One way to have liquid water on Mars at shallow depths would be through subglacial volcanism. Such volcano-ice interactions could be going on beneath the polar caps of Mars today, or even within the adjacent permafrost around the margins of the ice caps. Basalt lava fields are common on the Martian surface, and some cinder cones have been found near the polar caps. The rover traces on terrestrial ash fields and the Martian surface, as well as the chemical composition of basalts on Earth and Mars, are similar (Arvidson et al. 2004; Squyres et al. 2006). This is why research of terrestrial volcanoes, including the permafrost study, is expected to be a valuable step in understanding extraterrestrial volcanoes as one of the Earth's analogues, close to the extraterrestrial environment, represented by active volcanoes in permafrost areas. The key question concerning this volcanic permafrost model is the age of Martian volcanoes.
On Earth, most volcanoes are located in areas of collision of oceanic and continental plates. Despite active volcanism, permafrost often exists on slopes of high-elevation or high-latitude volcanoes (Kellerer-Pirklbauer 2007) in places such as Hawaii (Woodcock 1974), Iceland (Etzelmüller et al. 2007), Mexico (Palacios et al. 2007), Peru, North America, and Antarctica. On Mars, plate tectonics is not observed; nevertheless, more than 50% of Mars surface is known to be covered by rocks of volcanic origin, and displays of volcanism are observed everywhere (Carr 1996). The largest volcanoes are in three broad provinces: Tharsis, Elysium and Hellas. The regional elevations of Tarsus and Elysium are one of the youngest formations of Mars. But it must be mentioned that while we have no lava samples, the ages of volcanoes on Mars can only be roughly estimated by the number of impact craters, with newer regions having fewer craters (Fig. 21.1).
Tharsis is possessed of the biggest volcano in the Solar System - Olympus, which covers an area of 600 km in diameter and is 27 km high. The huge sizes of Martian volcanoes are the consequence of the stopped plate tectonic, when eruptions take place at the same point. Some volcanoes of Tarsus province undoubtedly were active in the last billion years, in that the least-cratered surfaces of lava flows of Olympus volcano were dated by Carr (1996) as a few hundred million years old or even less as ~30 million years.
The main question is: do such ecological niches as volcanoes and associated environments contain microbial communities? The task is to find thermophilic
microorganisms associated with volcanoes that have been deposited with products of eruption, and that have then survived in permafrost after the freezing of scoria and ash. Our study was carried out on the Kluchevskaya volcano group (Kamchatka Peninsula) which was formed starting from the late Pleistocene (Braitseva et al. 1995). The volcano group consists of Klyuchevsky, Bezymianny, Ushkovsky and Plosky Tolbachik, which are active volcanoes, and others that are not active today. Most of these volcanoes are higher than 3,000 m above sea level. At these points, the permafrost thickness is estimated to be 1,000 m. The mean annual ground temperature decreases from -1°C on the lower boundary of permafrost (~900 m) to -2.6°C at 1,300 m and -7°C at 2,500 m (Abramov and Gilichinsky 2008).
During the eruptions of these volcanoes in the last 2,000-3,000 years, thick (1216 m) layers of volcanic ash, sand and scoria were accumulated on the elevations occupied by permafrost, and at that time became frozen. The last eruption was in 1975-1976, and ~500 km2 were covered by scoria and ash; three new cinder cones and lava fields were formed (Fedotov and Markhinim 1983). The cores extracted from the borehole crossing these young volcano deposits contained biogenic CH4 (up to 1,900 |l kg-1) and viable bacteria, including thermophilic anaerobes (103 cells g-1), and among them, methanogens growing on CO2 + H2. Because thermophiles have not previously been found before in permafrost, the only way for these bacteria to appear within frozen volcanic horizons is through the eruption of a volcano or its surrounding associated strata. The important conclusion is that thermophiles might survive in permafrost and even produce biogenic gases. For future space missions, the permafrost volcano areas are promising test sites, and provide opportunities to study analogues of possible Martian ecosystems. Their original microbial communities represent an analogue for communities that probably might be found around Martian volcanoes. The methanogenic archaea found at such sites can likely adapt to temperatures <0°C, as has been found with other studied groups of anaerobes.
Results of the 2001 mapping of the Martian surface for the presence of chlorine by GRS spectrometer aboard the Mars Odyssey spacecraft showed significant variations of chlorine content from 0% to 1% (Keller et al. 2006). The lowest temperature at which salt-rich Martian ground water may still be in a liquid state is about -60°C (Zent and Fenale 1986). Taking into account this statement, brines may be found on Mars at inaccessible depths or at low latitudes. Areas with mean annual temperatures equal to or higher than -60°C are only found at the 30° latitudinal belt. At these latitudes Malin and Edgett (2003) found so-called gullies, freshly incised channels a few metres across. These indicate that a fluid had eroded the soil. Water is the most likely candidate responsible for the origin of these very young gullies (their age is estimated to be <1 million years), but the source of liquid water on a frozen planet is a mystery. It is quite possible that the source of liquid water is underground brine. Obviously gullies are high-priority targets for the search of life on Mars. Unfortunately, it is impossible to land a rover on gullies because of engineering constraints. But nearby plains, which contain material accumulated from gullies, may still contain cryopeg microorganisms in a frozen state.
Terrestrial cryopegs were exposed by boreholes along the Polar Ocean coastal zone, with mean annual ground temperatures varying between -2 and -12°C on Cape Barrow (Alaska), the Barents Sea coast, the Yamal Peninsula (surrounded by the Kara Sea) and the Kolyma lowland (East Siberian Sea). At the last site, cry-opegs are confined to a 20 m-thick marine horizon, sandwiched between non-saline terrigenous layers at depths of 40-50 m below the tundra surface (the mean annual ground temperature varying from -9°C to -11°C). Finely dispersed sand and sandy loams were deposited in shallow lagoons at temperatures slightly above 0°C. After regression of the Polar Ocean, the water-bottom sediments were exposed sub-aerially and froze. Because of the pressure caused by freezing, water was released as the freezing front penetrated downward. This was accompanied by a freezing out of salts in the water, to form lenses of overcooled sodium chloride brines with salinities of 170-300 g l-1. Later, the marine horizon was buried by a 15-20 m thick unit of lacustrine-alluvial late Pleistocene icy complex that was built up under harsh climate conditions, was syngenetically frozen and has never thawed. Within the marine horizon, the lenses occur at different depths, their thickness varying from 0.5 m to 1.5 m and their width from 3 m to 5 m. Some of them represent non-artesian water, and some exist under low pressure with a hydrostatic head. Different salinities of the brines confirm their lenticular nature and isolated bedding.
Bacteria isolated from cryopegs were not only adapted to subzero temperatures but also tolerant to the high salt concentrations. In addition, the detected microorganisms were both halophilic and psychrophilic, and such organisms have never been isolated from natural habitats. In the cold saline conditions of cryopegs, special communities were formed. Active adaptation to low temperatures of already studied bacteria gives hope that fully active and reproducing bacteria can be discovered in saline habitats at subzero temperatures. Biotic survival in the aquatic environment on a geological time scale indicates unknown bacterial adaptations. The microbial activity detected in cryopegs at temperatures as low as -15°C documents the fact that subzero temperatures themselves do not exclude biochemical reactions, and provides reason to conclude that in overcooled water the metabolic strategy of microbial survival operates, and that this strategy does not accept that cells can multiply in situ (Gilichinsky et al. 2005).
The unfrozen water films in terrestrial permafrost, high in salts, represent the same micro-brines, even in ultra-fresh sediments, and most investigators indicate that at least part of the permafrost community (20%, according Steven et al. 2006) grows at temperatures between -2 and -10°C (Shcherbakova et al. 2004, 2005; Ponder et al. 2005; Rodrigues et al. 2006; Bakermans et al. 2006).
Biotic survival in the late Cenozoic overcooled high-salt aquatic environments for 100,000 years and in Permian-Triassic saliniferous sediments 250 million years old (Dombrowskii 1963; Vreeland et al. 2000; Stan-Lotter et al. 2002, etc.) indicate unknown bacterial adaptations. What is more, in the cold saline conditions of over-cooled brines, special communities were formed, and some of them were novel species. Because the Opportunity rover detected rocks with high S concentrations (Rieder et al. 2004), it is interesting that sulfate reducers detected in cryopegs are halophilic and psychrophilic organisms at once that have never been isolated from natural habitats. The salt tolerance may be associated with cold tolerance on a geological scale. Experimental data showed that in the presence of 25% NaCl, halophiles survive better than non-halophiles under low (-20 to -80°C) temperatures, and extreme halophiles require NaCl concentrations above 15.6% (w/v) for growth (Rothschild and Mancinelli 2001; Mancinelli et al. 2004).
Basalt is not the only rock component of the Martian surface. Stratified sediments, presumably of marine origin, were discovered on Mars, which makes it different from the Moon. It is suggested that in the Noachian epoch the northern lowlands were occupied by ocean, and a range of cratered depressions represent seas, where marine sedimentation took place (Baker et al. 1991). These bottom sediments with high solute content might represent the opportunity for free water existing as brine lenses within permafrost, formed when Mars became cold. Mars is a cryogenic planet where free water only has the opportunity to exist in the presence of high solute content, probably as brine lenses within permafrost. These brines, like their terrestrial analogues, may contain microorganisms adapted to subzero temperature and high salinity. This is why the unique halo/psychrophilic community preserved hundreds of thousands of years in mineral-enriched Arctic cryopegs and in hundreds of million of years old salt deposits, provide the plausible prototype for Martian microbial life (Gilichinsky et al. 2003) either as an "oasis" for an extant, or the last refuge of an extinct biota (Mancinelli et al. 2004).
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