On the possibility of chemosynthetic ecosystems in subsurface habitats on Mars

“A great deal of work has been done to define the characteristics of such sites and to identify the environments that are conducive both to the sustenance of life and to the preservation of evidence of this life (McKay et al., 1996; Boston et al., 1992; Walter and Des Marais, 1993).”

“References: a1Geiss and Hess (1958), recalculated to the K-decay constants by Steiger and Jäger (1977); aEugster et al. (1997a); bBogard et al.”

“It has been proposed, on the basis of geochemical and thermodynamic considerations, that geologically derived hydrogen might support subsurface microbial communities on Mars and Europa in which methanogens form the base of the ecosyste”

“, 2013) and assuming that the necessary minerals, nutrients, and energy are present (Fisk and Giovannoni, 1999), these groundwater systems may support similar microbial metabolisms (Boston et al., 1992), including hydrogen-based methanogenesis (Chapelle et al.”

“Similarly, the apparent lack of photosynthetic life chemical forms of energy (Boston et al ., 1992; Shock, investigation of environments that support chemosynthesis on the modern Earth can enlighten our understanding of life on the early Earth and the situation that may have existed on Mars.”

“Resolving the question of the origin of atmospheric CH4 on Mars is even more challenging given that distinguishing abio- genic versus biogenic sources of CH4 in the terrestrial subsurface is still controversial (Gold, 1979; Kenney et al., 2002; Shock, 1995).”

“Microbes may remain on the surface in cryptoendolith niches [Cockell and Raven, 2004], permafrost water ice [Schulze-Makuch et al., 2005], or active in deep aquifer ecosystems [ Boston et al., 1992 ].”

“…environments may require input of electron acceptors (O2, NO 3-, SO4 2-) from the surface, but plausible scenarios exist to transport such compounds into subsurface environments on Mars if they are present at the surface (Boston et al., 1992; Fisk and Giovannoni, 1999; Michalski et al., 2013).”

“Like many astrobiologists, we seek to arrive at an understanding of the signatures of life and its workings that will have broader applicability beyond the minutiae specific to life on Earth.”

“Before the hydrogen-dependent subterranean biosphere hypothesis was proposed (Ivanov, 1990; Boston et al., 1992; Gold, 1992; Pedersen and Albinsson, 1992), it has been a general concept that all life on Earth depends on the sun via photosynthesis.”

“…Earth is presently the only body in the solar system capable of supporting a surface biosphere, but Mars, Europa, and possibly others may support vast volumes of habitable space within hundreds to thousands of meters of the surface (Boston et al., 1992; Kargel et al., 2000; Chyba & Phillips, 2002).”

“Caves on Mars could intercept subsurface groundwater and may provide windows into subsurface habitable environments, both past and present (e.g., Boston et al., 1992, 2001; Grin et al., 1998; Schulze-Makuch et al., 2005; Rasmussen et al., 2009).”

“As such, the largest and longest-lived putatively habitable environment on Mars is in the subsurface (e.g., Boston et al., 1992).”

“…very little input of organic matter from photosynthesis, they are frequently cited as possible analogues for habitable environments on early Earth and other planetary bodies (Boston et al. , 1992; Shock, 1997; Fisk and Giovannoni, 1999; McCollom, 1999; Varnes et al. , 2003; Schulte et al. , 2006).”

“Researchers also have suggested that alteration of mafic rocks could provide chemicals, such as hydrogen, to fuel chemosynthetic life (Boston et al., 1992; Stevens and McKin-ley, 1995; Kelley et al., 2005; Ferna´ndez-Remolar et al., 2008; Blank et al., 2009).”

“Several models have been developed to examine the significance of similar H 2 - and CH 4 - generating processes for chemoautotrophic life on early Earth and, potentially, Mars (Boston et al ., 1992; Lyons et al ., 2005; Oze and Sharma, 2005; Sleep et al ., 2004).”

“Viability of subsurface methanogenic organisms on Mars was suggested before the atmospheric methane was even discovered (Boston et al., 1992; Weiss et al., 2000; Kral et al., 2004).”

“…Corliss et al., 1981]; their existence on Mars, and the ability to provide some communication between the atmosphere and the crust, opens up the possibility that they might have provided a location for an independent origin of life at some point in Mars’ history [Chang, 1988; Boston et al., 1992].”

