Carbonates

(1) Carbonates in subsurface environments: The carbonates in ALH84001 formed in a subsurface environment, in this case in an igneous rock. The McKay team had identified globular features and lineations of such features in the carbonate deposits of ALH84001 that they interpreted as nanobacteria. Carbonates are a mineral phase whose formation may be mediated by microbial metabolisms (Riding, Reference Riding1991; Spadafora et al., Reference Spadafora, Perri, McKenzie and Vasconcelos2010), often preserving physical biosignatures, such as stromatolites as well as, occasionally, individual microbial cells (e.g. Fig. 3a; Perri et al., Reference Perri, Tucker and Spadafora2012). Biomineralization may be a passive process in which a mineral forms as a result of microbial metabolic processes affecting its immediate environment, for example, changing pH, or the production of metabolites that then combine with various ions in solution. It may also be actively induced, for instance, when bacteria control the Ca²⁺ content in their cells by using a cross-membrane proton pump to eliminate excess ions. The expelled Ca²⁺ then combines with CO₃⁻ in solution to precipitate around the cell walls (Bosak and Newman, Reference Bosak and Newman2003). In the subsurface, carbonate deposits can form naturally in certain carbonate cave systems (Fig. 4b; Cacchio et al., Reference Cacchio, Ercole, Cappuccio and Lepidi2003), as well as from drip water in mines (García et al., Reference García, Márquez and Moreno2016). These environments are aerobic to microaerophilic. Fossilization of the bacterium Acinetobacter gyllenbergii, isolated from Columbian mines, was demonstrated experimentally with the precipitation of carbonate around cell walls (García et al., Reference García, Márquez and Moreno2016). Subsurface carbonates also form in non-carbonate rock lithologies. For example, carbonates in fractures in granitic host rock formed as a result of microbial oxidation of methane (Drake et al., Reference Drake, Åström, Heim, Broman, Åström, Whitehouse, Ivarsson, Siljeström and Sjövall2015). The latter preserves the most extreme ¹³C depletion recorded to date (−125‰) as a result of the incorporation of C from biogenic methane in this energy-limited and C-poor environment. The carbonates also host lipid-derived organic components emanating from a microbial consortium comprising anaerobic methane-oxidizing archaea and sulphate-reducing bacteria (SRB). Note, however, that the biosignatures are confined to carbon-bearing mineral phases (clays) occurring at the boundaries of the calcite grains, not within the carbonate grains themselves.

In the case of the ALH84001 meteorite, it would in theory be possible for microorganisms to mediate carbonate precipitation, but it seems more likely that such processes are limited to heterotrophs. As these organisms obtain their energy and nutrients from the degradation of pre-existing carbon, one could hypothesize that such microorganisms were washed into fractures in lava flows at the surface of Mars. However, in a subsurface, oligotrophic environment without a primary carbon source, it is questionable as to whether the microorganisms would have been able to metabolize and produce a carbonate deposit. Nevertheless, similar to the precipitates in the ALH84001 meteorite, Benzerara et al. (Reference Benzerara, Menguy, Guyot, Dominici and Gillet2003) described nano-sized bacteriomorph crystallites of carbonate in a terrestrial weathering phase of pyroxenes in the Tatahouine meteorite, in this case associated with terrestrial microbes. They concluded that, while the formation of the crystallites was microbially-induced, the structures in themselves were chemical precipitates, i.e. abiotic growth, not fossilized microbes.

(2) Surface carbonate deposits: The majority of known microbially-mediated carbonate formation occurs in subaerial environments, in particular in relationship with phototrophic microbial mats resulting in tabular or three-dimensional stromatolitic structures (Warthmann et al., Reference Warthmann, van Lith, Vasconcelos, McKenzie and Karpoff2000; Dupraz et al., Reference Dupraz, Reid, Braissant, Decho, Norman and Visscher2009; Bosak et al., Reference Bosak, Knoll and Petroff2013). While it is unclear whether Martian life could have reached the evolutionary state of phototrophy owing to the phenomenon of punctuated habitability (Westall et al., Reference Westall, Campbell, Bréhéret, Foucher, Gautret, Hubert, Sorieul, Grassineau and Guido2015a), we cannot completely discount this possibility. Therefore, a biosignature of particular relevance for anaerobic early Mars is the microbial biomineralization of carbonate mediated by consortia of anaerobic phototrophs and their accompanying heterotrophic degraders, such as SRB. In this case, SRB activity creates the chemical conditions for the precipitation of carbonate by increasing alkalinity in the environment such that Ca²⁺ ions released from microbial extracellular polymeric substances (EPS), an important component of phototrophic biofilms and mats, react with the CO²⁻ dissolved in the aqueous phase to form CaCO₃. SRBs in such consortia precipitating nanocrystals of aragonite and CaSO₄ within degraded organic matter were documented from Mars-analogue, shallow water volcanoclastic sediments dated to 3.33 Ga from the Barberton Greenstone Belt (Westall et al., Reference Westall, de Vries, Nijman, Rouchon, Orberger, Pearson, Watson, Verchovsky, Wright, Rouzaud, Marchesini, Severine, Reimold and Gibson2006a, Reference Westall, Cavalazzi, Lemelle, Marrocchi, Rouzaud, Simionovici, Salomé, Mostefaoui, Andreazza, Foucher, Toporski, Jauss, Thiel, Southam, MacLean, Wirick, Hofmann, Meibom, Robert and Défarge2011).

Substantial carbonate precipitations in the form of mounds occur in association with cold methane seeps, as well as white smoker vents (Fig. 4a). Methane seeps are widespread and are found in the terrestrial rock record throughout the Phanerozoic (Barbieri and Cavalazzi, Reference Barbieri, Cavalazzi, Seckbach and Walsh2008). They host anaerobic chemosynthetic communities that oxidize methane and sulphide to obtain energy, using dissolved CO₂ as their carbon source. An increase of pH value driven by their metabolisms leads to the precipitation of calcium carbonate, as in the phototrophic mat communities described above. Although carbonate is formed by these processes, it is rare for individual cells to be preserved although fossil microbial filaments and mats have been documented within cold seep carbonate deposits of Devonian age from Morocco (Cavalazzi, Reference Cavalazzi2007; Cavalazzi et al., Reference Cavalazzi, Barbieri and Ori2007).

