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Ecology and molecular targets of hypermutation in the global microbiome

Author

Listed:
  • Simon Roux

    (Lawrence Berkeley National Laboratory)

  • Blair G. Paul

    (Marine Biological Laboratory)

  • Sarah C. Bagby

    (Case Western Reserve University)

  • Stephen Nayfach

    (Lawrence Berkeley National Laboratory)

  • Michelle A. Allen

    (The University of New South Wales)

  • Graeme Attwood

    (AgResearch Limited, Grasslands Research Centre)

  • Ricardo Cavicchioli

    (The University of New South Wales)

  • Ludmila Chistoserdova

    (University of Washington)

  • Robert J. Gruninger

    (Lethbridge Research and Development Centre, Agriculture and Agri-Food Canada)

  • Steven J. Hallam

    (University of British Columbia
    Graduate Program in Bioinformatics, University of British Columbia, Genome Sciences Centre
    Genome Science and Technology Program, University of British Columbia
    Life Sciences Institute, University of British Columbia)

  • Maria E. Hernandez

    (Instituto de Ecología A.C. Red de Manejo Biotechnológico de Recursos. Xalapa)

  • Matthias Hess

    (University of California Davis)

  • Wen-Tso Liu

    (University of Illinois at Urbana-Champaign)

  • Tim A. McAllister

    (Lethbridge Research and Development Centre, Agriculture and Agri-Food Canada)

  • Michelle A. O’Malley

    (University of California Santa Barbara)

  • Xuefeng Peng

    (Marine Science Institute, University of California Santa Barbara)

  • Virginia I. Rich

    (Ohio State University)

  • Scott R. Saleska

    (University of Arizona)

  • Emiley A. Eloe-Fadrosh

    (Lawrence Berkeley National Laboratory)

Abstract

Changes in the sequence of an organism’s genome, i.e., mutations, are the raw material of evolution. The frequency and location of mutations can be constrained by specific molecular mechanisms, such as diversity-generating retroelements (DGRs). DGRs have been characterized from cultivated bacteria and bacteriophages, and perform error-prone reverse transcription leading to mutations being introduced in specific target genes. DGR loci were also identified in several metagenomes, but the ecological roles and evolutionary drivers of these DGRs remain poorly understood. Here, we analyze a dataset of >30,000 DGRs from public metagenomes, establish six major lineages of DGRs including three primarily encoded by phages and seemingly used to diversify host attachment proteins, and demonstrate that DGRs are broadly active and responsible for >10% of all amino acid changes in some organisms. Overall, these results highlight the constraints under which DGRs evolve, and elucidate several distinct roles these elements play in natural communities.

Suggested Citation

  • Simon Roux & Blair G. Paul & Sarah C. Bagby & Stephen Nayfach & Michelle A. Allen & Graeme Attwood & Ricardo Cavicchioli & Ludmila Chistoserdova & Robert J. Gruninger & Steven J. Hallam & Maria E. Her, 2021. "Ecology and molecular targets of hypermutation in the global microbiome," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-23402-7
    DOI: 10.1038/s41467-021-23402-7
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    Cited by:

    1. Joachim Johansen & Damian R. Plichta & Jakob Nybo Nissen & Marie Louise Jespersen & Shiraz A. Shah & Ling Deng & Jakob Stokholm & Hans Bisgaard & Dennis Sandris Nielsen & Søren J. Sørensen & Simon Ras, 2022. "Genome binning of viral entities from bulk metagenomics data," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    2. Piotr Rozwalak & Jakub Barylski & Yasas Wijesekara & Bas E. Dutilh & Andrzej Zielezinski, 2024. "Ultraconserved bacteriophage genome sequence identified in 1300-year-old human palaeofaeces," Nature Communications, Nature, vol. 15(1), pages 1-10, December.

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