“Analogue for the creation of habitable environments on Mars; geothermal features and mineral deposits; caves; volcanoes; preservation of life; extremophiles (Boston et al. 1992; Gudmundsson et al. 1997; Bourgeois et al. 1998; Chapman et al. 2000; Preston et al. 2008; Herrera et al. 2009; Cousins & Crawford 2011) (11)…”

“…may represent analogues of the earliest biological communities to inhabit the Earth or of microbial communities that might exist on other planetary bodies such as Mars and Europa (e.g. Boston et al ., 1992; Jakosky & Shock, 1998; Fisk & Giovannoni, 1999; McCollom, 1999; Martin & Russell, 2003).”

“Liquid water may be possible in the subsurface of present-day Mars (e.g., Boston et al., 1992; McEwen et al., 2011; Ojha et al., 2015).”

“…of the more promising possibilities for Mars is that, during the planet's early transition to a colder climate, life may have adapted to a subterranean existence where warmer temperatures and the potential presence of groundwater has enabled it to persist to the present day (Boston et al. 1992).”

“A possible source of methane has been attributed to serpentinization, a fluid–rock reaction common in ultramafic rocks that has been hypothesized to occur on Mars (Boston et al., 1992; Formisano et al., 2004; Atreya et al., 2007; Oze and Sharma, 2007).”

“The subsurface of a rocky planet such as the Earth often contains redox gradients at a variety of spatial scales, which could provide energy for chemolithotrophs on Mars (Boston et al., 1992).”

“…1997; Shock & Schulte, 1998), and to developing search strategies for ancient biosignatures and extant life on Earth, Mars, Venus and Europa (cf. Boston et al ., 1992; Jakosky & Shock, 1998; Fisk & Giovannoni, 1999; McCollom, 1999; Zolotov & Shock, 2004; Sleep et al ., 2004; Schulte et al .,…”

“Even in the future when the remote detection of biosignatures is possible, it will be difficult to detect subsurface life (Boston et al., 1992; Gaidos et al., 1999; Jones et al., 2011; McMahon et al., 2013) that does not interact with the planet’s atmosphere and is completely sustained by free energy based on geochemi…”

“…alive to this day far underground, where the internal heat of the planet melts the underside of the permafrost shell into a liquid water aquifer (Boston et al., 1992), and has been proposed as the source of the recently-detected atmospheric methane (Formisano et al., 2004; Krasnopolsky, 2006).”

“Furthermore, extraterrestrial magnetite in the Martian meteorite ALH84001, which in some respects re-sembles biogenic magnetite formed on Earth, has been used as evidence supporting past biologic activity on Mars (McKay et al. 1996).”

“It is conceivable that such depths could support chemolithotrophic organisms (Boston et al ., 1992).”

“Such communities can serve as models for potential ecosystems on other worlds, such as Mars and Europa ( e.g. , Boston et al., 1992; Fisk and Giovannoni, 1999).”

“Accordingly, Mars (12) and Europa (77) may still have subsurface habitable conditions.”

“Thus, potentially extant methanogens are likely to be restricted to the martian subsurface—in endolithic ecosystems within pore spaces of sediment and rock (Boston et al., 1992) and in ice and permafrost (Tung et al., 2005).”

“, the subsurface) that could enable the existence of life (4).”

“Mars appears to meet the environmental conditions necessary to support life deep below the surface (hundreds of meters to several kilometers) where temperatures are high enough to allow liquid water (Boston et al. 1992).”

“The hydrothermal energy sources needed for chemoautotrophy on Earth would likely have been available on Mars (Boston et al., 1992).”

“A potential habitat for existence of methanogens on Mars might be a geothermal source of hydrogen, possibly due to volcanic or hydrothermal activity, or the reaction of basalt and anaerobic water (Boston et al., 1992; Stevens and McKinley, 1995; Chapelle et al., 2002), carbon dioxide, which is abundant in the martian…”

“…focus in light of data being returned from the planet and growing knowledge about life in extreme environments (e.g., McKay and Davis, 1991; Boston et al., 1992; Jakosky and Shock, 1998; Cabrol et al., 1999; Weiss et al., 2000a; Fairén et al., 2005, 2010; Schulze-Makuch et al., 2005;…”

“The deleterious surface of present-Mars has long since been recognized as a reason why habitable conditions, if they exist on Mars today, are likely to be localized to the deep subsurface (Boston et al. 1992).”

“It is thought that caves on Mars would retain liquid water longer than the surface, and the subsurface would offer protection from the harsh solar radiation, providing a possible refuge for life or the remnants of life forms (Boston 2010; Léveillé and Datta 2010; Northup et al. 2011; Popa et al. 2012).”

