Tandem repeats in giant archaeal Borg elements undergo rapid evolution and create new intrinsically disordered regions in proteins

Schoelmerich, Marie Charlotte; Sachdeva, Rohan; West-Roberts, Jacob; Waldburger, Lucas; Banfield, Jillian F.

doi:10.1371/journal.pbio.3001980

Tandem repeats in giant archaeal Borg elements undergo rapid evolution and create new intrinsically disordered regions in proteins

Journal Article · Thu Jan 26 00:00:00 EST 2023 · PLoS Biology (Online)

DOI:https://doi.org/10.1371/journal.pbio.3001980· OSTI ID:2470776

Schoelmerich, Marie Charlotte ^[1]; Sachdeva, Rohan ^[1]; West-Roberts, Jacob ^[1]; Waldburger, Lucas ^[1]; ^[2]

University of California, Berkeley, CA (United States)
University of California, Berkeley, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Borgs are huge, linear extrachromosomal elements associated with anaerobic methane-oxidizing archaea. Striking features of Borg genomes are pervasive tandem direct repeat (TR) regions. Here, we present six new Borg genomes and investigate the characteristics of TRs in all ten complete Borg genomes. We find that TR regions are rapidly evolving, recently formed, arise independently, and are virtually absent in host Methanoperedens genomes. Flanking partial repeats and A-enriched character constrain the TR formation mechanism. TRs can be in intergenic regions, where they might serve as regulatory RNAs, or in open reading frames (ORFs). TRs in ORFs are under very strong selective pressure, leading to perfect amino acid TRs (aaTRs) that are commonly intrinsically disordered regions. Proteins with aaTRs are often extracellular or membrane proteins, and functionally similar or homologous proteins often have aaTRs composed of the same amino acids. We propose that Borg aaTR-proteins functionally diversify Methanoperedens and all TRs are crucial for specific Borg–host associations and possibly cospeciation.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: Bill & Melinda Gates Foundation; USDOE

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 2470776

Journal Information:: PLoS Biology (Online), Journal Name: PLoS Biology (Online) Journal Issue: 1 Vol. 21; ISSN 1545-7885

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

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Tandem repeats in giant archaeal Borg elements undergo rapid evolution and create new intrinsically disordered regions in proteins

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