(3) Carbonates on Mars: Spectral analysis from orbit of the surface of Mars has detected carbonates associated with aqueous weathering profiles across the planet's Noachian terranes (pre 3.7 Ga), suggesting a warmer, wetter context for their formation (Bultel et al., Reference Bultel, Viennet, Poulet, Carter and Werner2019). These detections are associated with surficial weathering profiles, i.e. environments in which nutrients may have been lost by leaching, thereby reducing habitability (Duddy, Reference Duddy1980; Nesbitt et al., Reference Nesbitt, Markovics and Price1980), although such environments on the modern, oxygenated and highly habitable Earth host a diverse array of life. At the ExoMars 2022 Oxia Planum landing site, there is a spectral suggestion of carbonate associated with phyllosilicates (Mandon et al., Reference Mandon, Parkes Bowen, Quantin-Nataf, Bridges, Carter, Pan, Beck, Dehouck, Volat, Thomas, Cremonese, Tornabene and Thollot2021) although the exact environment of deposition in this case has yet to be elucidated, whether weathering, lacustrine or marine (Quantin-Nataf et al., Reference Quantin-Nataf, Carter, Mandon, Thollot, Balme, Volat, Pan, Loizeau, Millot, Breton, Dehouck, Fawdon, Gupta, Davis, Grindrod, Pacifici, Bultel, Allemand, Ody, Lozach and Broyer2021). On the other hand, Jezero crater, the landing site of the Mars 2020 Perseverance rover, displays carbonates in association with a variety of interpreted paleoenvironments, including weathering profiles of volcanic ash, as well as marginal lakeshore and/or fluvial precipitations of carbonate that are compared to carbonate reefs, microbialites or tufa, having the potential to preserve the kinds of biosignatures described above (Horgan et al., Reference Horgan, Anderson, Dromart, Amador and Rice2020). Similarly, Franz et al. (Reference Franz, Mahaffy, Webster, Flesch, Raaen, Freissinet, Atreya, House, McAdam, Knudson, Archer, Stern, Steele, Sutter, Eigenbrode, Glavin, Lewis, Malespin, Millan, Ming, Navarro-González and Summons2020) evoke carbonate in the endogenous carbon cycle of Gale crater (Fig. 5). The main problem with carbonates is their propensity to corrode under the acidic weathering conditions proposed for early Mars, which had a thicker CO₂ atmosphere than today (Viennet et al., Reference Viennet, Bultel and Werner2019). Such conditions would lead to the destruction or significant alteration of potential biosignatures.

Fig. 5. Possible carbon (and carbonate) cycle at Gale crater (Franz et al., Reference Franz, Mahaffy, Webster, Flesch, Raaen, Freissinet, Atreya, House, McAdam, Knudson, Archer, Stern, Steele, Sutter, Eigenbrode, Glavin, Lewis, Malespin, Millan, Ming, Navarro-González and Summons2020; Nature, permission).

Other mineral associations with biosignatures: While not associated with the ALH84001 meteorite, other minerals that are present on Mars, including silica, phyllosilicates and evaporitic phases such as sulphates, could also preserve biosignatures. In addition, the preservation of MISS in clastic sediments should be noted, for example, in the Palaeo-Mid Archaean formations of the Barberton Greenstone Belt in South Africa and the Pilbara Greenstone Belt in Australia (Noffke, Reference Noffke2010; Noffke et al., Reference Noffke, Christian, Wacey and Hazen2013).

Silica

(1) Siliceous hydrothermal environments, both subaqueous and subaerial, are prime sites for microbial development because of the significant supply of nutrients (Walter and Des Marais, Reference Walter and Des Marais1993; Cady and Farmer, Reference Cady and Farmer1996). With their high concentrations of nutrients (either organic, such as small molecules, gases such as CH₄, H₂), essential transition elements (Fe, Ni, V, Co, As), and variable gradients in pH, Eh and temperature, they provide a habitat for a wide variety of microbial life (Baross, Reference Baross1998). On present-day Earth, siliceous hydrothermal environments are essentially, but not only, associated with deep sea black smokers. Upon initial formation, these >300 °C environments are sterile but later become colonized by hyperthermophilic archaea transported by aqueous currents to the edifices (Wirth et al., Reference Wirth, Luckner and Wanner2018).

We will here consider hydrothermal environments on the early Earth because of their particular relevance for early Mars, the environments of the two planets being similar (Westall et al., Reference Westall, Foucher, Bost, Bertrand, Loizeau, Vago, Kminek, Gaboyer, Campbell, Bréhéret, Gautret and Cockell2015b). Marine hydrothermal environments on the early Earth occurred at all water depths including in the shallow water basins on the submerged oceanic plateaux that characterized the early protocontinents. Indeed, they also occur in the littoral and adjacent subaerial environments (Westall et al., Reference Westall, Campbell, Bréhéret, Foucher, Gautret, Hubert, Sorieul, Grassineau and Guido2015a, Reference Westall, Foucher, Bost, Bertrand, Loizeau, Vago, Kminek, Gaboyer, Campbell, Bréhéret, Gautret and Cockell2015b; Djokic et al., Reference Djokic, Van Kranendonk, Campbell, Walter and Ward2017). Higher heat flow from the early Earth's mantle (Sleep, Reference Sleep2000; Zahnle et al., Reference Zahnle, Ardnt, Cockell, Halliday, Nisbet, Selsis and Sleep2007; Kamber, Reference Kamber2015; Labrosse, Reference Labrosse2015; Van Kranendonk et al., Reference Van Kranendonk, Smithies, Griffin, Huston, Hickman, Champion, Anhaeusser and Pirajno2015) fuelled abundant volcanic and hydrothermal activity. Rare earth element (REE) signatures including Eu and Y anomalies, Y/Ho ratio, as well as the physical evidence of hydrothermal veins and pervasive silicification of all lithologies in contact with seawater, attest to the pervasive influence of hydrothermal fluids in the global ocean (e.g. Van Kranendonk, Reference Van Kranendonk2006; Hofmann and Bolhar, Reference Hofmann and Bolhar2007; Hofmann and Harris, Reference Hofmann and Harris2008; Westall et al., Reference Westall, Foucher, Bost, Bertrand, Loizeau, Vago, Kminek, Gaboyer, Campbell, Bréhéret, Gautret and Cockell2015b, Reference Westall, Hickman-Lewis, Hinman, Gautret, Campbell, Bréhéret, Foucher, Hubert, Sorieul, Dass, Kee, Georgelin and Brack2018), as well as in restricted shallow basins on top of the oceanic plateaux where influences from non-marine waters have been additionally detected (Hickman-Lewis et al., Reference Hickman-Lewis, Gourcerol, Westall, Manzini and Cavalazzi2020b).