“…heated liquid water for much of this time, representing a long-lived habitat that could have exchanged living cells with shorter-lived habitats at the surface (Boston et al., 1992; Clifford et al., 2010; Ehlmann et al., 2011; Fisk & Giovannoni, 1999; Thomas et al., 2017; Travis et al., 2003).”

“A significant body of literature exists on the potential habitability of different martian environments through time (e.g., Boston et al., 1992; Jakosky et al., 2003; Nisbet et al., 2007; Squyres et al., 2008; Tosca et al., 2008; Smith et al., 2009; Fairén et al., 2010; Johnson and Pratt, 2010).”

“Diffusion of H2 and CO downward into the Martian regolith could provide a subsurface biosphere with a continual source of energy for metabolism [Boston et al., 1992; Weiss et al., 2000].”

“More importantly, low-temperature aqueous alteration processes (such as serpentinization) associated with mafic and ultramafic rocks on Earth are thought to be geologically similar to those occurring on Mars (e.g., Boston et al., 1992; Ming et al., 2006; Wyatt and McSween, 2006).”

“It has been proposed, in recognition of environmental flexibility of microorganisms on Earth, that some microorganisms with specific physiological capabilities could survive on Mars (Friedmann and Ocampo-Friedmann, 1984; Boston et al ., 1992; McKay et al ., 1992a,b; Stevens and McKinley, 1995).”

“Several studies have attempted to trace the evolution of Martian habitability over time (Cockell et al. 2000; Fairén et al. 2010; Cockell 2014) and identify regions where life could have persisted (Boston et al. 1992; Davila & Schulze-Makuch 2016).”

“However, many authors have suggested that the subsurface of Mars might be conducive to life ( e.g ., Boston et al ., 1992, 2001; Carr, 1996; Nealson, 1997; Shock, 1997; Sleep and Zahnle, 1998; Fisk and Giovannoni, 1999).”

“Contrary to a theoretical primordial ocean, there is ample evidence that volcanic aquifers formed on Mars (e.g., Boston et al., 1992; Farmer, 1996; Mouginis-Mark and Christensen, 2005; Cousins and Crawford, 2011; Rodrı́guez and van Bergen, 2015).”

“Further,certaindeepsubsurfaceenvironmentsonEarth can serve as analogues to saline subsurface environments on other planets like Mars [6–12].”

“Deep subsurface anaerobic life ( e.g., methanogens) beneath the martian cryosphere ( * kilometers depth) is also possible if liquid water and an energy source ( e.g., the radiolysis of water; Chivian et al., 2008) are available (Boston et al., 1992; Szewzyk and Szewzyk, 1994).”

“[17] speculated that chemoautolithotrophic communities could exist in this”

“Subsurface environments and martian caves, which could contain permanent ice (Williams et al., 2010), have been proposed as astrobiological target sites (Boston et al., 1992; Boston, 2010; Northup et al., 2011).”

“Specifically to Mars, anaerobic chemolithoau-totrophs can potentially inhabit subglacial volcanic environments through the oxidation of inorganic compounds and fixation of carbon dioxide as the carbon source (Boston et al., 1992).”

“On Earth, the only biogenic source of methane is methanogenesis, and thus, methanogenic archaea are regarded as model organisms for possible life on Mars (Boston et al., 1992; Weiss et al., 2000; Jakosky et al., 2003; Morozova et al., 2007).”

“On Mars, caves may be especially important forms of shelter, given the harsh radiation environments at the surface (Boston et al., 1992, 2004; Leveille and Datta, 2010; Schulze-Makuch et al., 2005).”

“Any surface dwellers would be dormant during the currently dry Martian time period, perhaps aside from some suitable niche environments such as in lava caves (Boston et al. 1992).”

“If the surface is inhospitable, many have suggested (Boston et al. 1992) that the subsurface may hold liquid water aquifers that support chemosynthetic life.”

“Since robotic missions to Mars are currently under development (Mars Exploration Joint Initiative signed in 2009 between US space agency, NASA, and European Space Agency, ESA), microbiological studies in Earth’s caves can bring new insights in the search for life on Mars since researchers will need criteria with which…”

“Extrapolating our knowledge of terrestrial biotic sources to Mars, many consider methanogens (a type of CH 4 - producing archaean microbe) as a probable analogue to martian life-forms (Boston et al. , 1992; Weiss et al. , 2000; Schulze-Makuch et al. , 2008).”

“It has been suggested that after surface conditions on Mars became hostile for life, life may have found a refuge in the martian subsurface (Boston et al. , 1992).”