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      Spatial arrangement of several flagellins within bacterial flagella improves motility in different environments

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          Abstract

          Bacterial flagella are helical proteinaceous fibers, composed of the protein flagellin, that confer motility to many bacterial species. The genomes of about half of all flagellated species include more than one flagellin gene, for reasons mostly unknown. Here we show that two flagellins (FlaA and FlaB) are spatially arranged in the polar flagellum of Shewanella putrefaciens, with FlaA being more abundant close to the motor and FlaB in the remainder of the flagellar filament. Observations of swimming trajectories and numerical simulations demonstrate that this segmentation improves motility in a range of environmental conditions, compared to mutants with single-flagellin filaments. In particular, it facilitates screw-like motility, which enhances cellular spreading through obstructed environments. Similar mechanisms may apply to other bacterial species and may explain the maintenance of multiple flagellins to form the flagellar filament.

          Abstract

          It is unclear why many bacteria have more than one gene encoding flagellin, the protein that makes up flagella. Here, the authors show that a particular arrangement of two different flagellins in the polar flagellum of Shewanella putrefaciens facilitates screw-like motility through obstructed environments.

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          Coordinating assembly of a bacterial macromolecular machine.

          The assembly of large and complex organelles, such as the bacterial flagellum, poses the formidable problem of coupling temporal gene expression to specific stages of the organelle-assembly process. The discovery that levels of the bacterial flagellar regulatory protein FlgM are controlled by its secretion from the cell in response to the completion of an intermediate flagellar structure (the hook-basal body) was only the first of several discoveries of unique mechanisms that coordinate flagellar gene expression with assembly. In this Review, we discuss this mechanism, together with others that also coordinate gene regulation and flagellar assembly in Gram-negative bacteria.
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            Flagellar Hydrodynamics

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              Complete atomic model of the bacterial flagellar filament by electron cryomicroscopy.

              The bacterial flagellar filament is a helical propeller for bacterial locomotion. It is a helical assembly of a single protein, flagellin, and its tubular structure is formed by 11 protofilaments in two distinct conformations, L- and R-type, for supercoiling. The X-ray crystal structure of a flagellin fragment lacking about 100 terminal residues revealed the protofilament structure, but the full filament structure is still essential for understanding the mechanism of supercoiling and polymerization. Here we report a complete atomic model of the R-type filament by electron cryomicroscopy. A density map obtained from image data up to 4 A resolution shows the feature of alpha-helical backbone and some large side chains. The atomic model built on the map reveals intricate molecular packing and an alpha-helical coiled coil formed by the terminal chains in the inner core of the filament, with its intersubunit hydrophobic interactions having an important role in stabilizing the filament.
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                Author and article information

                Contributors
                laurence.wilson@york.ac.uk
                bruno.eckhardt@physik.uni-marburg.de
                kai.thormann@mikro.bio.uni-giessen.de
                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group UK (London )
                2041-1723
                18 December 2018
                18 December 2018
                2018
                : 9
                : 5369
                Affiliations
                [1 ]ISNI 0000 0001 2165 8627, GRID grid.8664.c, Institut für Mikrobiologie und Molekularbiologie, Justus-Liebig-Universität Gießen, ; 35392 Gießen, Germany
                [2 ]ISNI 0000 0004 1936 9756, GRID grid.10253.35, Fachbereich Physik und LOEWE Zentrum für Synthetische Mikrobiologie, Philipps-Universität Marburg, ; 35032 Marburg, Germany
                [3 ]ISNI 0000 0004 1936 9668, GRID grid.5685.e, Department of Physics, , University of York, Heslington, ; York, YO10 5DD UK
                [4 ]ISNI 0000 0004 1936 9668, GRID grid.5685.e, Department of Mathematics, , University of York, Heslington, ; York, YO10 5DD UK
                Author information
                http://orcid.org/0000-0001-6659-6001
                Article
                7802
                10.1038/s41467-018-07802-w
                6299084
                30560868
                f9bd2ccd-1af1-472d-9b40-6d95cb787e18
                © The Author(s) 2018

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 19 February 2018
                : 22 November 2018
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