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Bdelloid rotifers deploy horizontally acquired biosynthetic genes against a fungal pathogen

Author

Listed:
  • Reuben W. Nowell

    (University of Oxford
    Imperial College London; Silwood Park Campus
    Charlotte Auerbach Road
    University of Stirling)

  • Fernando Rodriguez

    (Marine Biological Laboratory)

  • Bette J. Hecox-Lea

    (Marine Biological Laboratory)

  • David B. Mark Welch

    (Marine Biological Laboratory)

  • Irina R. Arkhipova

    (Marine Biological Laboratory)

  • Timothy G. Barraclough

    (University of Oxford
    Imperial College London; Silwood Park Campus)

  • Christopher G. Wilson

    (University of Oxford
    Imperial College London; Silwood Park Campus)

Abstract

Coevolutionary antagonism generates relentless selection that can favour genetic exchange, including transfer of antibiotic synthesis and resistance genes among bacteria, and sexual recombination of disease resistance alleles in eukaryotes. We report an unusual link between biological conflict and DNA transfer in bdelloid rotifers, microscopic animals whose genomes show elevated levels of horizontal gene transfer from non-metazoan taxa. When rotifers were challenged with a fungal pathogen, horizontally acquired genes were over twice as likely to be upregulated as other genes — a stronger enrichment than observed for abiotic stressors. Among hundreds of upregulated genes, the most markedly overrepresented were clusters resembling bacterial polyketide and nonribosomal peptide synthetases that produce antibiotics. Upregulation of these clusters in a pathogen-resistant rotifer species was nearly ten times stronger than in a susceptible species. By acquiring, domesticating, and expressing non-metazoan biosynthetic pathways, bdelloids may have evolved to resist natural enemies using antimicrobial mechanisms absent from other animals.

Suggested Citation

  • Reuben W. Nowell & Fernando Rodriguez & Bette J. Hecox-Lea & David B. Mark Welch & Irina R. Arkhipova & Timothy G. Barraclough & Christopher G. Wilson, 2024. "Bdelloid rotifers deploy horizontally acquired biosynthetic genes against a fungal pathogen," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-49919-1
    DOI: 10.1038/s41467-024-49919-1
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    References listed on IDEAS

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    1. Jean-François Flot & Boris Hespeels & Xiang Li & Benjamin Noel & Irina Arkhipova & Etienne G. J. Danchin & Andreas Hejnol & Bernard Henrissat & Romain Koszul & Jean-Marc Aury & Valérie Barbe & Roxane-, 2013. "Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga," Nature, Nature, vol. 500(7463), pages 453-457, August.
    2. Bates, Douglas & Mächler, Martin & Bolker, Ben & Walker, Steve, 2015. "Fitting Linear Mixed-Effects Models Using lme4," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 67(i01).
    3. Seemay Chou & Matthew D. Daugherty & S. Brook Peterson & Jacob Biboy & Youyun Yang & Brandon L. Jutras & Lillian K. Fritz-Laylin & Michael A. Ferrin & Brittany N. Harding & Christine Jacobs-Wagner & X, 2015. "Transferred interbacterial antagonism genes augment eukaryotic innate immune function," Nature, Nature, vol. 518(7537), pages 98-101, February.
    4. Elena V. Linardopoulou & Eleanor M. Williams & Yuxin Fan & Cynthia Friedman & Janet M. Young & Barbara J. Trask, 2005. "Human subtelomeres are hot spots of interchromosomal recombination and segmental duplication," Nature, Nature, vol. 437(7055), pages 94-100, September.
    5. Fernando Rodriguez & Irina A. Yushenova & Daniel DiCorpo & Irina R. Arkhipova, 2022. "Bacterial N4-methylcytosine as an epigenetic mark in eukaryotic DNA," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    6. Emilien Nicolas & Paul Simion & Marc Guérineau & Matthieu Terwagne & Mathilde Colinet & Julie Virgo & Maxime Lingurski & Anaïs Boutsen & Marc Dieu & Bernard Hallet & Karine Doninck, 2023. "Horizontal acquisition of a DNA ligase improves DNA damage tolerance in eukaryotes," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    7. Olga A. Vakhrusheva & Elena A. Mnatsakanova & Yan R. Galimov & Tatiana V. Neretina & Evgeny S. Gerasimov & Sergey A. Naumenko & Svetlana G. Ozerova & Arthur O. Zalevsky & Irina A. Yushenova & Fernando, 2020. "Genomic signatures of recombination in a natural population of the bdelloid rotifer Adineta vaga," Nature Communications, Nature, vol. 11(1), pages 1-17, December.
    8. Likui Feng & Matthew T. Gordon & Ying Liu & Kari B. Basso & Rebecca A. Butcher, 2021. "Mapping the biosynthetic pathway of a hybrid polyketide-nonribosomal peptide in a metazoan," Nature Communications, Nature, vol. 12(1), pages 1-11, December.
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