Most physical evidence for hydrothermal activity on the early Earth points to subaqueous systems. Due to pervasive silicification (>96% SiO₂) of Palaeoarchaean sediments and the immediately underlying volcanics owing to oversaturation of silica in the early oceans, any physical expression of vents is difficult to detect, although some hydrothermal veins are readily identifiable by virtue of their cross-cutting nature (Hofmann and Bolhar, Reference Hofmann and Bolhar2007; Westall et al., Reference Westall, Campbell, Bréhéret, Foucher, Gautret, Hubert, Sorieul, Grassineau and Guido2015a). Veins can also form bedding-parallel intrusions into partially lithified sediment (Westall et al., Reference Westall, Campbell, Bréhéret, Foucher, Gautret, Hubert, Sorieul, Grassineau and Guido2015a). The 3.33 Ga Josefsdal Chert from the Barberton Greenstone Belt in South Africa comprises both volcanic sands and chemically precipitated sedimentary silica gel, now chert. Adjacent to hydrothermal vents, the volcanic sands are heavily encrusted by carbonaceous matter (CM), while silica gel mixed with very fine volcanic dust is characterized by stellate clots of CM identified as probable chemotrophic biomass (Westall et al., Reference Westall, Campbell, Bréhéret, Foucher, Gautret, Hubert, Sorieul, Grassineau and Guido2015a, Reference Westall, Foucher, Bost, Bertrand, Loizeau, Vago, Kminek, Gaboyer, Campbell, Bréhéret, Gautret and Cockell2015b; Hickman-Lewis et al., Reference Hickman-Lewis, Cavalazzi, Sorieul, Gautret, Foucher, Whitehouse, Jeon, Georgelin, Cockell and Westall2020a). The 3D, irregular, stellate formations of CM around the volcanic clasts (up to 30 μm thickness) and in irregular clots within the silica gel (up to 500 μm diameter) are categorically incompatible with abiotic CM aggregation, deposition or diffusion. In addition, the CM has enhanced concentrations of transition metals (Fe, V, Ni, As and Co), and a δ¹³C signature dominantly between −21.0 and −11.5‰ and as light as −41.3‰. These elemental and isotopic signatures, together with the morphological distribution of the CM and its petrographic context, suggest that this kerogen represents the remnants of lithotrophic or organotrophic consortia, possibly cycling methane or nitrogen (Hickman-Lewis et al., Reference Hickman-Lewis, Cavalazzi, Sorieul, Gautret, Foucher, Whitehouse, Jeon, Georgelin, Cockell and Westall2020a). When observed in field exposures, however, the heavy silicification makes direct detection of the clotted colonies in these sediments difficult, although sometimes a faint mottled texture reveals the presence of the carbonaceous clots.

It is rare for individual cells to be preserved morphologically in these ancient sediments, rapid silicification prior to heterotrophic degradation being a prerequisite (e.g. Fig. 3b). The rarely preserved examples show that individual cells are generally too small (<1 μm) to be analysed individually by in situ methods on Mars, although, as we have seen above, it may be possible to identify the carbonaceous remains of colonies of several 100 s μm size.

Not all Palaeoarchaean hydrothermal environments are subaqueous. Recently, subaerial sinter springs, similar to those on the modern Earth, have been described from the 3.48 Ga Dresser Formation, Pilbara, Australia. Djokic et al. (Reference Djokic, Van Kranendonk, Campbell, Walter and Ward2017, Reference Djokic, Van Kranendonk, Campbell, Havig, Walter and Guido2021) used textures and REE and yttrium geochemistry to demonstrate similarities between the Dresser geyserites and Phanerozoic hot spring sinters, noting the temporal association of a diverse suite of textural biosignatures that indicates a thriving microbial community. The biosignatures are primarily physical in nature, including stromatolites and microbial palisade fabric preserved in inferred mineralized exopolymeric substance. It is suggested that such geyserites and their textural features could be an explanation for the silica deposits identified around Home Plate in Gusev Crater (Ruff and Farmer, Reference Ruff and Farmer2016; Djokic et al., Reference Djokic, Van Kranendonk, Campbell, Havig, Walter and Guido2021).

Silica as a chemical sediment was ubiquitous on the early Earth both because of generally high silica concentrations in the sea water (Siever, Reference Siever1992) due to high rates of weathering of exposed landmasses and lack of removal by organisms using silica as a framework for their cells (e.g. diatoms that evolved later), and because of elevated hydrothermal influence. Another significant silica contribution comes from the devitrification of subaqueous volcanic sediments. This high concentration of silica in the early oceans was the prime reason for the silicification of early sediments and volcanic rocks exposed to seawater. It is also the reason for the rapid preservation of microbial biosignatures, even in non-hydrothermal, oligotrophic environments, as described by Westall et al. (Reference Westall, Cavalazzi, Lemelle, Marrocchi, Rouzaud, Simionovici, Salomé, Mostefaoui, Andreazza, Foucher, Toporski, Jauss, Thiel, Southam, MacLean, Wirick, Hofmann, Meibom, Robert and Défarge2011, Reference Westall, Campbell, Bréhéret, Foucher, Gautret, Hubert, Sorieul, Grassineau and Guido2015a).

