Trace gases, microbes and life beyond Earth

By definition, trace gases individually make up ≤1% (or 10,000 parts per million, ppm) of planetary atmospheres. Despite of these low concentrations, the significance of Earth’s many trace gases extends far beyond what their abundances suggest. Carbon dioxide (CO₂, about 400 ppm) accounts for a large fraction of the gases that cause the ‘greenhouse effect’, known more accurately as ‘radiative forcing’, and represents a fundamental unit of the carbon cycle. Methane (CH₄, about 2 ppm) also contributes to radiative forcing and plays significant roles in atmospheric chemistry. CO (about 0.3 ppm) determines the oxidative state of the atmosphere and partially regulates the concentration of many organic volatiles, including CH₄.

Results from more than a century of research have not only revealed the phylogenetic, physiological and ecological diversity of trace gas-utilising bacteria, they have shown unequivocally that these bacteria have largely determined the composition of the atmosphere throughout most of Earth’s history. Indeed, they are responsible for the atmospheric chemical disequilibrium that famously led James Lovelock, a primary originator of the Gaia Hypothesis, to claim that the equilibrium state of an atmosphere indicates whether a planet likely does or does not harbour life. Relative to Earth, no other planet in the solar system supports an atmosphere far from equilibrium. So, following Lovelock’s logic, no other planet likely supports life, at least not at a scale large enough to impact the atmosphere.

Nonetheless, the search for evidence of past and extant life on Mars has intensified over time rather than diminishing, fuelled in part by discoveries that support the existence of ancient oceans and even contemporary liquid water. While future discoveries might yet document globally extensive life that could have affected Mars’ atmosphere early in its history, it is evident that extant life, if it exists, is neither globally distributed nor capable of generating a chemical disequilibrium in the atmosphere. Microbial life might exist in Mars’ subsurface but, if it does, its impact on the atmosphere appears to be limited to infrequent enigmatic puffs of CH₄ that have little overall atmospheric chemical consequence.

In spite of extremely challenging conditions, relics of ancient microbial life might yet persist at or near the regolith surface. If so, any extant populations or communities would likely occur at very low abundances in isolated patches. Though any such communities would be too small to noticeably affect Mars’ atmospheric composition, they might nonetheless depend on the atmosphere for sources of carbon and energy. CO₂, which accounts for 94.9% of Mars’ atmosphere, represents an obvious source of cell carbon for microbes that function as chemolithoautotrophs, but sources of suitable reductants are unclear.

Ferrous and metallic iron occur in various mineral phases found on Mars, but the extent to which they might be available as physiologically relevant reductants has not been adequately evaluated. A model study with Methanothermobacter wolfei revealed a potential role for metallic iron in methanogenesis, while a study with Acidithiobacillus ferrooxidans documented growth on ferrous iron-containing minerals in a Mars regolith simulant. However, the extent to which these reactions might occur on Mars, where in particular, and under what conditions remains largely speculative.

In contrast to the patchiness in the regolith of potential solid or aqueous substrates that could be locally depleted over time, Mars’ atmosphere represents a relatively well-mixed, constant and ubiquitous source of substrates that could be used by putative microbial populations colonising habitable regions of the surface or near surface. Since habitable zones appear quite limited, any populations that colonised them would be too small to impact atmospheric composition, but they could be sustained by trace gas consumption.

CO is an especially intriguing candidate gas, since it is well known as a source of energy, and in some cases cell carbon, for a wide range of terrestrial bacteria, including aerobes, facultative anaerobes and obligate anaerobes. The former two groups are distinguished from the latter in numerous ways, but most significantly by end-products (CO₂ versus CO₂, H₂ and acetate) and enzymatic mechanisms (molybdenum-dependent versus nickel-dependent CO dehydrogenases [CODHs]).

Ni-dependent CO oxidation almost certainly arose very early during the history of Earth’s microbiota, and could also have arisen at a similar time on Mars (4.2–3.8 billion years ago). Evolution of a molybdenum-dependent process that used nitric oxide (NO), nitrite or nitrate as electron acceptors instead of molecular oxygen might have occurred subsequently, although the window for extensive microbial evolution on Mars was considerably shorter than on Earth due to dramatic decreases in temperature and water availability, and increases in radiation exposure as the Noachian period ended (3.5 billion years ago). These changes resulted in conditions hostile to life at a global scale. Several lines of evidence show that terrestrial microbes have remarkable capacities for long-term survival under extreme conditions. But could CO oxidisers of any kind have survived at local scales, adapted to extreme conditions and persisted to the present?

