cryosphere began to develop soon after the final break-up of Gondwana and the isolation of the Antarctic continent. It is believed to have been started on the Eocene-Oligocene boundary (Barrett 1996; Wilson et al. 1996; DeConto and Pollard 2003). The discussion of Neogene stability has focused mainly on the state of the ice sheet, which is the most variable part of the cryosphere. Permafrost is the more stable end-member of the cryosphere, and the conditions needed for ice degradation, even if they existed in a climatic optimum, are not sufficient to thaw the permafrost. Permafrost degradation is only possible when mean annual ground temperatures, -28°C now, rise above freezing, i.e., a significant warming to 25°C or above is required to degrade the permafrost once formed. There is no evidence to date of such significant temperature variation, which indicates that the Antarctic climatic and geological history was favorable to the formation and persistence of pre-Pliocene permafrost. For example, early Oligocene sediments (38 million years) obtained by the Cape Rogers drilling project contain cold tundra pollen spectra. Antarctic permafrost may, therefore, be more than 30 million years old

(Gilichinsky et al. 2007a) and date from Antarctic ice sheets predicted in early Oligocene times (Zachos et al. 2001).

Viable microorganisms were isolated from the cores taken in Beacon Valley from beneath an 8.1 million years volcanic ash layer (Gilichinsky et al. 2007a) that has been interpreted as a direct air-fall deposit (Sugden et al. 1995), and this age is supported by several studies (Schaefer et al. 2000). The age of isolated communities remains controversial, because recent investigation has questioned this age relationship, and calculations indicate that sublimation rates would be too high for the ice to persist for 8.1 million years (Ng et al. 2005). However, Bidle et al. (2007) isolated microorganisms from the ice beneath this ash; these authors again affirm an age of 8.1 million years. From an age perspective, the Glacigene Sirius Group sediments on Mount Feather may be even older. They were estimated to be at least 2 million years in age (Webb and Harwood 1991) and possibly as old as 15 million years (Marchant et al. 1996). The age for the superficial deposits where bacteria were sampled in the permafrost is 5 million years (Wilson et al. 2002). If this age is correct, these are, to date, the oldest confirmed viable microorganisms discovered in permafrost and the oldest viable communities reported on Earth (Gilichinsky et al. 2007a).

It would be advantageous to locate relics of the oldest Antarctic permafrost. These are possibly to be found at the high hypsometric levels of ice-free areas such as the Dry Valleys, along the Polar Plato and Trans-Antarctic Mountains, and on Northern Victoria Land. It is desirable to date the layers within them and to test for the presence of viable cells. The limiting age, if one exists, within the most ancient Antarctic permafrost cores, where the viable organisms were no longer present, could be established as the age limit for life preservation within permafrost at subzero temperatures. Any positive results obtained from Antarctic microbial data will extend the geological scale and increase the known temporal limits of cryobio-sphere, i.e., duration of life preservation.

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