Silica can also be concentrated in evaporitic settings, contributing to the entombment of microorganisms inhabiting the environment. Examples include the ~800 Ma Draken Formation in Svalbard where enhanced silica concentrations in an evaporitic environment resulted in the silicification of cyanobacterial mats (Foucher and Westall, Reference Foucher and Westall2013). While we do not expect to find cyanobacterial ecosystems on Mars, this example demonstrates the high fidelity of preservation by evaporitic silica and, in addition, documents a different type of biosignature, metastable minerals. In this example, metastable opal occurs within the organically preserved cell envelopes of the cyanobacteria while the enclosing silica cement is recrystallized to quartz, the organic phase enhancing the stability of the metastable mineral. It is further noteworthy that a beautifully preserved sequence of delicate microbial biofilms in the 3.33 Ga Josefsdal Chert formed in an evaporitic environment as attested to by the pseudomorph evaporite minerals embedded in their surfaces (Westall et al., Reference Westall, Cavalazzi, Lemelle, Marrocchi, Rouzaud, Simionovici, Salomé, Mostefaoui, Andreazza, Foucher, Toporski, Jauss, Thiel, Southam, MacLean, Wirick, Hofmann, Meibom, Robert and Défarge2011). NanoSIMS scans across the thicknesses of the biofilms document that they had been thoroughly silicified.

Continuing with the theme of weathering profiles on Mars evoked above, Rutledge et al. (Reference Rutledge, Horgan, Havig, Rampe, Scudder and Hamilton2018) documented high rates of glacial alteration of basaltic volcanic materials and the subsequent precipitation of amorphous (opaline) silica on rock surfaces in subglacial conditions on Iceland, analogous to those on early Mars; however, no biosignatures occur in these phases. Interestingly, a significant amount of poorly crystalline silica phases is mixed in with the detrital products of glacial weathering of the volcanic rock. X-ray amorphous silica is an important constituent of the sediments in Gale Crater where it can constitute up to 90% of the rock (Rapin et al., Reference Rapin, Chauviré, Gabriel, McAdam, Ehlmann, Hardgrove, Meslin, Rondeau, Dehouck, Franz, Mangold, Chipera, Wiens, Frydenvang and Schröder2018).

(2) Silica on Mars: Hydrated silica deposits have been detected from orbit in many locations at the surface of Mars. Sun and Milliken (Reference Sun and Milliken2018) determined that the mineral phases detected fall into two categories: amorphous and/or dehydrated silica-bearing bedrock deposits, and more crystalline and/or hydrated silica-bearing aeolian deposits. The latter provide evidence of impact-related, hydrothermally produced opaline silica and the former altered volcanic phases or dehydrated silica (Pineau et al., Reference Pineau, Le Deit, Chauviré, Carter, Rondeau and Mangold2020).

The most significant deposit of silica on Mars found to date is that around Home Plate, where amorphous SiO₂.nH₂O occurs in what may be an ancient volcanic hydrothermal setting in Gusev crater (Fig. 6(a) and (b); Squyres et al., Reference Squyres, Arvidson, Ruff, Gellert, Morris, Ming, Crumpler, Farmer, Marais, Yen, McLennan, Calvin, Bell, Clark, Wang, McCoy, Schmidt and de Souza2008; Ruff et al., Reference Ruff, Farmer, Calvin, Herkenhoff, Johnson, Morris, Rice, Arvidson, Bell, Christensen and Squyres2011). This deposit has been attributed to either fumarole-related, acid-sulphate leaching or precipitation from hot spring fluids with the latter being a privileged hypothesis based on analogue textural observations (Ruff and Farmer, Reference Ruff and Farmer2016) from hot springs at El Tatio in Chile. These authors suggest that the nodular and digitate silica structures at El Tatio, produced by a combination of biotic and abiotic processes, are very similar to those observed at Home Plate. Djokic et al. (Reference Djokic, Van Kranendonk, Campbell, Havig, Walter and Guido2021) also suggest similarities between textural biosignatures in Palaeoarchaean geyserites and those of Home Plate.

Fig. 6. (a) High-resolution image of Home Plate from orbit (Tao et al., Reference Tao, Conway, Muller, Putri, Thomas and Cremonese2021). (b) Comparison of the Home Plate silica deposits in Gusev Crater, Mars (left), with the El Tatio hot spring deposits in the Atacama (right); field views above, details of the silica spicules below (Ruff and Farmer, Reference Ruff and Farmer2016).

Hydrated (opaline) silica deposits detected in Jezero crater are of interest because they are a good mineral phase for biosignature preservation (Tarnas et al., Reference Tarnas, Mustard, Lin, Goudge, Amador, Bramble, Kremer, Zhang, Itoh and Parente2019). Associated with specific rock units, such as the opal-magnesite-smectite series detected in the olivine-rich unit and the opal-Al-phyllosilicate phase series co-located with the basement unit, the formation processes of the hydrated silica deposits are not yet understood. Possible candidates are: primary volcanism, diagenesis, authigenic formation in a lacustrine environment, detrital transport of material formed authigenically in the Jezero watershed, or transport to Jezero crater via aeolian processes.

Hydrated silica has been detected from orbit at the edges of deltaic fan deposits formed in relationship with a standing body of water in Oxia Planum, the chosen landing site for the ExoMars 2022 mission (Quantin-Nataf et al., Reference Quantin-Nataf, Carter, Mandon, Thollot, Balme, Volat, Pan, Loizeau, Millot, Breton, Dehouck, Fawdon, Gupta, Davis, Grindrod, Pacifici, Bultel, Allemand, Ody, Lozach and Broyer2021). Here, the hydrated silica deposits overlie clay-rich facies and indicate a changing hydrological regime possibly related to marine regression, or at least the drying of a water-filled basin, concurrent with the global hydrological trajectory of Mars through the Noachian and Hesperian periods.

