Chadwick, Grayson L. and Skennerton, Connor T. and Laso-Pérez, Rafael and Leu, Andy O. and Speth, Daan R. and Yu, Hang and Morgan-Lang, Connor and Hatzenpichler, Roland and Goudeau, Danielle and Malmstrom, Rex and Brazelton, William J. and Woyke, Tanja and Hallam, Steven J. and Tyson, Gene W. and Wegener, Gunter and Boetius, Antje and Orphan, Victoria J. (2022) Comparative genomics reveals electron transfer and syntrophic mechanisms differentiating methanotrophic and methanogenic archaea. PLoS Biology, 20 (1). Art. No. e3001508. ISSN 1544-9173. PMCID PMC9012536. doi:10.1371/journal.pbio.3001508. https://resolver.caltech.edu/CaltechAUTHORS:20210929-145417503
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Abstract
The anaerobic oxidation of methane coupled to sulfate reduction is a microbially mediated process requiring a syntrophic partnership between anaerobic methanotrophic (ANME) archaea and sulfate-reducing bacteria (SRB). Based on genome taxonomy, ANME lineages are polyphyletic within the phylum Halobacterota, none of which have been isolated in pure culture. Here, we reconstruct 28 ANME genomes from environmental metagenomes and flow sorted syntrophic consortia. Together with a reanalysis of previously published datasets, these genomes enable a comparative analysis of all marine ANME clades. We review the genomic features that separate ANME from their methanogenic relatives and identify what differentiates ANME clades. Large multiheme cytochromes and bioenergetic complexes predicted to be involved in novel electron bifurcation reactions are well distributed and conserved in the ANME archaea, while significant variations in the anabolic C1 pathways exists between clades. Our analysis raises the possibility that methylotrophic methanogenesis may have evolved from a methanotrophic ancestor.
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| Additional Information: | © 2022. This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication. Received: August 27, 2021; Accepted: December 8, 2021; Published: January 5, 2022. We extend our sincere thanks to Emil Ruff, Anke Meyerdierks, and Katrin Knittel for their contributions to sample preparation and sequencing of ANME from the Haakon Mosby and Amon mud volcano, Susanne Menger for the cultivation of AOM consortia at the Max Planck Institute for Marine Microbiology, Ed Delong, Christina Preston, and Peter Girguis for their early support of this project and contribution of fosmid library data at MBARI, Shulei Sun, Mark Ellisman (UCSD), Titus Brown, Rachel Poretsky, Josh Steele (Caltech), and Fauzi Haroon (University of Queensland) for their contributions to the bioinformatic analysis of ANME, and Stephanie Connon and Alice Michel (Caltech) for assistance with sequencing 16S rRNA genes from single AOM consortia. We acknowledge the support of all crews of the numerous expeditions that were essential for deep-sea sample collection and processing, including Chief Scientist Susan Lang and the scientific party of the 2018 Lost City Expedition. Grayson L. Chadwick is currently supported by the Miller Institute for Basic Research in Science, University of California Berkeley and Victoria J. Orphan is a Canadian Institute for Advanced Research fellow (CIFAR) in the Earth 4D program. Funding: The work conducted by the U.S. Department of Energy Joint Genome Institute [https://jgi.doe.gov/], a Department of Energy Office of Science User Facility, is supported under Contract No. DE-AC02-05CH11231. Funding for this study was received by the DFG Leibniz grant [https://www.dfg.de/en/funded_projects/prizewinners/leibniz_prize/index.html] and by the Max Planck Society [https://www.mpg.de/] to A.B. Genomes of BONCAT-FACS sorted ANME-consortia were generated via a Joint Genome Institute Director Discretionary Project Award to R.H. and V.J.O. [https://jgi.doe.gov/]. Work with the fosmid libraries was performed under the auspices of the Natural Sciences and Engineering Research Council of Canada, Genome British Columbia, the Canada Foundation for Innovation, Compute/Calcul Canada, and the U.S. Department of Energy Joint Genome Institute supported by the Office of Science of U.S. Department of Energy Contract DE-AC02-05CH11231 to S.H. The National Science Foundation provided support for the Lost City cruise and metagenome sequencing to W.B. (OCE- 1536702/1536405). [https://www.nsf.gov/]. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Author Contributions: Conceptualization: Grayson L. Chadwick, Connor T. Skennerton, Roland Hatzenpichler, Steven J. Hallam, Gene W. Tyson, Gunter Wegener, Antje Boetius, Victoria J. Orphan. Data curation: Grayson L. Chadwick, Connor T. Skennerton, Rafael Laso-Perez, Andy O. Leu, Daan R. Speth, Hang Yu, Connor Morgan-Lang, Roland Hatzenpichler, Danielle Goudeau, Rex Malmstrom, William J. Brazelton, Tanja Woyke, Steven J. Hallam, Gene W. Tyson. Formal analysis: Grayson L. Chadwick, Connor T. Skennerton, Daan R. Speth, Roland Hatzenpichler, Rex Malmstrom, Steven J. Hallam, Gunter Wegener, Victoria J. Orphan. Funding acquisition: Roland Hatzenpichler, Rex Malmstrom, Tanja Woyke, Antje Boetius, Victoria J. Orphan. Investigation: Grayson L. Chadwick, Connor T. Skennerton, Rafael Laso-Perez, Andy O. Leu, Daan R. Speth, Hang Yu, Connor Morgan-Lang, Steven J. Hallam, Gene W. Tyson, Antje Boetius, Victoria J. Orphan. Methodology: Grayson L. Chadwick, Connor T. Skennerton, Daan R. Speth, Connor Morgan- Lang, Roland Hatzenpichler, Danielle Goudeau, Rex Malmstrom, Steven J. Hallam, Gene W. Tyson, Victoria J. Orphan. Project administration: Victoria J. Orphan. Resources: Roland Hatzenpichler, William J. Brazelton, Gunter Wegener, Antje Boetius. Supervision: Tanja Woyke, Steven J. Hallam, Gene W. Tyson, Gunter Wegener, Antje Boetius, Victoria J. Orphan. Validation: Grayson L. Chadwick, Connor T. Skennerton. Visualization: Grayson L. Chadwick, Connor T. Skennerton. Writing – original draft: Grayson L. Chadwick, Connor T. Skennerton, Victoria J. Orphan. Writing – review & editing: Grayson L. Chadwick, Connor T. Skennerton, Rafael Laso-Perez, Andy O. Leu, Daan R. Speth, Hang Yu, Roland Hatzenpichler, Rex Malmstrom, William J. Brazelton, Steven J. Hallam, Gene W. Tyson, Gunter Wegener, Antje Boetius, Victoria J. Orphan. Competing interests: S.J.H. is a co-founder of Koonkie Inc., a bioinformatics consulting company that designs and provides scalable algorithmic and data analytics solutions in the cloud. Data Availability: The novel genomes reported in this study are all available in the NCBI database. The accession numbers for these genomes are provided in Table 1. Data products such as protein alignments, phylogenetic tree files, and manual gene annotation lists are provided in the Supporting Information files. | ||||||||||||||||||||||||||||||||||||
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| Issue or Number: | 1 | ||||||||||||||||||||||||||||||||||||
| PubMed Central ID: | PMC9012536 | ||||||||||||||||||||||||||||||||||||
| DOI: | 10.1371/journal.pbio.3001508 | ||||||||||||||||||||||||||||||||||||
| Record Number: | CaltechAUTHORS:20210929-145417503 | ||||||||||||||||||||||||||||||||||||
| Persistent URL: | https://resolver.caltech.edu/CaltechAUTHORS:20210929-145417503 | ||||||||||||||||||||||||||||||||||||
| Official Citation: | Chadwick GL, Skennerton CT, Laso-Perez R, Leu AO, Speth DR, Yu H, et al. (2022) Comparative genomics reveals electron transfer and syntrophic mechanisms differentiating methanotrophic and methanogenic archaea. PLoS Biol 20(1): e3001508. https://doi.org/10.1371/journal.pbio.3001508 | ||||||||||||||||||||||||||||||||||||
| Usage Policy: | No commercial reproduction, distribution, display or performance rights in this work are provided. | ||||||||||||||||||||||||||||||||||||
| ID Code: | 111085 | ||||||||||||||||||||||||||||||||||||
| Collection: | CaltechAUTHORS | ||||||||||||||||||||||||||||||||||||
| Deposited By: | Tony Diaz | ||||||||||||||||||||||||||||||||||||
| Deposited On: | 29 Sep 2021 16:46 | ||||||||||||||||||||||||||||||||||||
| Last Modified: | 25 Apr 2022 21:12 |
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