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c-di-GMP modulates type IV MSHA pilus retraction and surface attachment in Vibrio cholerae

Author

Listed:
  • Kyle A. Floyd

    (University of California – Santa Cruz)

  • Calvin K. Lee

    (University of California – Los Angeles)

  • Wujing Xian

    (University of California – Los Angeles)

  • Mahmoud Nametalla

    (Brooklyn College
    CUNY Graduate Center)

  • Aneesa Valentine

    (Brooklyn College
    CUNY Graduate Center)

  • Benjamin Crair

    (Yale University)

  • Shiwei Zhu

    (Yale University)

  • Hannah Q. Hughes

    (Indiana University – Bloomington)

  • Jennifer L. Chlebek

    (Indiana University – Bloomington)

  • Daniel C. Wu

    (University of California – Santa Cruz)

  • Jin Hwan Park

    (University of California – Santa Cruz)

  • Ali M. Farhat

    (University of California – Los Angeles)

  • Charles J. Lomba

    (University of California – Los Angeles)

  • Courtney K. Ellison

    (Indiana University – Bloomington
    Princeton University)

  • Yves V. Brun

    (University of Montreal)

  • Javier Campos-Gomez

    (University of Alabama at Birmingham)

  • Ankur B. Dalia

    (Indiana University – Bloomington)

  • Jun Liu

    (Yale University)

  • Nicolas Biais

    (Brooklyn College
    CUNY Graduate Center)

  • Gerard C. L. Wong

    (University of California – Los Angeles)

  • Fitnat H. Yildiz

    (University of California – Santa Cruz)

Abstract

Biofilm formation by Vibrio cholerae facilitates environmental persistence, and hyperinfectivity within the host. Biofilm formation is regulated by 3’,5’-cyclic diguanylate (c-di-GMP) and requires production of the type IV mannose-sensitive hemagglutinin (MSHA) pilus. Here, we show that the MSHA pilus is a dynamic extendable and retractable system, and its activity is directly controlled by c-di-GMP. The interaction between c-di-GMP and the ATPase MshE promotes pilus extension, whereas low levels of c-di-GMP correlate with enhanced retraction. Loss of retraction facilitated by the ATPase PilT increases near-surface roaming motility, and impairs initial surface attachment. However, prolonged retraction upon surface attachment results in reduced MSHA-mediated surface anchoring and increased levels of detachment. Our results indicate that c-di-GMP directly controls MshE activity, thus regulating MSHA pilus extension and retraction dynamics, and modulating V. cholerae surface attachment and colonization.

Suggested Citation

  • Kyle A. Floyd & Calvin K. Lee & Wujing Xian & Mahmoud Nametalla & Aneesa Valentine & Benjamin Crair & Shiwei Zhu & Hannah Q. Hughes & Jennifer L. Chlebek & Daniel C. Wu & Jin Hwan Park & Ali M. Farhat, 2020. "c-di-GMP modulates type IV MSHA pilus retraction and surface attachment in Vibrio cholerae," Nature Communications, Nature, vol. 11(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-020-15331-8
    DOI: 10.1038/s41467-020-15331-8
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    Cited by:

    1. Xin Huang & Thomas Nero & Ranjuna Weerasekera & Katherine H. Matej & Alex Hinbest & Zhaowei Jiang & Rebecca F. Lee & Longjun Wu & Cecilia Chak & Japinder Nijjer & Isabella Gibaldi & Hang Yang & Nathan, 2023. "Vibrio cholerae biofilms use modular adhesins with glycan-targeting and nonspecific surface binding domains for colonization," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    2. Xia Li & Wenfang Yin & Junjie Desmond Lin & Yong Zhang & Quan Guo & Gerun Wang & Xiayu Chen & Binbin Cui & Mingfang Wang & Min Chen & Peng Li & Ya-Wen He & Wei Qian & Haibin Luo & Lian-Hui Zhang & Xue, 2023. "Regulation of the physiology and virulence of Ralstonia solanacearum by the second messenger 2′,3′-cyclic guanosine monophosphate," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    3. María Pérez-Burgos & Marco Herfurth & Andreas Kaczmarczyk & Andrea Harms & Katrin Huber & Urs Jenal & Timo Glatter & Lotte Søgaard-Andersen, 2024. "A deterministic, c-di-GMP-dependent program ensures the generation of phenotypically similar, symmetric daughter cells during cytokinesis," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    4. Cong Liu & Di Sun & Jiawen Liu & Ying Chen & Xuge Zhou & Yunrui Ru & Jingrong Zhu & Weijie Liu, 2022. "cAMP and c-di-GMP synergistically support biofilm maintenance through the direct interaction of their effectors," Nature Communications, Nature, vol. 13(1), pages 1-15, December.

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