Phyllosilicates

Direct morphological evidence of life will be difficult to detect on Mars because of (1) the very small size of the individual microorganisms, (2) the difficulty of distinguishing eventual microbial ‘clotted’ textures from abiotic ones, and (3) the possibility that distinctive macroscopic features, such as complex stromatolites, may not occur on Mars. Phyllosilicate minerals, however, have a propensity to accumulate and preserve organic matter, which chelates onto and in between the silicate sheets. As such, they are favoured mineral phases for the conservation of potential organic biosignatures (Bishop et al., Reference Bishop, Loizeau, McKeown, Saper, Dyar, Des Marais, Parente and Murchie2013; Vago et al., Reference Vago, Westall, Coates, Jaumann, Korablev, Ciarletti, Mitrofanov, Josset, De Sanctis, Bibring, Rull, Goesmann, Steininger, Goetz, Brinckerhoff, Szopa, Raulin, Westall, Edwards, Whyte, Fairén, Bibring, Bridges, Hauber, Ori, Werner, Loizeau, Kuzmin, Williams, Flahaut, Forget, Vago, Rodionov, Korablev, Svedhem, Sefton-Nash, Kminek, Lorenzoni, Joudrier, Mikhailov, Zashchirinskiy, Alexashkin, Calantropio, Merlo, Poulakis, Witasse, Bayle, Bayón, Meierhenrich, Carter, García-Ruiz, Baglioni, Haldemann, Ball, Debus, Lindner, Haessig, Monteiro, Trautner, Voland, Rebeyre, Goulty, Didot, Durrant, Zekri, Koschny, Toni, Visentin, Zwick, van Winnendael, Azkarate and Carreau2017), although environmental parameters on Mars, such as UV radiation and acid leaching, can negatively influence the long-term preservation of organic molecules, even associated with phyllosilicates (Gil-Lozano et al., Reference Gil-Lozano, Fairén, Muñoz-Iglesias, Fernández-Sampedro, Prieto-Ballesteros, Gago-Duport, Losa-Adams, Carrizo, Bishop, Fornaro and Mateo-Martí2020).

The hypothesis is that phyllosilicates on Mars may have chelated the organic remnants of microbial life. These minerals can also physically fossilize microorganisms and their EPS. Wacey et al. (Reference Wacey, Saunders, Roberts, Menon, Green, Kong, Culwick, Strother and Brasier2014) noted the role of authigenic clay precipitation in organism preservation based on experimental investigations and studies of phenomena in the natural environment, ranging from marine settings, lakes, rivers and hydrothermal systems. A variety of clay mineral types, including Fe-rich phyllosilicates (e.g. nontronite), as well as Al clays (kaolinite and halloysite), and Mg or K-rich clays, are implicated in this process (Fig. 3(d)). The composition of the authigenic minerals that precipitate under the influence of microbial mediation depends on factors, such as pH, Eh, sulphate concentration, ionic availability and the nature of the biological substrate, which will affect its affinity for specific ions.

Authigenic precipitation or chelation of phyllosilicates may occur on the surfaces of individual organisms in multispecies communities. Under specific physico-chemical conditions, this leads to the replacement of whole microbial mats by phyllosilicates. Phyllosilicates chelating to the surfaces of microorganisms form a ‘halo’ around them. Such phenomena have been observed in Oligocene (~30 Ma) deep sea sediments (Monty et al., Reference Monty, Westall and van der Gaast1991; Westall and Rincé, Reference Westall and Rincé1994), as well as in artificial fossilization of microbes in their deep sea sedimentary matrices (Fig. 3(c); Westall et al., Reference Westall, Boni and Guerzoni1995). In all cases, there is an intimate intergrowth of phyllosilicates with microbial polymer (EPS) such that fibril-like strands of polymer stretch between packets of phyllosilicates (Westall et al., Reference Westall, Foucher, Bost, Bertrand, Loizeau, Vago, Kminek, Gaboyer, Campbell, Bréhéret, Gautret and Cockell2015b).

The importance of phyllosilicates in the preservation of soft-bodied organisms was highlighted in ~500 My Burgess Shale-type deposits hosting soft-bodied fauna, where kaolinite played an important role in the preservation process (Gaines et al., Reference Gaines, Briggs and Yuanlong2008; LaFlamme et al., Reference Laflamme, Schiffbauer, Narbonne and Briggs2011). Experimental studies showed how this process worked. Working with cyanobacteria, well known for their formation of significant mats that covered the Ediacaran seafloors, thus entombing the soft-bodied macrobiota, Newman et al. (Reference Newman, Mariotti, Pruss and Bosak2016) exposed the microorganisms to elevated concentrations of clay minerals and silica, showing that clays coated the sheaths of the microorganisms through two mechanisms: trapping and indirect precipitation. Extending the importance of phyllosilicate precipitation to the cell walls of microorganisms, Wacey et al. (Reference Wacey, Saunders, Roberts, Menon, Green, Kong, Culwick, Strother and Brasier2014) studied 1 Ga lake sediments of the Torridon Group, Scotland, and described a microbially-mediated Fe-rich phyllosilicate phase that occurs in direct contact with cellular material; the Fe-rich phyllosilicates replace the most labile biological material, while a K-rich clay occurs within and exterior to cell envelopes, forming where the supply of Fe was exhausted (Fig. 3(d)).

Phyllosilicates on Mars: Orbital spectral measurements of the surface of Mars have identified large areas covered by diverse phyllosilicate phases. Their distribution and associations with other mineral phases suggest major compositional changes through time related to changing global environmental conditions on Mars (e.g. Poulet et al., Reference Poulet, Bibring, Mustard, Gendrin, Mangold, Langevin, Arvidson, Gondet, Gomez, Berthé, Bibring, Langevin, Erard, Forni, Gendrin, Gondet, Manaud, Poulet, Poulleau, Soufflot, Combes, Drossart, Encrenaz, Fouchet, Melchiorri, Bellucci, Altieri, Formisano, Fonti, Capaccioni, Cerroni, Coradini, Korablev, Kottsov, Ignatiev, Titov, Zasova, Mangold, Pinet, Schmitt, Sotin, Hauber, Hoffmann, Jaumann, Keller, Arvidson, Mustard and Forget2005; Bishop et al., Reference Bishop, Fairén, Michalski, Gago-Duport, Baker, Velbel, Gross and Rampe2018). There is much debate as to the formation mechanisms and environmental constraints for the clays observed at Mars’ surface. Their relative abundance in the Noachian suggests that, in its early history, Mars had a long-lived warmer and wetter climate, although this scenario is at odds with climate models, which suggest that Noachian Mars was cold. Nevertheless, geomorphological features unambiguously indicate water activity at the surface of the planet. Noting that the time necessary for clay minerals to form in cold environments is extremely long, and taking into account climate models, geomorphological signatures and mineral phases, Bishop et al. (Reference Bishop, Fairén, Michalski, Gago-Duport, Baker, Velbel, Gross and Rampe2018) hypothesized phyllosilicate formation during sporadic, short-term warm and wet periods on a generally cold early Mars. They concluded that associations of Mg-rich clay-bearing rocks with mixed Fe/Mg smectite, chlorite, talc, serpentine and zeolite likely formed in subsurface hydrothermal environments. On the other hand, other assemblages exhibiting vertical zonation of Al/Fe³⁺-rich and Fe/Mg smectites, as well as sulphates are interpreted to have formed in different physico-chemical environments with different rock/water ratios on the surface of Mars. Another possibility is that the phyllosilicates could have formed preferentially in the water region in contact with a ‘hot’ ground – that is, heated from the interior, but not necessarily in the subsurface. In this scenario, most of Mars would have been cold (consistent with the then reduced insolation and with climate models), but with topical warm environments, where water flow and alteration could proceed mediated by internal heat. So, for example, some of the ancient hydrous features we observe today could have flowed under a top-frozen layer of water.

