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

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....

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Main Authors: Marie Charlotte Schoelmerich, Rohan Sachdeva, Jacob West-Roberts, Lucas Waldburger, Jillian F Banfield
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2023-01-01
Series:PLoS Biology
Online Access:https://doi.org/10.1371/journal.pbio.3001980
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author Marie Charlotte Schoelmerich
Rohan Sachdeva
Jacob West-Roberts
Lucas Waldburger
Jillian F Banfield
author_facet Marie Charlotte Schoelmerich
Rohan Sachdeva
Jacob West-Roberts
Lucas Waldburger
Jillian F Banfield
author_sort Marie Charlotte Schoelmerich
collection DOAJ
description 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.
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spelling doaj.art-c241af8b12f14f2d933774eb88d9dbcd2023-02-25T05:30:52ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852023-01-01211e300198010.1371/journal.pbio.3001980Tandem repeats in giant archaeal Borg elements undergo rapid evolution and create new intrinsically disordered regions in proteins.Marie Charlotte SchoelmerichRohan SachdevaJacob West-RobertsLucas WaldburgerJillian F BanfieldBorgs 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.https://doi.org/10.1371/journal.pbio.3001980
spellingShingle Marie Charlotte Schoelmerich
Rohan Sachdeva
Jacob West-Roberts
Lucas Waldburger
Jillian F Banfield
Tandem repeats in giant archaeal Borg elements undergo rapid evolution and create new intrinsically disordered regions in proteins.
PLoS Biology
title Tandem repeats in giant archaeal Borg elements undergo rapid evolution and create new intrinsically disordered regions in proteins.
title_full Tandem repeats in giant archaeal Borg elements undergo rapid evolution and create new intrinsically disordered regions in proteins.
title_fullStr Tandem repeats in giant archaeal Borg elements undergo rapid evolution and create new intrinsically disordered regions in proteins.
title_full_unstemmed Tandem repeats in giant archaeal Borg elements undergo rapid evolution and create new intrinsically disordered regions in proteins.
title_short Tandem repeats in giant archaeal Borg elements undergo rapid evolution and create new intrinsically disordered regions in proteins.
title_sort tandem repeats in giant archaeal borg elements undergo rapid evolution and create new intrinsically disordered regions in proteins
url https://doi.org/10.1371/journal.pbio.3001980
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