Microbially induced precipitation of silica by anaerobic methane-oxidizing consortia and implications for microbial fossil preservation

Abstract

Authigenic carbonate minerals can preserve biosignatures of microbial anaerobic oxidation of methane (AOM) in the rock record. It is not currently known whether the microorganisms that mediate sulfate-coupled AOM—often occurring as multicelled consortia of anaerobic methanotrophic archaea (ANME) and sulfate-reducing bacteria (SRB)—are preserved as microfossils. Electron microscopy of ANME-SRB consortia in methane seep sediments has shown that these microorganisms can be associated with silicate minerals such as clays [Chen et al ., Sci. Rep. 4 , 1–9 (2014)], but the biogenicity of these phases, their geochemical composition, and their potential preservation in the rock record is poorly constrained. Long-term laboratory AOM enrichment cultures in sediment-free artificial seawater [Yu et al ., Appl. Environ. Microbiol. 88 , e02109-21 (2022)] resulted in precipitation of amorphous silicate particles (~200 nm) within clusters of exopolymer-rich AOM consortia from media undersaturated with respect to silica, suggestive of a microbially mediated process. The use of techniques like correlative fluorescence in situ hybridization (FISH), scanning electron microscopy with energy dispersive X-ray spectroscopy (SEM-EDS), and nanoscale secondary ion mass spectrometry (nanoSIMS) on AOM consortia from methane seep authigenic carbonates and sediments further revealed that they are enveloped in a silica-rich phase similar to the mineral phase on ANME-SRB consortia in enrichment cultures. Like in cyanobacteria [Moore et al ., Geology 48 , 862–866 (2020)], the Si-rich phases on ANME-SRB consortia identified here may enhance their preservation as microfossils. The morphology of these silica-rich precipitates, consistent with amorphous-type clay-like spheroids formed within organic assemblages, provides an additional mineralogical signature that may assist in the search for structural remnants of microbial consortia in rocks which formed in methane-rich environments from Earth and other planetary bodies.

Molybdenum Isotope Fingerprinting of Microbial Sulfate Reduction in Seep Carbonate Rocks

“…Marine seeps-with their locally enhanced sulfate reduction and a high abundance of sulfate-reducing bacteria-are typified by (a) prominent pyrite production, (b) high abundance of authigenic Mo in the sediments, and (c) the occurrence of highly depleted δ 13 C signatures in both organic matter and authigenic carbonate rocks (e.g., Feng et al, 2021;Hu et al, 2014;Peckmann & Thiel, 2004). Methanotrophic archaea and associated sulfate-reducing bacteria assimilate highly 13 C-depleted bicarbonate and methane into their biomass (e.g., Bowles et al, 2020;Osorio-Rodriguez et al, 2023;Wegener et al, 2008), contributing to the highly 13 C-depleted TOC at seeps (e.g., Feng et al, 2021). Enhanced sulfate reduction at seeps can be generally inferred from more negative δ 13 C carb and δ 13 C TOC values, although the fact that methane-rich fluids at seeps worldwide carry distinctive and variable δ 13 C compositions (due to different origins, such as thermogenic and biogenic methane) complicates the use of δ 13 C carb and δ 13 C TOC as a proxy for the intensity of sulfate reduction.…”

“…For instance, for Site F of the South China Sea, a higher Δ 98 Mo carb-OM value along with higher S py and Mo py contents suggests enhanced sulfate reduction and corresponding sulfate-reducing bacterial activity. In seepage areas, any increase in the rate of sulfate reduction is accompanied by enhanced metabolic activity and/or an increase in the biomass of sulfate-reducing bacteria (Glass et al, 2014;Osorio-Rodriguez et al, 2023). Such enhanced microbial activity is likely to come along with a greater sequestration of light Mo isotopes from the surrounding pore water onto the microbially derived organic matter, hence resulting in enhanced Mo isotope fractionation and higher Δ 98 Mo carb-OM values (Figure 4).…”