Although terrestrial CO oxidisers are very diverse phylogenetically and operate across a wide range of ecological conditions (e.g. pH, temperature, salinity and nutrient availability), CO-oxidising bacterial halophiles and euryarchaeal extreme halophiles in particular, represent ideal models for understanding the potential for CO to contribute to long-term microbial survival, and for exploring adaptations to surface or near surface conditions on Mars that might be permissive for life. Since high salt concentrations are necessary for maintaining water in a liquid state at low temperatures and pressures, extreme halophiles have long been proposed as models for Mars and other extra-terrestrial systems. They have also attracted interest because they have been cultured from ancient, geologically isolated salt deposits – implying that they persist on scales of 10⁶ years or more.

More recent observations have revealed that the capacity for CO oxidation using molybdenum-dependent CODHs occurs in numerous euryarchaeal extreme halophiles. Isolates obtained from salt crusts, saline soils and brine pools oxidise CO at concentrations lower than those in Earth’s ambient atmosphere, which are far below levels that occur in Mars’ atmosphere. This implies that CO oxidisers in surface or shallow near-surface brines on Mars could be sustained by CO uptake, perhaps analogous to observations for young terrestrial volcanic deposits and Antarctic desert soils, which derive energy for survival, in part, from atmospheric CO.

Of course, it must be emphasised that the composition of Martian brines likely differs substantially from brines on Earth. The presence in the former of magnesium and sodium perchlorates in relatively high concentrations represents a key distinction. Although perchlorates can serve as electron acceptors for dissimilatory perchlorate-reducing bacteria, perchlorate concentrations in terrestrial ecosystems are typically micromolar or less.

In contrast, brines on Mars could contain molar perchlorate concentrations in solutions with water activities or chaotropicities that are impermissible for life. Nonetheless, where water activities and chaotropicity are permissive, communities of extreme halophiles might persist in the presence of perchlorate while carrying out very slow rates of metabolism, analogous to those in the terrestrial deep subsurface. In this context, it is promising that some CO-oxidising halophiles and extreme halophiles not only tolerate molar perchlorate levels, but also couple perchlorate reduction to anaerobic CO oxidation. Thus, extreme halophiles could plausibly have evolved on Mars with a capacity for both CO oxidation and perchlorate reduction to chlorite or chloride. Notably, photochemical reactions in Mars’ atmosphere could sustain uptake by producing CO from CO₂, resulting in a light-dependent ecosystem.

Mars has been the primary focus for studies of extra-terrestrial life for multiple, obvious reasons. However, it is not the only system where CO might support microbial life. The presence of CO has been reported for both the moons Europa and Enceladus and could contribute to microbial metabolism in their oceans as it does on Earth. More intriguing, however, is the possibility that CO could contribute to a microbial ecosystem in the atmosphere of Venus, which contains about 17 ppm CO, well above concentrations in Earth’s atmosphere.

Although surface temperatures on Venus are impermissible for life, habitable conditions (e.g. temperature, pressure and water availability) exist in the lower cloud layer, and have long spurred speculation about stable communities of airborne microbes. Any such communities would differ markedly from putative communities on Mars due to much warmer temperatures, greater water availability and the presence of sulfuric acid aerosols. These conditions might be incompatible with molybdenum-dependent CO oxidation as we currently know it but could support acidophilic nickel-dependent CO oxidisers. The latter group of obligate anaerobes includes thermophilic acetogens, sulphate reducers and CO disproportionators. Extremely acidophilic nickel-dependent CO oxidisers have not yet been documented, but extensive surveys for them have not yet been carried out. It remains to be seen whether there are physiological constraints on their evolution.

Thus, while Lovelock’s inferences about the relationship between atmospheric composition and life within the solar system or on exoplanets are likely true as a first approximation – Mars, Venus and other systems could still harbour microbial life that depends on trace gases. The ubiquity of CO, its relatively high concentrations in some atmospheres and the exceptional physiological and phylogenetic diversity of terrestrial CO oxidisers make it an excellent candidate for expanded research, both on Earth and as a part of planetary exploration.