Crash landing of Vibrio cholerae by MSHA pili-assisted braking and anchoring in a viscoelastic environment

Mannose-sensitive hemagglutinin (MSHA) pili and flagellum are critical for the surface attachment of Vibrio cholerae, the first step of V. cholerae colonization on host surfaces. However, the cell landing mechanism remains largely unknown, particularly in viscoelastic environments such as the mucus...

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Main Authors: Wenchao Zhang, Mei Luo, Chunying Feng, Huaqing Liu, Hong Zhang, Rachel R Bennett, Andrew S Utada, Zhi Liu, Kun Zhao
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2021-07-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/60655
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spelling doaj-b91a8051d0de4d83999dbc45b15d78f32021-07-15T14:22:39ZengeLife Sciences Publications LtdeLife2050-084X2021-07-011010.7554/eLife.60655Crash landing of Vibrio cholerae by MSHA pili-assisted braking and anchoring in a viscoelastic environmentWenchao Zhang0Mei Luo1Chunying Feng2Huaqing Liu3Hong Zhang4Rachel R Bennett5https://orcid.org/0000-0002-6409-6967Andrew S Utada6https://orcid.org/0000-0003-4542-6315Zhi Liu7Kun Zhao8https://orcid.org/0000-0003-3928-1981Frontier Science Center for Synthetic Biology and Key Laboratory of Systems Bioengineering (Ministry of Education), School of Chemical Engineering and Technology, Tianjin University, Tianjin, ChinaDepartment of Biotechnology, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, ChinaFrontier Science Center for Synthetic Biology and Key Laboratory of Systems Bioengineering (Ministry of Education), School of Chemical Engineering and Technology, Tianjin University, Tianjin, ChinaFrontier Science Center for Synthetic Biology and Key Laboratory of Systems Bioengineering (Ministry of Education), School of Chemical Engineering and Technology, Tianjin University, Tianjin, ChinaFrontier Science Center for Synthetic Biology and Key Laboratory of Systems Bioengineering (Ministry of Education), School of Chemical Engineering and Technology, Tianjin University, Tianjin, ChinaSchool of Mathematics, University of Bristol, Bristol, United KingdomFaculty of Life and Environmental Sciences, University of Tsukuba, Ibaraki, Japan; The Microbiology Research Center for Sustainability, University of Tsukuba, Ibaraki, JapanDepartment of Biotechnology, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, ChinaFrontier Science Center for Synthetic Biology and Key Laboratory of Systems Bioengineering (Ministry of Education), School of Chemical Engineering and Technology, Tianjin University, Tianjin, ChinaMannose-sensitive hemagglutinin (MSHA) pili and flagellum are critical for the surface attachment of Vibrio cholerae, the first step of V. cholerae colonization on host surfaces. However, the cell landing mechanism remains largely unknown, particularly in viscoelastic environments such as the mucus layers of intestines. Here, combining the cysteine-substitution-based labeling method with single-cell tracking techniques, we quantitatively characterized the landing of V. cholerae by directly observing both pili and flagellum of cells in a viscoelastic non-Newtonian solution consisting of 2% Luria-Bertani and 1% methylcellulose (LB+MC). The results show that MSHA pili are evenly distributed along the cell length and can stick to surfaces at any point along the filament. With such properties, MSHA pili are observed to act as a brake and anchor during cell landing which includes three phases: running, lingering, and attaching. Importantly, loss of MSHA pili results in a more dramatic increase in mean path length in LB+MC than in 2% LB only or in 20% Ficoll solutions, indicating that the role of MSHA pili during cell landing is more apparent in viscoelastic non-Newtonian fluids than viscous Newtonian ones. Our work provides a detailed picture of the landing dynamics of V. cholerae under viscoelastic conditions, which can provide insights into ways to better control V. cholerae infections in a real mucus-like environment.https://elifesciences.org/articles/60655Vibrio choleraeMSHA pilussurface landingmotility
collection DOAJ
language English
format Article
sources DOAJ
author Wenchao Zhang
Mei Luo
Chunying Feng
Huaqing Liu
Hong Zhang
Rachel R Bennett
Andrew S Utada
Zhi Liu
Kun Zhao
spellingShingle Wenchao Zhang
Mei Luo
Chunying Feng
Huaqing Liu
Hong Zhang
Rachel R Bennett
Andrew S Utada
Zhi Liu
Kun Zhao
Crash landing of Vibrio cholerae by MSHA pili-assisted braking and anchoring in a viscoelastic environment
eLife
Vibrio cholerae
MSHA pilus
surface landing
motility
author_facet Wenchao Zhang
Mei Luo
Chunying Feng
Huaqing Liu
Hong Zhang
Rachel R Bennett
Andrew S Utada
Zhi Liu
Kun Zhao
author_sort Wenchao Zhang
title Crash landing of Vibrio cholerae by MSHA pili-assisted braking and anchoring in a viscoelastic environment
title_short Crash landing of Vibrio cholerae by MSHA pili-assisted braking and anchoring in a viscoelastic environment
title_full Crash landing of Vibrio cholerae by MSHA pili-assisted braking and anchoring in a viscoelastic environment
title_fullStr Crash landing of Vibrio cholerae by MSHA pili-assisted braking and anchoring in a viscoelastic environment
title_full_unstemmed Crash landing of Vibrio cholerae by MSHA pili-assisted braking and anchoring in a viscoelastic environment
title_sort crash landing of vibrio cholerae by msha pili-assisted braking and anchoring in a viscoelastic environment
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2021-07-01
description Mannose-sensitive hemagglutinin (MSHA) pili and flagellum are critical for the surface attachment of Vibrio cholerae, the first step of V. cholerae colonization on host surfaces. However, the cell landing mechanism remains largely unknown, particularly in viscoelastic environments such as the mucus layers of intestines. Here, combining the cysteine-substitution-based labeling method with single-cell tracking techniques, we quantitatively characterized the landing of V. cholerae by directly observing both pili and flagellum of cells in a viscoelastic non-Newtonian solution consisting of 2% Luria-Bertani and 1% methylcellulose (LB+MC). The results show that MSHA pili are evenly distributed along the cell length and can stick to surfaces at any point along the filament. With such properties, MSHA pili are observed to act as a brake and anchor during cell landing which includes three phases: running, lingering, and attaching. Importantly, loss of MSHA pili results in a more dramatic increase in mean path length in LB+MC than in 2% LB only or in 20% Ficoll solutions, indicating that the role of MSHA pili during cell landing is more apparent in viscoelastic non-Newtonian fluids than viscous Newtonian ones. Our work provides a detailed picture of the landing dynamics of V. cholerae under viscoelastic conditions, which can provide insights into ways to better control V. cholerae infections in a real mucus-like environment.
topic Vibrio cholerae
MSHA pilus
surface landing
motility
url https://elifesciences.org/articles/60655
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