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Borgs are giant genetic elements with potential to expand metabolic capacity

Author

Listed:
  • Basem Al-Shayeb

    (University of California
    University of California)

  • Marie C. Schoelmerich

    (University of California)

  • Jacob West-Roberts

    (University of California)

  • Luis E. Valentin-Alvarado

    (University of California
    University of California)

  • Rohan Sachdeva

    (University of California
    University of California)

  • Susan Mullen

    (University of California)

  • Alexander Crits-Christoph

    (University of California
    University of California)

  • Michael J. Wilkins

    (Colorado State University)

  • Kenneth H. Williams

    (Lawrence Berkeley National Laboratory
    Rocky Mountain Biological Lab)

  • Jennifer A. Doudna

    (University of California
    University of California)

  • Jillian F. Banfield

    (University of California
    University of California
    University of California
    Lawrence Berkeley National Laboratory)

Abstract

Anaerobic methane oxidation exerts a key control on greenhouse gas emissions1, yet factors that modulate the activity of microorganisms performing this function remain poorly understood. Here we discovered extraordinarily large, diverse DNA sequences that primarily encode hypothetical proteins through studying groundwater, sediments and wetland soil where methane production and oxidation occur. Four curated, complete genomes are linear, up to approximately 1 Mb in length and share genome organization, including replichore 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 highly divergent archaeal extrachromosomal elements 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 spp. in four distinct ecosystems. Borgs provide methane-oxidizing Methanoperedens archaea access to genes encoding proteins involved in redox reactions and energy conservation (for example, clusters of multihaem cytochromes and methyl coenzyme M reductase). These data suggest that Borgs might have previously unrecognized roles in the metabolism of this group of archaea, which are known to modulate greenhouse gas emissions, but further studies are now needed to establish their functional relevance.

Suggested Citation

  • 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 & Jennif, 2022. "Borgs are giant genetic elements with potential to expand metabolic capacity," Nature, Nature, vol. 610(7933), pages 731-736, October.
  • Handle: RePEc:nat:nature:v:610:y:2022:i:7933:d:10.1038_s41586-022-05256-1
    DOI: 10.1038/s41586-022-05256-1
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    Cited by:

    1. Luis E. Valentin-Alvarado & Kathryn E. Appler & Valerie Anda & Marie C. Schoelmerich & Jacob West-Roberts & Veronika Kivenson & Alexander Crits-Christoph & Lynn Ly & Rohan Sachdeva & Chris Greening & , 2024. "Asgard archaea modulate potential methanogenesis substrates in wetland soil," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    2. Zhi-Ping Zhong & Jingjie Du & Stephan Köstlbacher & Petra Pjevac & Sandi Orlić & Matthew B. Sullivan, 2024. "Viral potential to modulate microbial methane metabolism varies by habitat," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    3. Marie C. Schoelmerich & Lynn Ly & Jacob West-Roberts & Ling-Dong Shi & Cong Shen & Nikhil S. Malvankar & Najwa Taib & Simonetta Gribaldo & Ben J. Woodcroft & Christopher W. Schadt & Basem Al-Shayeb & , 2024. "Borg extrachromosomal elements of methane-oxidizing archaea have conserved and expressed genetic repertoires," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    4. Marie C. Schoelmerich & Heleen T. Ouboter & Rohan Sachdeva & Petar I. Penev & Yuki Amano & Jacob West-Roberts & Cornelia U. Welte & Jillian F. Banfield, 2022. "A widespread group of large plasmids in methanotrophic Methanoperedens archaea," Nature Communications, Nature, vol. 13(1), pages 1-11, December.

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