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Vibrio cholerae use pili and flagella synergistically to effect motility switching and conditional surface attachment.

ABSTRACT: We show that Vibrio cholerae, the causative agent of cholera, use their flagella and mannose-sensitive hemagglutinin (MSHA) type IV pili synergistically to switch between two complementary motility states that together facilitate surface selection and attachment. Flagellar rotation counter-rotates the cell body, causing MSHA pili to have periodic mechanical contact with the surface for surface-skimming cells. Using tracking algorithms at 5?ms resolution we observe two motility behaviours: 'roaming', characterized by meandering trajectories, and 'orbiting', characterized by repetitive high-curvature orbits. We develop a hydrodynamic model showing that these phenotypes result from a nonlinear relationship between trajectory shape and frictional forces between pili and the surface: strong pili-surface interactions generate orbiting motion, increasing the local bacterial loiter time. Time-lapse imaging reveals how only orbiting mode cells can attach irreversibly and form microcolonies. These observations suggest that MSHA pili are crucial for surface selection, irreversible attachment, and ultimately microcolony formation.

SUBMITTER: Utada AS

PROVIDER: S-EPMC4420032 | biostudies-literature | 2014 Sep

REPOSITORIES: biostudies-literature

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Vibrio cholerae use pili and flagella synergistically to effect motility switching and conditional surface attachment.

Utada Andrew S AS Bennett Rachel R RR Fong Jiunn C N JCN Gibiansky Maxsim L ML Yildiz Fitnat H FH Golestanian Ramin R Wong Gerard C L GCL

Nature communications 20140919

We show that Vibrio cholerae, the causative agent of cholera, use their flagella and mannose-sensitive hemagglutinin (MSHA) type IV pili synergistically to switch between two complementary motility states that together facilitate surface selection and attachment. Flagellar rotation counter-rotates the cell body, causing MSHA pili to have periodic mechanical contact with the surface for surface-skimming cells. Using tracking algorithms at 5 ms resolution we observe two motility behaviours: 'roami ...[more]

PMID: 25234699

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Project description:Understanding the survival strategies of pandemic cholera pathogens in aquatic environments is important for preventing their dissemination. Here, we report a phenomenon wherein long-term cultivation of Vibrio cholerae under nutrient-limited condition (M9 minimal medium supplemented with 0.2% glucose) causes mutations in flagella-related genes, thus inhibiting motility. Moreover, the motility defect reduced the transition of the viable but nonculturable state of the organisms. Maintenance of proliferative capability allows for the rapid population growth and prolonged survival in environments with nutrient sources. Diverse flagella-related genes, including flrA, flrC, flrD, flhA, flhF, fliD, fliF, fliG, fliH, fliI, fliP, fliQ, flgF, flgL, flgK, motX, and pomA, underwent mutations during the cultivation. However, only one gene (site) was mutated in a single V. cholerae. Longer cultivation for up to 300 days yielded further mutations in metabolism-related genes and the loss of virulence factors (e.g., CTX phage) and large DNA regions (~35 kb). These mutations were detected in most organisms of V. cholerae, accompanying the loss of genomic integrity. Motility-defective variants with mutations in the acetate kinase gene had become predominant in culturable cells after long-term cultivation in independently replicated experiments. These findings shed light on a survival mechanism in which V. cholerae adapts to an environmental niche by accumulating mutations. IMPORTANCE Vibrio cholerae undergoes a transition to a viable but non-culturable (VNC) state when subjected to various environmental stresses. We showed here that flagellar motility was involved in the development of the VNC state of V. cholerae. In this study, motility-defective isolates with mutations in various flagella-related genes, but not motile isolates, were predominantly obtained under the stress of long-term batch culture. Other genomic regions were highly conserved, suggesting that the mutations were selective. During the stationary phase of long-term culture, V. cholerae isolates with mutations in the acetate kinase and flagella-related genes were predominant. This study suggests that genes involved in specific functions in V. cholerae undergo mutations under certain environmental conditions.

Project description:Cholera disease is caused by Vibrio cholerae infecting the lining of the small intestine and results in severe diarrhea. V. cholerae's swimming motility is known to play a crucial role in pathogenicity and may aid the bacteria in crossing the intestinal mucus barrier to reach sites of infection, but the exact mechanisms are unknown. The cell can be either pushed or pulled by its single polar flagellum, but there is no consensus on the resulting repertoire of motility behaviors. We use high-throughput three-dimensional (3D) bacterial tracking to observe V. cholerae swimming in buffer, in viscous solutions of the synthetic polymer PVP, and in mucin solutions that may mimic the host environment. We perform a statistical characterization of its motility behavior on the basis of large 3D trajectory data sets. We find that V. cholerae performs asymmetric run-reverse-flick motility, consisting of a sequence of a forward run, reversal, and a shorter backward run, followed by a turn by approximately 90°, called a flick, preceding the next forward run. Unlike many run-reverse-flick swimmers, V. cholerae's backward runs are much shorter than its forward runs, resulting in an increased effective diffusivity. We also find that the swimming speed is not constant but subject to frequent decreases. The turning frequency in mucin matches that observed in buffer. Run-reverse-flick motility and speed fluctuations are present in all environments studied, suggesting that these behaviors also occur in natural aquatic habitats as well as the host environment. IMPORTANCE Cholera disease produces vomiting and severe diarrhea and causes approximately 100,000 deaths per year worldwide. The disease is caused by the bacterium Vibrio cholerae colonizing the lining of the small intestine. V. cholerae's ability to swim is known to increase its infectivity, but the underlying mechanisms are not known. One possibility is that swimming aids in crossing the protective mucus barrier that covers the lining of the small intestine. Our work characterizing how V. cholerae swims in environments that mimic properties of the host environment may advance the understanding of how motility contributes to infection.

Dataset Information

Vibrio cholerae use pili and flagella synergistically to effect motility switching and conditional surface attachment.

Publications

Vibrio cholerae use pili and flagella synergistically to effect motility switching and conditional surface attachment.

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