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.
Copyright and License
© 2023 the Author(s). Published by PNAS. This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).
Acknowledgement
We would like to acknowledge Jake Bailey, Tom Bristow, Ted Present, Paul Myrow, Kelsey Moore, and Jen Glass for contributing to discussions about this work and the thoughtful comments from K. Konhauser and anonymous reviewers who improved this work. We would like to thank Chi Ma for assistance with SEM-EDS, Yunbin Guan for assistance with NanoSIMS, and Nathan Dalleska for help with ICP-MS analysis. We are additionally grateful to Alice Michel for discussions regarding sample preparation for FISH-SEM. We further acknowledge the crews of R/V Atlantis and R/V Western Flyer for assistance in sample collection and processing. Funding for this work was provided by the US Department of Energy's Office of Science (DE-SC0020373), the NSF BIO-OCE grant (#1634002), a Gordon and Betty Moore Foundation Marine Microbiology Investigator grant (#3780), the Simons Collaboration for the Origin of Life, and a grant from the Center for Environmental Microbial Interactions (to V.J.O.). K.S.M. was supported in part by a NSF Graduate Research Fellowship and a Schlanger Ocean Drilling Fellowship. V.J.O. is a CIFAR science fellow in the Earth 4D program. Portions of this work were developed from the doctoral dissertation of Kyle Metcalfe, Symbiotic Diversity and Mineral-Associated Microbial Ecology in Marine Microbiomes; Anne Dekas, Diazotrophy in the Deep: An Analysis of the Distribution, Magnitude, Geochemical Controls, and Biological Mediators of Deep-Sea Benthic Nitrogen Fixation; and Daniela Osorio Rodriguez, Microbial Transformations of Sulfur: Environmental and (Paleo) Ecological Implications.
Contributions
D.O.-R., K.S.M., J.P.G., and V.J.O. designed research; D.O.-R., K.S.M., S.E.M., H.Y., A.E.D., M.E., and T.D. performed research; D.O.-R., K.S.M., S.E.M., L.A., J.P.G., and V.J.O. analyzed data; and D.O.-R. and K.S.M. wrote the paper.
Data Availability
All data and custom scripts were collected and stored using Git version control. Code for raw data processing, analysis, and figure generation is available in the GitHub repository (https://github.com/daniosro/Si_biomineralization_ANME_SRB) (92). All other data are included in the manuscript and/or supporting information.
Conflict of Interest
The authors declare no competing interest.
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Additional details
- ISSN
- 1091-6490
- DOI
- 10.1073/pnas.2302156120
- PMCID
- PMC10743459
- United States Department of Energy
- DE-C0020373
- National Science Foundation
- OCE-1634002
- Gordon and Betty Moore Foundation
- 3780
- Simons Foundation
- California Institute of Technology
- Caltech Center for Environmental Microbial Interactions
- National Science Foundation
- NSF Graduate Research Fellowship
- Canadian Institute for Advanced Research
- Accepted
-
2023-11-06Accepted paper
- Available
-
2023-12-11Published online
- Available
-
2023-12-19Published in issue
- Caltech groups
- Division of Geological and Planetary Sciences, Caltech Center for Environmental Microbial Interactions (CEMI)
- Publication Status
- Published