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      Water surface tension modulates the swarming mechanics of Bacillus subtilis

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          Abstract

          Many Bacillus subtilis strains swarm, often forming colonies with tendrils on agar medium. It is known that B. subtilis swarming requires flagella and a biosurfactant, surfactin. In this study, we find that water surface tension plays a role in swarming dynamics. B. subtilis colonies were found to contain water, and when a low amount of surfactin is produced, the water surface tension of the colony restricts expansion, causing bacterial density to rise. The increased density induces a quorum sensing response that leads to heightened production of surfactin, which then weakens water surface tension to allow colony expansion. When the barrier formed by water surface tension is breached at a specific location, a stream of bacteria swarms out of the colony to form a tendril. If a B. subtilis strain produces surfactin at levels that can substantially weaken the overall water surface tension of the colony, water floods the agar surface in a thin layer, within which bacteria swarm and migrate rapidly. This study sheds light on the role of water surface tension in regulating B. subtilis swarming, and provides insight into the mechanisms underlying swarming initiation and tendril formation.

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          Most cited references34

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          Swarming motility in undomesticated Bacillus subtilis.

          Swarming motility was identified and characterized in an undomesticated strain of Bacillus subtilis. Rapid surface migration was preceded by a cell density-dependent lag period, which could be eliminated if actively swarming cells were used as the inoculum. The leading edge of the swarm was characterized by multicellular rafts of highly flagellated cells. Flagellum biosynthesis and surfactant production were required for swarming. Swarming was not found in any of several standard laboratory strains. Laboratory strains are characteristically unable to produce surfactant, but such a strain remained unable to swarm even when surfactant was provided by extracellular complementation. We conclude that robust swarming is a feature of undomesticated B. subtilis and that this behaviour has been lost or attenuated in laboratory strains through the accumulation of multiple genetic defects.
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            Biochemical and genetic characterization of a competence pheromone from B. subtilis.

            We have purified and characterized a modified peptide pheromone that accumulates in culture medium as B. subtilis grows to high density. This pheromone is required for the development of genetic competence. When added to cells at low density, the pheromone induces the premature development of competence. The peptide moiety of the pheromone matches nine of the last ten amino acids predicted from a 55 codon open reading frame, comX. comX and comQ, the gene immediately upstream of comX, are required for production of the pheromone. Response to the pheromone requires the comP-comA two-component regulatory system and the oligopeptide permease encoded by spo0K. Spo0K could transport the pheromone into the cell, or function as a receptor, binding the pheromone and sending a transmembrane signal, leading to activation of the ComA transcription factor and induction of competence development.
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              Genes governing swarming in Bacillus subtilis and evidence for a phase variation mechanism controlling surface motility.

              Undomesticated strains of Bacillus subtilis, but not laboratory strains, exhibit robust swarming motility on solid surfaces. The failure of laboratory strains to swarm is caused by a mutation in a gene (sfp) needed for surfactin synthesis and a mutation(s) in an additional unknown gene(s). Insertional mutagenesis of the undomesticated 3610 strain with the transposon mini-Tn10 was carried out to discover genes needed for swarming but not swimming motility. Four such newly identified swarming genes are reported, three of which (swrA, swrB, and efp) had not been previously characterized and one of which (swrC) was known to play a role in resistance to the antibacterial effect of surfactin. Laboratory strains were found to harbour a frameshift mutation in the swrA gene. When corrected for the swrA mutation, as well as the mutation in sfp, laboratory strains regained the capacity to swarm and did so as robustly as the wild strain. The swrA mutation was an insertion of an A:T base pair in a homopolymeric stretch of eight A:T base pairs, and readily reverted to the wild type. These findings suggest that the swrA insertion and its reversion take place by slipped-strand mispairing during DNA replication and that swarming motility is subject to phase variation.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                24 September 2015
                2015
                : 6
                : 1017
                Affiliations
                [1] 1Department of Microbiology and Immunology, Chang Gung University Taoyuan, Taiwan
                [2] 2Research Center for Bacterial Pathogenesis, Chang Gung University Taoyuan, Taiwan
                [3] 3Graduate School of Biotechnology and Bioengineering, Yuan Ze University Taoyuan, Taiwan
                [4] 4Department of Medical Biotechnology and Laboratory Science Proteomic Center, College of Medicine, Chang Gung University Taoyuan, Taiwan
                [5] 5Department of Medical Research and Development, Chang Gung Memorial Hospital Chiayi Branch Chiayi, Taiwan
                Author notes

                Edited by: Akos T. Kovacs, Friedrich Schiller University of Jena, Germany

                Reviewed by: Moshe Shemesh, Agricultural Research Organization, Israel; Diego Francisco Romero, University of Malaga, Spain

                *Correspondence: Shih-Tung Liu, Department of Microbiology and Immunology, Chang Gung University, 259, Wen-Hwa 1st Road, Kwei-Shan, Taoyuan 333, Taiwan cgliu@ 123456mail.cgu.edu.tw

                This article was submitted to Microbial Physiology and Metabolism, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2015.01017
                4616241
                26557106
                f96213b3-1bc2-4320-88e8-ca77ae388e2a
                Copyright © 2015 Ke, Hsueh, Cheng, Wu and Liu.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 24 June 2015
                : 08 September 2015
                Page count
                Figures: 8, Tables: 3, Equations: 0, References: 38, Pages: 12, Words: 8975
                Categories
                Microbiology
                Original Research

                Microbiology & Virology
                bacillus subtilis,swarming,water surface tension,surfactin,quorum sensing
                Microbiology & Virology
                bacillus subtilis, swarming, water surface tension, surfactin, quorum sensing

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