Clays at Gale crater: Gale crater is a ~150 km diameter impact crater of Mars located at the limit of the cratered highlands of the south and the low plains of the north. Its age is about 3.6–3.8 Ga (Noachian-Hesperian boundary) according to the crater counts (Thomson et al., Reference Thomson, Bridges, Milliken, Baldridge, Hook, Crowley, Marion, de Souza Filho, Brown and Weitz2011). Orbital observations by the visible-infrared spectrometer, Compact Reconnaissance Imaging Spectrometer for Mars (CRISM) and the spectro-imager, Thermal Emission Imaging System (THEMIS) characterized the mineral phases in the crater, while the Mars Science Laboratory mission's rover Curiosity has been assessing past habitability in the region. Mount Sharp (formally named Aeolis Mons), the large central mound inside the crater, has relatively flat strata that may have preserved evidence of the evolution of the Mars environment (Grotzinger et al., Reference Grotzinger, Crisp, Vasavada, Anderson, Baker, Barry, Blake, Conrad, Edgett, Ferdowski, Gellert, Gilbert, Golombek, Gómez-Elvira, Hassler, Jandura, Litvak, Mahaffy, Maki, Meyer, Malin, Mitrofanov, Simmonds, Vaniman, Welch and Wiens2012). The older, lower part of the mound contains clays minerals mixed with hydrated sulphates, indicating aqueous activity, while the younger layers higher on the mound are covered by a dust mantle (Milliken et al., Reference Milliken, Grotzinger and Thomson2010; Thomson et al., Reference Thomson, Bridges, Milliken, Baldridge, Hook, Crowley, Marion, de Souza Filho, Brown and Weitz2011; Wray, Reference Wray2013).

Fluvial valley walls and crater rims and floors contain olivine-bearing bedrock associated with Fe/Mg phyllosilicates, kaolin family minerals, hydrated silica and other hydrated/hydroxylated phases (Wray, Reference Wray2013; Carter et al., Reference Carter, Viviano-Beck, Loizeau, Bishop and Le Deit2015; Ehlmann and Buz, Reference Ehlmann and Buz2015). CRISM spectra of the walls and rims show absorption bands that can be associated to Fe/Mg phyllosilicates, such as nontronite and saponite, while the Mount Sharp spectra exhibit different spectral properties characteristic of Al phyllosilicates, including montmorillonite and kaolinite (Buz et al., Reference Buz, Ehlmann, Pan and Grotzinger2017). The detection of different types of phyllosilicates thus suggests protoliths of a different nature or the formation of clays by fluids of different composition. There are several suggested scenarios to explain the origin of the clays on the crater floor: either the clays were transported to the crater floor from the already partially altered crater rim; or they were formed in situ by alteration of the mafic bedrock by water and subsequently altered as a result of burial diagenesis (Buz et al., Reference Buz, Ehlmann, Pan and Grotzinger2017).

Clay minerals at Jezero Crater: The 3.7 Ga old Jezero Crater at the edge of Isidis Planitia hosts a well-formed delta and deposits indicating the presence of lakes in the past. At the landing site of the Mars 2020 mission and the Perseverance rover, there is a diversity of phyllosilicate-bearing units that may have high biosignature preservation potential, including Al-clays and potential Fe-Mg-bearing smectites (Goudge et al., Reference Goudge, Mustard, Head, Fassett and Wiseman2015; Brown et al., Reference Brown, Viviano and Goudge2020; Horgan et al., Reference Horgan, Anderson, Dromart, Amador and Rice2020). These units are predominantly associated with the western delta, although zones of phyllosilicate-rich mineralogy have also been identified dispersed throughout the crater (Horgan et al., Reference Horgan, Anderson, Dromart, Amador and Rice2020), including the region close to the rover landing site. Additionally, localized zones of phyllosilicate richness have been noted within the marginal olivine carbonate unit (Goudge et al., Reference Goudge, Mustard, Head, Fassett and Wiseman2015; Horgan et al., Reference Horgan, Anderson, Dromart, Amador and Rice2020). Systematic variations in CRISM spectral parameters have been used to infer variability in Fe/Mg-phyllosilicates and Mg-carbonates between the different (stratigraphic) units of Jezero crater; however, these interpretations await validation by surface observations and analyses. The regional-scale origin of phyllosilicate-rich phases and their relationships with the surrounding crater floor and margin units have been addressed in detail by Brown et al. (Reference Brown, Viviano and Goudge2020); these scenarios imply a complex geological history at Jezero crater with aqueous periods that may have been conducive to habitability throughout the Noachian and earliest Hesperian. Of particular interest for habitability and palaeoenvironment is the unresolved origin of Fe/Mg-phyllosilicates, which may have formed during near-surface weathering and diagenesis, through post-impact hydrothermal activity, or both (Ehlmann et al., Reference Ehlmann, Bell, Brown, Horgan, Hurowitz, Kelemen, Mangold, Mayhew, Quantin, Rapin, Razzell Hollis, Scheller, Shuster, Stack, Sun, Tarnas and Treiman2021).

