Borg extrachromosomal elements of methane-oxidizing archaea have conserved and expressed genetic repertoires

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, Xiaoguang Dai, Christopher Mozsary, Scott Hickey, Christine He, John Beaulaurier, Sissel Juul, Rohan Sachdeva and Jillian F. Banfield ()
Additional contact information
Marie C. Schoelmerich: University of California
Lynn Ly: Oxford Nanopore Technologies Inc
Jacob West-Roberts: University of California
Ling-Dong Shi: University of California
Cong Shen: Yale University
Nikhil S. Malvankar: Yale University
Najwa Taib: Unit Evolutionary Biology of the Microbial Cell
Simonetta Gribaldo: Unit Evolutionary Biology of the Microbial Cell
Ben J. Woodcroft: Queensland University of Technology (QUT), Translational Research Institute
Christopher W. Schadt: Oak Ridge National Laboratory
Basem Al-Shayeb: University of California
Xiaoguang Dai: Oxford Nanopore Technologies Inc
Christopher Mozsary: Oxford Nanopore Technologies Inc
Scott Hickey: Oxford Nanopore Technologies Inc
Christine He: Oxford Nanopore Technologies Inc
John Beaulaurier: Oxford Nanopore Technologies Inc
Sissel Juul: Oxford Nanopore Technologies Inc
Rohan Sachdeva: University of California
Jillian F. Banfield: University of California

Nature Communications, 2024, vol. 15, issue 1, 1-17

Abstract: Abstract Borgs are huge extrachromosomal elements (ECE) of anaerobic methane-consuming “Candidatus Methanoperedens” archaea. Here, we used nanopore sequencing to validate published complete genomes curated from short reads and to reconstruct new genomes. 13 complete and four near-complete linear genomes share 40 genes that define a largely syntenous genome backbone. We use these conserved genes to identify new Borgs from peatland soil and to delineate Borg phylogeny, revealing two major clades. Remarkably, Borg genes encoding nanowire-like electron-transferring cytochromes and cell surface proteins are more highly expressed than those of host Methanoperedens, indicating that Borgs augment the Methanoperedens activity in situ. We reconstructed the first complete 4.00 Mbp genome for a Methanoperedens that is inferred to be a Borg host and predicted its methylation motifs, which differ from pervasive TC and CC methylation motifs of the Borgs. Thus, methylation may enable Methanoperedens to distinguish their genomes from those of Borgs. Very high Borg to Methanoperedens ratios and structural predictions suggest that Borgs may be capable of encapsulation. The findings clearly define Borgs as a distinct class of ECE with shared genomic signatures, establish their diversification from a common ancestor with genetic inheritance, and raise the possibility of periodic existence outside of host cells.

Date: 2024
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DOI: 10.1038/s41467-024-49548-8

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