Microbial iron reduction on Earth and Mars

Abstract

The search for life beyond Earth is the driving force behind several future missions to Mars. An essential task in the lead-up to these missions is a critical assessment of the habitability for, and feasibility of, life. However, little research has been conducted on this issue, and our understanding of the plausibility for life on Mars remains unconstrained. Owing to the anoxic and iron-rich nature of Mars, microbial iron reduction (MIR) represents a compelling candidate metabolism to operate in the Martian subsurface, past and present. The objectives of this thesis are to address the feasibility of MIR on Mars by i) better defining the habitability of MIR on Earth, and ii) assessing the range and availability of organic electron donors in the subsurface of Earth and Mars. Samples collected from Mars-relevant environments on Earth were used to initiate MIR enrichment cultures at 4°C, 15°C and 30°C. Results indicate MIR is widespread in riverbed and subglacial sediments but not sediments from desert or recent volcanic plains. The iron-reducing microorganisms in subglacial enrichments are at least psychrotolerant and in some cases psychrophilc. Culture-independent methods highlighted the changes in diversity between temperature conditions for subglacial sediments, and indicated that members of the prolific MIR Geobacteraceae family are common. The genera Geobacter and Desulfosporosinus are responsible for MIR in the majority of enrichments. Long-term anoxia and the availability of redox constituents are the major factors controlling MIR in these environments. A MIR enrichment culture was unable to use shales and kerogens as the sole source of electron donors for MIR, despite the presence of known electron donors. Furthermore, MIR was inhibited by the presence of certain kerogens. The causes of inhibition are unknown, and are likely to be a combination of chemical and physical factors. Experiments were conducted to assess the ability of three pure strains and a MIR enrichment to use non-proteinogenic amino acids common to carbonaceous meteorites as electron donors for MIR. Results demonstrate that γ-aminobutyric acid served as an electron donor for the enrichment culture, but no other amino acids supported MIR by this or other iron-reducing cultures. The D-form of chiral amino acids was found to exert a strong inhibitory effect, which decreased in line with concentration. Theoretical calculations using published meteoritic accretion rates onto the surface of Mars indicate that the build up inhibitory amino acids may place important constrains on habitability over geologic time scales. Contamination of a pure strain of Geobacter metallireducens with a strain of Clostridium revealed a syntrophic relationship between these microorganisms. Anaerobic heterotrophs are likely to play an important role in maintaining an available supply of electron donors for MIR and similar chemoorganic metabolisms operating in the subsurface. This research indicates that MIR remains a feasible metabolism to operate on Mars providing a readily available redox couple is present. However, given the observed inhibition in the presence of bulk carbonaceous material and certain amino acids found in meteorites, the use of extraterrestrial carbonaceous material in the Martian subsurface for microbial iron reduction is questionable, and should be the focus of future research