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Borgs are giant extrachromosomal elements with the potential to augment methane oxidation

View ORCID ProfileBasem Al-Shayeb, View ORCID ProfileMarie C. Schoelmerich, Jacob West-Roberts, Luis E. Valentin-Alvarado, View ORCID ProfileRohan Sachdeva, Susan Mullen, View ORCID ProfileAlexander Crits-Christoph, View ORCID ProfileMichael J. Wilkins, View ORCID ProfileKenneth H. Williams, Jennifer A. Doudna, Jillian F. Banfield
doi: https://doi.org/10.1101/2021.07.10.451761
Basem Al-Shayeb
1Innovative Genomics Institute, University of California, Berkeley, CA, USA
2Department of Plant and Microbial Biology, University of California, Berkeley, CA, USA
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  • ORCID record for Basem Al-Shayeb
Marie C. Schoelmerich
1Innovative Genomics Institute, University of California, Berkeley, CA, USA
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  • ORCID record for Marie C. Schoelmerich
Jacob West-Roberts
3Environmental Science, Policy and Management, University of California, Berkeley, CA, USA
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Luis E. Valentin-Alvarado
1Innovative Genomics Institute, University of California, Berkeley, CA, USA
2Department of Plant and Microbial Biology, University of California, Berkeley, CA, USA
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Rohan Sachdeva
1Innovative Genomics Institute, University of California, Berkeley, CA, USA
4Earth and Planetary Science, University of California, Berkeley, CA, USA
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Susan Mullen
4Earth and Planetary Science, University of California, Berkeley, CA, USA
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Alexander Crits-Christoph
1Innovative Genomics Institute, University of California, Berkeley, CA, USA
2Department of Plant and Microbial Biology, University of California, Berkeley, CA, USA
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Michael J. Wilkins
5Department of Soil and Crop Sciences, Colorado State University, Colorado, USA
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Kenneth H. Williams
6Lawrence Berkeley National Laboratory, Berkeley, CA, USA
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  • ORCID record for Kenneth H. Williams
Jennifer A. Doudna
1Innovative Genomics Institute, University of California, Berkeley, CA, USA
7Department of Chemistry, University of California, Berkeley, CA, USA
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Jillian F. Banfield
1Innovative Genomics Institute, University of California, Berkeley, CA, USA
3Environmental Science, Policy and Management, University of California, Berkeley, CA, USA
4Earth and Planetary Science, University of California, Berkeley, CA, USA
6Lawrence Berkeley National Laboratory, Berkeley, CA, USA
8The University of Melbourne, Australia
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  • For correspondence: jbanfield@berkeley.edu
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Summary

Anaerobic methane oxidation exerts a key control on greenhouse gas emissions 1, yet factors that modulate the activity of microorganisms performing this function remain little explored. In studying groundwater, sediments, and wetland soil where methane production and oxidation occur, we discovered extraordinarily large, diverse DNA sequences that primarily encode hypothetical proteins. Four curated, complete genomes are linear, up to ~1 Mbp in length and share genome organization, including replicore structure, long inverted terminal repeats, and genome-wide unique perfect tandem direct repeats that are intergenic or generate amino acid repeats. We infer that these are a new type of archaeal extrachromosomal element with a distinct evolutionary origin. Gene sequence similarity, phylogeny, and local divergence of sequence composition indicate that many of their genes were assimilated from methane-oxidizing Methanoperedens archaea. We refer to these elements as “Borgs”. We identified at least 19 different Borg types coexisting with Methanoperedens in four distinct ecosystems. Borg genes expand redox and respiratory capacity (e.g., clusters of multiheme cytochromes), ability to respond to changing environmental conditions, and likely augment Methanoperedens capacity for methane oxidation (e.g., methyl coenzyme M reductase). By this process, Borgs could play a previously unrecognized role in controlling greenhouse gas emissions.

Competing Interest Statement

J.A.D. is a co-founder of Caribou Biosciences, Editas Medicine, Intellia Therapeutics, Scribe Therapeutics, and Mammoth Biosciences. J.A.D. is a scientific advisory board member of Caribou Biosciences, Intellia Therapeutics, eFFECTOR Therapeutics, Scribe Therapeutics, Synthego, Inari Agriculture and Mammoth Biosciences. J.A.D. is a director at Johnson & Johnson and has sponsored research projects by Pfizer, Roche Biopharma, and Biogen. J.F.B. is a founder of Metagenomi. The remaining authors declare no competing interests.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Borgs are giant extrachromosomal elements with the potential to augment methane oxidation
Basem Al-Shayeb, Marie C. Schoelmerich, Jacob West-Roberts, Luis E. Valentin-Alvarado, Rohan Sachdeva, Susan Mullen, Alexander Crits-Christoph, Michael J. Wilkins, Kenneth H. Williams, Jennifer A. Doudna, Jillian F. Banfield
bioRxiv 2021.07.10.451761; doi: https://doi.org/10.1101/2021.07.10.451761
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Borgs are giant extrachromosomal elements with the potential to augment methane oxidation
Basem Al-Shayeb, Marie C. Schoelmerich, Jacob West-Roberts, Luis E. Valentin-Alvarado, Rohan Sachdeva, Susan Mullen, Alexander Crits-Christoph, Michael J. Wilkins, Kenneth H. Williams, Jennifer A. Doudna, Jillian F. Banfield
bioRxiv 2021.07.10.451761; doi: https://doi.org/10.1101/2021.07.10.451761

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