Clay minerals at Oxia Planum: Oxia Planum is a ~4 Ga depression located near the equator of the planet, on the eastern border of Chryse Planitia. It is the landing site chosen for the ESA (European Space Agency)-Roscosmos ExoMars 2022 mission. The Rosalind Franklin rover will touch down on 10 June 2023 to begin its search for traces of past and present life on Mars and to study the aqueous environment (Vago et al., Reference Vago, Westall, Coates, Jaumann, Korablev, Ciarletti, Mitrofanov, Josset, De Sanctis, Bibring, Rull, Goesmann, Steininger, Goetz, Brinckerhoff, Szopa, Raulin, Westall, Edwards, Whyte, Fairén, Bibring, Bridges, Hauber, Ori, Werner, Loizeau, Kuzmin, Williams, Flahaut, Forget, Vago, Rodionov, Korablev, Svedhem, Sefton-Nash, Kminek, Lorenzoni, Joudrier, Mikhailov, Zashchirinskiy, Alexashkin, Calantropio, Merlo, Poulakis, Witasse, Bayle, Bayón, Meierhenrich, Carter, García-Ruiz, Baglioni, Haldemann, Ball, Debus, Lindner, Haessig, Monteiro, Trautner, Voland, Rebeyre, Goulty, Didot, Durrant, Zekri, Koschny, Toni, Visentin, Zwick, van Winnendael, Azkarate and Carreau2017). Oxia Planum is particularly flat and contains clay-rich lithofacies that suggest past water activity in the region. The clay deposits show absorption bands centred at 1.9 and 2.3 μm that are characteristic of Fe/Mg clays, probably a vermiculite-smectite type of clay (Carter et al., Reference Carter, Quantin, Thollot, Loizeau, Ody and Lozach2016). In some places, an additional spectral absorption at 2.5 μm likely suggests the presence of a carbonate or other type of clay mineral. If carbonate phases are present, the site may have been preserved from any acidic environment, which enhances its potential for preserving traces of life (Mandon et al., Reference Mandon, Parkes Bowen, Quantin-Nataf, Bridges, Carter, Pan, Beck, Dehouck, Volat, Thomas, Cremonese, Tornabene and Thollot2021).

The layered clay-bearing unit has a total thickness of 100 m, with each layer varying from 0.7 to 3 m in thickness. According to HiRISE images, the clay-rich facies corresponds to a fractured material of different tonalities that is widely exposed and can be divided into two sub-units: the first one has a reddish tone with smaller fractures and the second one overlaps the first one and has a bluish tone with wider fractures (Quantin-Nataf et al., Reference Quantin-Nataf, Carter, Mandon, Thollot, Balme, Volat, Pan, Loizeau, Millot, Breton, Dehouck, Fawdon, Gupta, Davis, Grindrod, Pacifici, Bultel, Allemand, Ody, Lozach and Broyer2021). The colour difference is explained by mineralogical composition, rather than variable surficial dust or sand cover (Mandon et al., Reference Mandon, Parkes Bowen, Quantin-Nataf, Bridges, Carter, Pan, Beck, Dehouck, Volat, Thomas, Cremonese, Tornabene and Thollot2021). The clay-rich deposits cover terrains of mid- and late-Noachian age, draping the paleotopography, therefore, the unit is mid-Noachian or younger. These strata are systematically overlain by a thin, mid-toned, mantling unit that appears to be indurated and layered with a thickness of ~5 m (Quantin-Nataf et al., Reference Quantin-Nataf, Carter, Mandon, Thollot, Balme, Volat, Pan, Loizeau, Millot, Breton, Dehouck, Fawdon, Gupta, Davis, Grindrod, Pacifici, Bultel, Allemand, Ody, Lozach and Broyer2021). The clays may have a marine or lacustrine sedimentary origin. Other units present in the region include deltaic and fluvial deposits, remnant rounded buttes and a dark resistant unit. The latter is recognizable by its rough, dark and massive appearance and it notably overlies the other units. Its thickness is ~20 m, it appears to be composed of mafic minerals, and is probably of volcanic origin, possibly Amazonian in age (Carter et al., Reference Carter, Quantin, Thollot, Loizeau, Ody and Lozach2016; Quantin-Nataf et al., Reference Quantin-Nataf, Carter, Mandon, Thollot, Balme, Volat, Pan, Loizeau, Millot, Breton, Dehouck, Fawdon, Gupta, Davis, Grindrod, Pacifici, Bultel, Allemand, Ody, Lozach and Broyer2021). Thus, volcanic rocks covered the clays and other aqueous deposits, preserving potential biosignatures from the severe radiation and oxidation of the surface of the planet. The clay-bearing facies have been exposed by erosion relatively recently.

