Convergent evolution of viral-like Borg archaeal extrachromosomal elements and giant eukaryotic viruses

Jillian F. Banfield (), Luis E. Valentin-Alvarado, Ling-Dong Shi, Colin Michael Robinson, Rebecca S. Bamert, Fasseli Coulibaly, Zachary K. Barth, Frank O. Aylward, Marie C. Schoelmerich, Shufei Lei, Rohan Sachdeva and Gavin J. Knott ()
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Jillian F. Banfield: Monash University, Biomedicine Discovery Institute
Luis E. Valentin-Alvarado: Monash University, Biomedicine Discovery Institute
Ling-Dong Shi: Berkeley, Innovative Genomics Institute, UC Berkeley
Colin Michael Robinson: Berkeley, Plant and Microbial Biology, UC Berkeley
Rebecca S. Bamert: Monash University, Biomedicine Discovery Institute
Fasseli Coulibaly: Berkeley, Innovative Genomics Institute, UC Berkeley
Zachary K. Barth: Virginia Polytechnic Institute and State University
Frank O. Aylward: Virginia Polytechnic Institute and State University
Marie C. Schoelmerich: Berkeley, Innovative Genomics Institute, UC Berkeley
Shufei Lei: Berkeley, Innovative Genomics Institute, UC Berkeley
Rohan Sachdeva: Berkeley, Innovative Genomics Institute, UC Berkeley
Gavin J. Knott: Monash University, Biomedicine Discovery Institute

Nature Communications, 2025, vol. 16, issue 1, 1-14

Abstract: Abstract Borgs are huge extrachromosomal elements of anaerobic methane-oxidizing archaea. They exist in exceedingly complex microbiomes, lack cultivated hosts and have few protein functional annotations, precluding their classification as plasmids, viruses or other. Here, we use in silico structure prediction methods to investigate potential roles for ~10,000 Borg proteins. Prioritizing analysis of multicopy genes that could signal importance for Borg lifestyles, we uncover highly represented de-ubiquitination-like Zn-metalloproteases that may counter host targeting of Borg proteins for proteolysis. Also prevalent are clusters of multicopy genes for production of diverse glycoconjugates that could contribute to decoration of the host cell surface, or of putative capsid proteins that we predict multimerize into pentagonal and hexagonal arrays. Features including megabase-scale linear genomes with inverted terminal repeats, genomic repertoires for energy metabolism, central carbon compound transformations and translation, and pervasive direct repeat regions are shared with giant viruses of eukaryotes, although analyses suggest that these parallels arose via convergent evolution. If Borgs are giant archaeal viruses they would fill the gap in the tri(um)virate of giant viruses of all three domains of life.

Date: 2025
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DOI: 10.1038/s41467-025-65646-7

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