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      Prophage-triggered membrane vesicle formation through peptidoglycan damage in Bacillus subtilis

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          Abstract

          Bacteria release membrane vesicles (MVs) that play important roles in various biological processes. However, the mechanisms of MV formation in Gram-positive bacteria are unclear, as these cells possess a single cytoplasmic membrane that is surrounded by a thick cell wall. Here we use live cell imaging and electron cryo-tomography to describe a mechanism for MV formation in Bacillus subtilis. We show that the expression of a prophage-encoded endolysin in a sub-population of cells generates holes in the peptidoglycan cell wall. Through these openings, cytoplasmic membrane material protrudes into the extracellular space and is released as MVs. Due to the loss of membrane integrity, the induced cells eventually die. The vesicle-producing cells induce MV formation in neighboring cells by the enzymatic action of the released endolysin. Our results support the idea that endolysins may be important for MV formation in bacteria, and this mechanism may potentially be useful for the production of MVs for applications in biomedicine and nanotechnology.

          Abstract

          It is unclear how Gram-positive bacteria, with a thick cell wall, can release membrane vesicles. Here, Toyofuku et al. show that a prophage-encoded endolysin can generate holes in the cell wall through which cytoplasmic membrane material protrudes and is released as vesicles.

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          Most cited references 63

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          Fiji: an open-source platform for biological-image analysis.

          Fiji is a distribution of the popular open-source software ImageJ focused on biological-image analysis. Fiji uses modern software engineering practices to combine powerful software libraries with a broad range of scripting languages to enable rapid prototyping of image-processing algorithms. Fiji facilitates the transformation of new algorithms into ImageJ plugins that can be shared with end users through an integrated update system. We propose Fiji as a platform for productive collaboration between computer science and biology research communities.
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            Automated electron microscope tomography using robust prediction of specimen movements.

             D Mastronarde (2005)
            A new method was developed to acquire images automatically at a series of specimen tilts, as required for tomographic reconstruction. The method uses changes in specimen position at previous tilt angles to predict the position at the current tilt angle. Actual measurement of the position or focus is skipped if the statistical error of the prediction is low enough. This method allows a tilt series to be acquired rapidly when conditions are good but falls back toward the traditional approach of taking focusing and tracking images when necessary. The method has been implemented in a program, SerialEM, that provides an efficient environment for data acquisition. This program includes control of an energy filter as well as a low-dose imaging mode, in which tracking and focusing occur away from the area of interest. The program can automatically acquire a montage of overlapping frames, allowing tomography of areas larger than the field of the CCD camera. It also includes tools for navigating between specimen positions and finding regions of interest.
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              The complete genome sequence of the gram-positive bacterium Bacillus subtilis.

              Bacillus subtilis is the best-characterized member of the Gram-positive bacteria. Its genome of 4,214,810 base pairs comprises 4,100 protein-coding genes. Of these protein-coding genes, 53% are represented once, while a quarter of the genome corresponds to several gene families that have been greatly expanded by gene duplication, the largest family containing 77 putative ATP-binding transport proteins. In addition, a large proportion of the genetic capacity is devoted to the utilization of a variety of carbon sources, including many plant-derived molecules. The identification of five signal peptidase genes, as well as several genes for components of the secretion apparatus, is important given the capacity of Bacillus strains to secrete large amounts of industrially important enzymes. