EXTREMOPHILES as Astrobiological Models. Группа авторов

The following activities have been detected using samples from both boreholes: iron and sulfur oxidizers, iron and sulfate reducers, methanogens, acetogens, methanotrophs and denitrifiers.

Figure 2.5 Bacteria detected using the CARD-FISH probe EUB338-1 at 420 mbs. (Image credit: the authors).

The results obtained so far in the MARTE and IPBSL drilling projects give us the following scenario: as groundwater encounters the volcanogenic-hosted massive sulfide (VHMS) system, both biotic and abiotic processes are triggered. Electron donors available for microbial metabolism include metal sulfides, ferrous iron, , hydrogen, nitrite and reduced organic matter. The list of possible electron acceptors includes ferric iron, sulfate, nitrate and CO₂. These compounds can support different anaerobic respiration metabolisms. This is not a complete list; further analysis of the enrichment cultures allowed us to isolate microorganisms developing in the strict anaerobic conditions detected in the subsurface [2.88] [2.67] and their physiological and genomic characterization should provide new insight into the array of metabolisms operating in the subsurface of the IPB. These results confirm the hypothesis that microorganisms are active in the subsurface of the IPB and are responsible for the extreme conditions detected in the river. This observation has important astrobiological implications [2.11] [2.43].

2.7 Methanogenesis in Non-Methanogenic Conditions

      Although methane can be produced abiotically, more than eighty per cent of the methane existing in the Earth atmosphere is generated by methanogenic archaea. With only a few exceptions, methanogenic activities are normally detected in environments with circumneutral pH and negative (reduced) redox potentials [2.66] [2.102]. These conditions are very different from those detected in the Tinto basin (acidic and high (oxidized) redox potentials). For a long time, methanogenic activities were not considered to be operating in the Tinto basin for this reason.

      After the detection of methane in the borehole fluids of the MARTE project and in the Martian atmosphere [2.46] [2.81], regular inspections for methanogenic activity were implemented in the study of the anoxic sediment of the Tinto basin. The first sampling station in which methane generation was detected was Campo de Galdérias, at the origin of the river [2.100]. Sediments from this station exhibited specific locations with negative reduced redox potential, surrounded by the high positive oxidation redox potential characteristic of the river. Pressure applied to the ground around this sampling site released gases occluded in the sediments. Microcosms using these reduced sediments showed very active methane generation after reaching negative redox potentials and a significant pH increase, following the spike with different methanogenic substrates. The highest methane production was obtained after addition of methanol [2.100].

      A second site, JL Dam, was selected for further analysis. Cores from this sampling site exhibited distinctive black bands with negative reduced redox potential and circumneutral pH among acidic reddish-brown sediments with positive oxidized redox potentials, similar to those detected in the sediments collected along the course of the river. The sequence of amplified 16S rRNA gene from the blackish bands corresponded to Methanosaeta concilii. Enrichment cultures using different methanogenic substrates allowed the identification of M. concilii using organic substrates, Methanobacterium bryantii using H₂ and Methanosarcina barkeri using methanol [2.100].

      How can we explain the development of methanogenic activities in an ecosystem in which the characteristic pH and redox potential are the opposite of the required conditions? This apparent contradiction is resolved when we analyze the results at the microscopic level. The generation of micro-niches in a semi-solid matrix, such as sediments, or even more, in a solid matrix within a deep subsurface rock, could facilitate the growth of microorganisms generating environmental conditions quite different from the restrictive ones existing in the ecosystem [2.31]. As mentioned above, the use of fluorescence in situ hybridization allowed the detection of these micro-niches in the porous rocks of the deep subsurface of the IPB, many of which included biofilms with different types of microorganisms, sharing space and metabolisms [2.31].

The presence of methanogens in an environment controlled by iron has important astrobiological implications since it could be a model for the biotic generation of Martian atmospheric methane [2.46] [2.81] [2.105]. The recurrent argument that the environmental conditions of Mars are not suitable for generating biological methane could be contradicted by the methanogenic activities detected in the sediments of Rio Tinto and the subsurface of the IPB, a geochemical and mineralogical terrestrial analogue of Mars [2.36] [2.37] (Figure 2.2).

2.8 Rio Tinto: A Geochemical and Mineralogical Terrestrial Analog of Mars

      In 2000, Christensen et al. [2.24] [2.25] reported the occurrence of extensive outcrops of hematite in the region of Terra Meridiani. This mineral is abundant in Rio Tinto as the result of the maturation of ferric acidic minerals. This enigmatic enrichment led to the selection of Meridiani as the landing site for the Opportunity rover in 2004. During the exploration of this area, Opportunity detected hematite occurring in spheroidal concretions that were named blueberries. However, the most intriguing and revealing finding was the abundance of sulfates [2.93] [2.101] [2.80] where the main mineral phase was jarosite, as detected by Mössbauer spectroscopy on board the Opportunity [2.63]. Later on, it was observed that the acidic sulfates were very extensive in different Mars regions, supporting the idea that Mars had been exposed to a low-pH episode lasting hundreds of millions of years [2.79] [2.33] [2.29], whose origin has been related to the weathering of metallic sulfides [2.34] [2.112]. Very recently, the formation of iron sulfides associated with hydrothermal materials that are similar to the hydrothermal rocks of the Rio Tinto basement was reported [2.78]. This suggests that the biogeochemical cycles of the putative biosphere that could have emerged on Mars might have been dominated by S and Fe metabolism, as is observed in Rio Tinto.

In this context, Rio Tinto becomes an excellent terrestrial reference in two aspects. On one hand, it provides direct information about the physicochemical and biological processes that are involved in the formation of the iron-rich acidic minerals such as iron oxides and sulfates [2.57] [2.58] [2.37]. On the other hand, the evolution of the acidic system over the last 30 million years is recorded in the form of alteration materials and iron-rich terraces that show the diagenetic pathways followed by the iron-rich minerals over time [2.35] [2.37] [2.41]. The association of modern and ancient deposits at Rio Tinto can provide key information to understanding the origin and maturation of the iron-rich deposits that are found in vast areas of Mars like Aram Chaos, Meridiani Planum, Valles Marineris, Mawrth Vallis and Syrtis Major [2.63] [2.79] [2.33] [2.29] [2.71]. From an astrobiological perspective, Rio Tinto shows us how biological activity is produced and recorded under extreme acidic conditions over millions of years. The modern environment and its ancient acidic materials of surface and subsurface areas show a wide diversity of biological traces, including microstructures, minerals, stable isotope signatures and molecular compounds, suggesting that these biosignatures survived the diagenesis and maturation processes over 30 million of years of geological evolution [2.43]. As discussed before, the micron-sized crystals of Fe-bearing carbonates likely produced by Acidiphilium sp. are found in the acidic sediments going from modern to the oldest ferruginous materials of over 30 million years [2.42]. Although carbonate minerals are highly unstable under the acidic conditions of Rio Tinto, mineral precipitation is favored by metabolic activity in micron-size cellular scale sites that allow net preservation in the oldest acidic materials of the basin. Furthermore, the occurrence of microbial-derived minerals is also observed associated with microbial structures in the deep subsurface of the Rio Tinto crust [2.43]. Over the course of the last 30 million years, iron and sulfur biogeochemical cycling in the basement has been recorded as carbonate-bearing microstructures