The Martian surface is cold, dry, exposed to biologically harmful radiation and apparently barren today. Nevertheless, there is clear geological evidence for warmer, wetter intervals in the past that could have supported life at or near the surface. This evidence has motivated National Aeronautics and Space Administration and European Space Agency to prioritize the search for any remains or traces of organisms from early Mars in forthcoming missions. Informed by (1) stratigraphic, mineralogical and geochemical data collected by previous and current missions, (2) Earth's fossil record, and (3) experimental studies of organic decay and preservation, we here consider whether, how, and where fossils and isotopic biosignatures could have been preserved in the depositional environments and mineralizing media thought to have been present in habitable settings on early Mars. We conclude that Noachian‐Hesperian Fe‐bearing clay‐rich fluvio‐lacustrine siliciclastic deposits, especially where enriched in silica, currently represent the most promising and best understood astropaleontological targets. Siliceous sinters would also be an excellent target, but their presence on Mars awaits confirmation. More work is needed to improve our understanding of fossil preservation in the context of other environments specific to Mars, particularly within evaporative salts and pore/fracture‐filling subsurface minerals.
Oxygenic photosynthesis supplies organic carbon to the modern biosphere, but it is uncertain when this metabolism originated. Based on the inferred presence of manganese oxides in the sediments as old as 3 billion years, it has been proposed that photosynthetic reaction centers capable of splitting water arose by that time. However, this assumes that manganese oxides can only be produced in the presence of molecular oxygen 1 , reactive oxygen species 2,3 or by high-potential photosynthetic reaction centers 4,5 . Here we show that anoxygenic photosynthetic microbial communities biomineralize manganese oxides under strictly anaerobic conditions and in the absence of high-potential photosynthetic reaction centers. This light-dependent process can produce manganese oxide minerals and stimulate the redox cycling of carbon, sulfur, nitrogen and other elements in the photic zones of modern anoxic water bodies and sediments. Microbial oxidation of Mn(II) in the absence of molecular oxygen during the Archean Eon would have produced geochemical signals identical to those used to date the evolution of oxygenic photosynthesis before the Great Oxidation Event (GOE) 6,7 . Manganese (Mn) and more than 30 of its described oxides and hydroxides mediate the cycling of various trace metals and nutrients in the environment. The microbial ability to oxidize Mn(II) anaerobically is also hypothesized to have been a critical step in the evolution of oxygenic photosynthesis on the early Earth 4 . However, modern microbes are not known to anaerobically oxidize manganese. Here, we demonstrate this activity in active microbial cultures that grow in the presence of nanomolar oxygen concentrations relevant for the Archean Earth.Inoculum for the enrichment cultures of strictly anaerobic, photosynthetic biofilms came from the meromictic Fayetteville Green Lake (FGL), NY. The anaerobic photic zone of the lake contains 20 nM to 61 µM Mn(II) and 0-0.04 mM of H 2 S [8], and the most abundant phototroph there is the green sulfur bacterium Chlorobium sp. 9 . This microbe uses sulfide, hypothesized to be the oldest electron donor for photosynthesis 10 , as an electron donor. Photosynthetic biofilms of this organism and other strict anaerobes (Fig. 1a) were enriched in a minimal medium amended with 20-50 µM Na 2 S and 1 mM MnCl 2 and equilibrated with an anaerobic atmosphere of 80% N 2 and 20% CO 2 at pH 7. The concentration of O 2 in the medium was lower than 2 nM during the course of the experiment and the maximum total inflow of O 2 over two weeks was lower than 300 nmol (see Methods and Extended Data Fig. 1). These experimental concentrations match the upper estimates for the Archean Earth 11 . The anaerobic medium also lacked other potential oxidants for Mn(II) such as nitrite, nitrate and H 2 O 2 and these species were not produced in sterile controls (Extended Data Section 5). References 1 Tebo, B. M. et al. Biogenic manganese oxides: properties and mechanisms of formation.
The use of metals as biosignatures in the fossil stromatolite record requires understanding of the processes controlling the initial metal(loid) incorporation and diagenetic preservation in living microbialites. Here, we report the distribution of metals and the organic fraction within the lithifying microbialite of the hypersaline Big Pond Lake (Bahamas). Using synchrotron-based X-ray microfluorescence, confocal, and biphoton microscopies at different scales (cm-μm) in combination with traditional geochemical analyses, we show that the initial cation sorption at the surface of an active microbialite is governed by passive binding to the organic matrix, resulting in a homogeneous metal distribution. During early diagenesis, the metabolic activity in deeper microbialite layers slows down and the distribution of the metals becomes progressively heterogeneous, resulting from remobilization and concentration as metal(loid)-enriched sulfides, which are aligned with the lamination of the microbialite. In addition, we were able to identify globules containing significant Mn, Cu, Zn, and As enrichments potentially produced through microbial activity. The similarity of the metal(loid) distributions observed in the Big Pond microbialite to those observed in the Archean stromatolites of Tumbiana provides the foundation for a conceptual model of the evolution of the metal distribution through initial growth, early diagenesis, and fossilization of a microbialite, with a potential application to the fossil record.
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