Evaporite minerals

Inorganic precipitation from supersaturated solutions forms evaporitic deposits in a variety of marine and terrestrial environments. Evaporite deposits – soluble salts precipitating from brines (Warren, Reference Warren2016) – and minerals have good biosignature preservation potential because they can embed and preserve sediments containing organic matter, as well as trapping microorganisms including endoliths and fluid-gas-solid inclusions. Such deposits can be preserved over long periods of geological time (e.g. Shkolyar and Farmer, Reference Shkolyar and Farmer2018; Benison, Reference Benison2019). Rapid growth of halite and gypsum from brines may easily entrap primary fluid inclusions that could serve as proxies for environmental conditions, including life. A number of taphonomic processes in evaporites and postdepositional changes, such as sediment phase solubility, porosity, permeability and postdepositional contamination, which can negatively affect the preservation of biosignatures (e.g. Barbieri, Reference Barbieri, de Vera and Seckbach2013). Nevertheless, there are several factors that can enhance biosignature preservation even though the window for preservation occurs under a narrow range of conditions that exist immediately after deposition (e.g. Shkolyar and Farmer, Reference Shkolyar and Farmer2018; Benison, Reference Benison2019). For instance, in hypersaline sabka environments, the dense-stratified brines can increase bottom-water anoxia and promote organic preservation (e.g. Westall and Cavalazzi, Reference Westall, Cavalazzi, Thiel and Reitner2011). On Earth, many kinds of halophiles have been isolated from a wide range of evaporitic environments, including sabka, salt marshes, undersea salt domes and subterranean halite deposits from evaporated ancient seas (e.g. Warren, Reference Warren2016; Benison, Reference Benison2019). Microorganisms have been isolated from salt crystals, evaporite deposits and associated fluid inclusions, in the rock record (Stan-Lotter et al., Reference Stan-Lotter, Pfaffenhuemer, Legat, Busse, Radax and Gruber2002; Vreeland et al., Reference Vreeland, Jones, Monson, Rosenzweig, Lowenstein, Timofeeff, Satterfield, Cho, Park and Wallace2007; Schubert et al., Reference Schubert, Lowenstein, Timofeeff and Parker2010; Fendrihan et al., Reference Fendrihan, Dornmayr-Pfaffenhuemer, Gerbl, Holzinger, Grösbacher, Briza, Erler, Gruber, Plätzer and Stan-Lotter2012; Carnevale et al., Reference Carnevale, Gennari, Lozar, Natalicchio, Pellegrino and Dela Pierre2019). For example, great palaeobiodiversity is described for the Miocenic Messinian evaporitic deposits, Italy (Carnevale et al., Reference Carnevale, Gennari, Lozar, Natalicchio, Pellegrino and Dela Pierre2019). Recently, the unique extreme environments at the Dallol geothermal area, Ethiopia (Cavalazzi et al., Reference Cavalazzi, Barbieri, Gómez, Capaccioni, Olsson-Francis, Pondrelli, Rossi, Hickman-Lewis, Agangi, Gasparotto, Glamoclija, Ori, Rodriguez and Hagos2019; Cavalazzi and Filippidou, Reference Cavalazzi, Filippidou, Branislav, Joseph and Roger2021) have provided the opportunity to study life at its biophysical limits in a hypersaline poly-extreme environment (Belilla et al., Reference Belilla, Moreira, Jardillier, Reboul, Benzerara, López-García, Bertolino, López-Archilla and López-García2019; Gómez et al., Reference Gómez, Cavalazzi, Rodríguez, Amils, Ori, Olsson-Francis, Escudero, Martínez and Miruts2019). Importantly, MISS are common in such environments where evaporate minerals may form on and within the microbial mats (Noffke, Reference Noffke2021).

Evaporites on Mars: Evaporite minerals and deposits, such as hydrated Mg or Fe sulphates, have been observed on Mars both from orbit and in situ (Squyres et al., Reference Squyres, Knoll, Arvidson, Clark, Grotzinger, Jolliff, McLennan, Tosca, Bell and Calvin2006; Rapin et al., Reference Rapin, Meslin, Maurice, Vaniman, Nachon, Mangold, Schröder, Gasnault, Forni and Wiens2016), suggesting formation under evaporitic conditions within the context of past shallow lake, mudflat/sandflat and eolian environments, as well as past shallow acid saline groundwaters (Grotzinger et al., Reference Grotzinger, Arvidson, Bell Iii, Calvin, Clark, Fike, Golombek, Greeley, Haldemann and Herkenhoff2005; Hynek et al., Reference Hynek, Osterloo and Kierein-Young2015; Lynch et al., Reference Lynch, Horgan, Munakata-Marr, Hanley, Schneider, Rey, Spear, Jackson and Ritter2015; Pondrelli et al., Reference Pondrelli, Rossi, Le Deit, Fueten, Schmidt, van Gasselt, Hauber and Pozzobon2017; Benison, Reference Benison2019). Sulphate- and other salt-bearing deposits occur in several places on Mars, including Meridiani Planum, Gusev Crater and Gale Crater (Grotzinger et al., Reference Grotzinger, Arvidson, Bell Iii, Calvin, Clark, Fike, Golombek, Greeley, Haldemann and Herkenhoff2005; Ehlmann et al., Reference Ehlmann, Anderson, Andrews-Hanna, Catling, Christensen, Cohen, Dressing, Edwards, Elkins-Tanton, Farley, Fassett, Fischer, Fraeman, Golombek, Hamilton, Hayes, Herd, Horgan, Hu, Jakosky, Johnson, Kasting, Kerber, Kinch, Kite, Knutson, Lunine, Mahaffy, Mangold, McCubbin, Mustard, Niles, Quantin-Nataf, Rice, Stack, Stevenson, Stewart, Toplis, Usui, Weiss, Werner, Wordsworth, Wray, Yingst, Yung and Zahnle2016; Pondrelli et al., Reference Pondrelli, Rossi, Le Deit, Fueten, Schmidt, van Gasselt, Hauber and Pozzobon2017). The thermochemical stability of such deposits under Martian conditions would enhance their potential for preserving possible halophilic microorganisms.

At Gale crater, for example, muddy to sandy sediments deposited in a lacustrine environment are characterized by a network of fractures filled in with light-toned deposits of sulphate evaporites, as well as nodules and raised ridges of similar materials. The fractures formed in the consolidated sediments owing to subsequent compression and extension related to fluid overpressure and cracking (De Toffoli et al., Reference De Toffoli, Mangold, Massironi, Zanella, Pozzobon, Le Mouélic, L'haridon and Cremonese2020). They were then infilled by briny solutions that deposited the evaporite mineral suites. Rapin et al. (Reference Rapin, Ehlmann, Dromart, Schieber, Thomas, Fischer, Fox, Stein, Nachon and Clark2019) documented bulk enrichments within the bedrock of significant amounts of calcium sulphate intercalated with a stratum enriched in hydrated magnesium sulphate resulting from early diagenetic, pre-compaction salt precipitation from brines concentrated by evaporation. Such environments would be habitable for halophilic-type microorganisms.

Experimental studies document the ability of halophiles to survive when exposed to surface Mars conditions (e.g. UV radiation, cold temperatures and desiccation; Oren, Reference Oren2014). For all these reasons, evaporite deposits are a key exploration target for the ongoing astrobiological exploration of Mars and for future Mars Sample Return programs (Hays et al., Reference Hays, Graham, Des Marais, Hausrath, Horgan, McCollom, Parenteau, Potter-McIntyre, Williams and Lynch2017).