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Broadly conserved FlgV controls flagellar assembly and Borrelia burgdorferi dissemination in mice

Author

Listed:
  • Maxime Zamba-Campero

    (National Institutes of Health)

  • Daniel Soliman

    (National Institutes of Health)

  • Huaxin Yu

    (Yale School of Medicine
    Yale University)

  • Amanda G. Lasseter

    (University of Central Florida College of Medicine)

  • Yuen-Yan Chang

    (National Institutes of Health)

  • Julia L. Silberman

    (National Institutes of Health)

  • Jun Liu

    (Yale School of Medicine
    Yale University)

  • L. Aravind

    (National Institutes of Health)

  • Mollie W. Jewett

    (University of Central Florida College of Medicine)

  • Gisela Storz

    (National Institutes of Health)

  • Philip P. Adams

    (National Institutes of Health
    University of Central Florida College of Medicine
    National Institutes of Health
    National Institutes of Health)

Abstract

Flagella propel pathogens through their environments, yet are expensive to synthesize and are immunogenic. Thus, complex hierarchical regulatory networks control flagellar gene expression. Spirochetes are highly motile bacteria, but peculiarly, the archetypal flagellar regulator σ28 is absent in the Lyme spirochete Borrelia burgdorferi. Here, we show that gene bb0268 (flgV) in B. burgdorferi, previously and incorrectly annotated to encode the RNA-binding protein Hfq, is instead a structural flagellar component that modulates flagellar assembly. The flgV gene is broadly conserved in the flagellar superoperon alongside σ28 in many Spirochaetae, Firmicutes and other phyla, with distant homologs in Epsilonproteobacteria. We find that B. burgdorferi FlgV is localized within flagellar basal bodies, and strains lacking flgV produce fewer and shorter flagellar filaments and are defective in cell division and motility. During the enzootic cycle, flgV-deficient B. burgdorferi survive and replicate in Ixodes ticks but are attenuated for infection and dissemination in mice. Our work defines infection timepoints when spirochete motility is most crucial and implicates FlgV as a broadly distributed structural flagellar component that modulates flagellar assembly.

Suggested Citation

  • Maxime Zamba-Campero & Daniel Soliman & Huaxin Yu & Amanda G. Lasseter & Yuen-Yan Chang & Julia L. Silberman & Jun Liu & L. Aravind & Mollie W. Jewett & Gisela Storz & Philip P. Adams, 2024. "Broadly conserved FlgV controls flagellar assembly and Borrelia burgdorferi dissemination in mice," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-54806-w
    DOI: 10.1038/s41467-024-54806-w
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    References listed on IDEAS

    as
    1. Emily Petroni & Caroline Esnault & Daniel Tetreault & Ryan K. Dale & Gisela Storz & Philip P. Adams, 2023. "Extensive diversity in RNA termination and regulation revealed by transcriptome mapping for the Lyme pathogen Borrelia burgdorferi," Nature Communications, Nature, vol. 14(1), pages 1-23, December.
    2. Josh Abramson & Jonas Adler & Jack Dunger & Richard Evans & Tim Green & Alexander Pritzel & Olaf Ronneberger & Lindsay Willmore & Andrew J. Ballard & Joshua Bambrick & Sebastian W. Bodenstein & David , 2024. "Accurate structure prediction of biomolecular interactions with AlphaFold 3," Nature, Nature, vol. 630(8016), pages 493-500, June.
    3. Jenny Wachter & Britney Cheff & Chad Hillman & Valentina Carracoi & David W. Dorward & Craig Martens & Kent Barbian & Glenn Nardone & L. Renee Olano & Margie Kinnersley & Patrick R. Secor & Patricia A, 2023. "Coupled induction of prophage and virulence factors during tick transmission of the Lyme disease spirochete," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
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