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Mcr-dependent methanogenesis in Archaeoglobaceae enriched from a terrestrial hot spring

The ISME Journal volume 17, pages 1649–1659 (2023)Cite this article

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Abstract

The preeminent source of biological methane on Earth is methyl coenzyme M reductase (Mcr)-dependent archaeal methanogenesis. A growing body of evidence suggests a diversity of archaea possess Mcr, although experimental validation of hypothesized methane metabolisms has been missing. Here, we provide evidence of a functional Mcr-based methanogenesis pathway in a novel member of the family Archaeoglobaceae, designated Methanoglobus nevadensis, which we enriched from a terrestrial hot spring on the polysaccharide xyloglucan. Our incubation assays demonstrate methane production that is highly sensitive to the Mcr inhibitor bromoethanesulfonate, stimulated by xyloglucan and xyloglucan-derived sugars, concomitant with the consumption of molecular hydrogen, and causing a deuterium fractionation in methane characteristic of hydrogenotrophic and methylotrophic methanogens. Combined with the recovery and analysis of a high-quality M. nevadensis metagenome-assembled genome encoding a divergent Mcr and diverse potential electron and carbon transfer pathways, our observations suggest methanogenesis in M. nevadensis occurs via Mcr and is fueled by the consumption of cross-fed byproducts of xyloglucan fermentation mediated by other community members. Phylogenetic analysis shows close affiliation of the M. nevadensis Mcr with those from Korarchaeota, Nezhaarchaeota, Verstraetearchaeota, and other Archaeoglobales that are divergent from well-characterized Mcr. We propose these archaea likely also use functional Mcr complexes to generate methane on the basis of our experimental validation in M. nevadensis. Thus, divergent Mcr-encoding archaea may be underestimated sources of biological methane in terrestrial and marine hydrothermal environments.

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Fig. 1: Community composition and methane production data of the xyloglucan-degrading culture.
Fig. 2: Enrichment of M. nevadensis among multiple McrA-encoding taxa in GBS.
Fig. 3: Possible methanogenesis pathways in M. nevadensis.
Fig. 4: Headspace H2 concentration in triplicate cultures between day 12 and 20.
Fig. 5: Isotopic composition of in-situ and culture methane gas in a δ13C-δ 2H space.
Fig. 6: Schematic illustration of speculated modes of methane formation by M. nevadensis in the xyloglucan enrichment culture.

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Data availability

Metagenome and 16S rRNA gene sequence data were deposited in the NCBI database as Bioproject PRJNA956542.

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Acknowledgements

We thank Marike Palmer for advice on systematics, Alma Parada for discussions about the computational approach, Alexander Jaffe for feedback on the manuscript, David and Sandy Jamieson for access to Great Boiling Spring, Alexander Manriquez for help with sampling at GBS, and Michael Morikone for initial metagenome analysis of the xyloglucan culture. We appreciate the CSUSB Genomics course of Spring 2018 for assistance with xyloglucan culture DNA extraction and long read sequencing.

Funding

Funding was provided by the National Science Foundation (NSF) grant DEB 1557042 and National Aeronautics and Space Administration (NASA) grant 80NNSC17KO548 and 80NSSC19M0150. SB was further supported by the NASA Postdoctoral Program (section Astrobiology), administered by Oak Ridge Associated Universities under contract with NASA. MEQ received critical funding from Stanford’s IntroSems Plus program for undergraduate students. GLC was supported by the Miller Institute for Basic Research in Science at U.C. Berkeley. Additional funding for metagenomes was provided by the U.S. Department of Energy’s Joint Genome Institute (DOE-JGI) under project 10.46936/10.25585/60007294 and DOE grant DE-EE0000716; the Nevada Renewable Energy Consortium, funded by the DOE.

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Authors and Affiliations

  1. Department of Earth System Science, Stanford University, Stanford, CA, USA

    Steffen Buessecker, Melanie E. Quan & Anne E. Dekas

  2. Department of Molecular and Cell Biology, University of California, Berkeley, CA, USA

    Grayson L. Chadwick

  3. School of Life Sciences, University of Nevada, Las Vegas, Las Vegas, NV, USA

    Brian P. Hedlund

  4. Department of Biology, California State University, San Bernardino, San Bernardino, CA, USA

    Jeremy A. Dodsworth

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Contributions

SB and AED developed the experimental design with input from BPH and JAD. SB conducted the experiments with assistance from MEQ. JAD achieved enrichment of M. nevadensis and has maintained the XG-degrading culture long-term. Metagenomic work was done by SB and GLC. GLC performed the metabolic inference and further enrichment of M. nevadensis. SB and JAD conducted field work at GBS. SB wrote the paper with contributions from GLC, BPH, and AED, and all authors edited the final version.

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Correspondence to Steffen Buessecker or Anne E. Dekas.

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Buessecker, S., Chadwick, G.L., Quan, M.E. et al. Mcr-dependent methanogenesis in Archaeoglobaceae enriched from a terrestrial hot spring. ISME J 17, 1649–1659 (2023). https://doi.org/10.1038/s41396-023-01472-3

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