Linking methane oxidation with perchlorate reduction: a microbial base for possible Martian life

Recent observations of methane (CH₄) and perchlorate (ClO₄^-) within the atmosphere and surface of Mars, respectively, provide impetus for establishing a metabolic linkage between these compounds whereby CH₄ acts as an electron donor and perchlorate acts as an electron acceptor. Direct linkage through anaerobic oxidation of methane (AOM) has not been observed. However, indirect syntrophic oxygenase-dependent oxidation of CH₄ with an aerobic methane oxidizer is feasible. The pathway for anaerobic dissimilatory perchlorate reduction includes 3 steps. The first 2 are sequential reductions of (1) perchlorate to chlorate and (2) chlorate to chlorite, mediated by perchlorate reductase. The third step is disproportionation of chlorite to chloride and molecular oxygen, mediated by chlorite dismutase. Utilization of thusly derived oxygen by hydrocarbon-degrading organisms in anoxic environments was first demonstrated by Coates et. al. (1998)¹, however the link to aerobic methane oxidation was not examined at that time. Here, we systematically explore the potential for several species of aerobic methanotrophs to couple with chlorite during dissimilatory perchlorate reduction. In one experiment, 0.5 kPa CH₄ was completely removed in one day from the headspace of combined cell suspensions of Dechloromonas agitata strain CKB and Methylococcus capsulatus in the presence of 5 mM chlorite. Oxidation of labeled ¹⁴CH₄ to ¹⁴CO₂ under similar conditions was later confirmed. Another experiment demonstrated complete removal of 0.2 kPa CH₄ over several days by Methylobacter albus strain BG8 with strain CKB in the presence of 5 mM chlorite. Finally, we observed complete removal of 0.2 kPa CH₄ in bottles containing natural soil (enriched in methanotrophs by CH₄ additions over several weeks) and strain CKB and in the presence of 10 mM chlorite. This soil, collected from a pristine lake shoreline, demonstrated endogenous methane, perchlorate, chlorate and chlorite uptake. Other soil and sediment environments are being tested for methane oxidation linked either directly or indirectly with perchlorate reduction. ¹ Coates, JD, Bruce, Haddock, JD, (1998) Anoxic bioremediation of hydrocarbons. Nature, 396, 730.