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

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 120; no. 51; p. e2302156120
• Main Authors: Osorio-Rodriguez, Daniela, Metcalfe, Kyle S, McGlynn, Shawn E, Yu, Hang, Dekas, Anne E, Ellisman, Mark, Deerinck, Tom, Aristilde, Ludmilla, Grotzinger, John P, Orphan, Victoria J
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 19.12.2023
• Subjects: amorphous silica; Anaerobic microorganisms; Anaerobiosis; ANME-SRB; Archaea; Archaea - genetics; Artificial seawater; authigenic carbonates; Bacteria; Biological Sciences; Carbonates; Chemical analysis; Chemical precipitation; Clay; Clay minerals; Consortia; Cyanobacteria; Electron microscopy; endolithic microorganisms; ENVIRONMENTAL SCIENCES; Fluorescence; Fluorescence in situ hybridization; Fossils; Geologic Sediments - microbiology; Geology; GEOSCIENCES; In Situ Hybridization, Fluorescence; Mass spectrometry; Mass spectroscopy; Methane; methane oxidation; methane seeps; microbial biomineralization; Microbial Consortia; microfossils; Microorganisms; Microscopy; Minerals; Oxidation; Oxidation-Reduction; Phylogeny; Physical Sciences; Precipitates; Preservation; Rocks; Scanning electron microscopy; Seawater; Secondary ion mass spectrometry; Sediments; Silica; silica cycle; Silicates; Silicon Dioxide; Spheroids; Sulfate reduction; Sulfate-reducing bacteria; Sulfates; Water analysis; X-ray spectroscopy; microfossils; methane seeps; amorphous silica; ANME-SRB; microbial biomineralization
• ISSN: 0027-8424; 1091-6490; 1091-6490
• DOI: 10.1073/pnas.2302156120

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 ., , 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 ., , 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 ., , 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.