Borgs are giant genetic elements with potential to expand metabolic capacity

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 and Jillian F. Banfield ()
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Basem Al-Shayeb: University of California
Marie C. Schoelmerich: University of California
Jacob West-Roberts: University of California
Luis E. Valentin-Alvarado: University of California
Rohan Sachdeva: University of California
Susan Mullen: University of California
Alexander Crits-Christoph: University of California
Michael J. Wilkins: Colorado State University
Kenneth H. Williams: Lawrence Berkeley National Laboratory
Jennifer A. Doudna: University of California
Jillian F. Banfield: University of California

Nature, 2022, vol. 610, issue 7933, 731-736

Abstract: 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.

Date: 2022
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DOI: 10.1038/s41586-022-05256-1

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