Extreme C-13-depletions and organic sulfur content argue for S-fueled anaerobic methane oxidation in 2.72 Ga old stromatolites

The extreme C-13-depletions recorded in Neoarchean organic matter (OM) have commonly been interpreted as markers of methanotrophy. This methane oxidation metabolism could have been performed using oxidants such as dioxygen, sulfate, nitrite/nitrate, and/or Fe3+- and Mn4+- minerals. Acetogenesis using acetyl-CoA metabolism may produce similar C-13-depletions. We investigated delta C-13 and S/C values of OM in 2.72 Ga old lacustrine stromatolites of the Tumbiana Formation (Australia) using Secondary Ion Mass Spectrometry (SIMS), coupled with X-ray spectroscopy. Type-A OM is embedded in quartz and/or chlorite. We show that mixtures of chlorite bias negatively the delta C-13(org) of associated OM measured by SIMS, likely through recombination of hydrogen from chlorite with carbon from OM during analysis. Type-A OM, associated with quartz or interleaved with chlorites (but remote enough to avoid H-recombination), displays delta C-13(org) between -56.1 and -50.6% VPDB (mean: 53.5%, SD +/- 1.8%). The intimate association of Type-A OM with Fe-rich chlorite and its main occurrence in pyritic layers coupled with C-13-depletions is most parsimoniously interpreted as anaerobic methanotrophy using Fe3+- minerals and/or oxidized S. Type-B OM comprises <2-mu m organic globules embedded in calcite. A mass balance correction using the delta C-13 values measured on Type-B globules mixed with calcite and those measured on pure calcite yielded corrected delta C-13*(org) values for the globules ranging between -65.2 and -52.5% (mean -58.8%, SD +/- 3.6%). In a context where Fe and S reduction could outcompete acetogenesis for a fraction of any available H-2, these extremely low delta C-13(org) values are difficult to explain with chemoautotrophic acetogenesis. Atomic S/C ratios in Type-B globules reach up to 0.042, i.e. up to tenfold the values (0.003-0.004) in Type A-OM. These organic S concentrations, combined with the extremely low delta C-13*(org) values, support anaerobic oxidation of methane coupled to sulfur oxidation. Finally, Type-C OM, interpreted as migrated pyrobitumen nodules, displays delta C-13(org) of -48 to -39.1%. The most extreme low-delta C-13(org) values of the Precambrian are thus best interpreted as the result of lacustrine methanotrophy fueled by oxidized S and/or Fe species, which likely derived from oxygenic and/or anoxygenic photosynthesis. Photosynthesis, followed by methanogenesis and methanotrophy may have been important in lakes at a time of supercontinent growth and eruption of large subaerial igneous provinces. In this context, anaerobic methanotrophy could have played a part in regulating atmospheric methane. (C) 2018 Elsevier Ltd. All rights reserved.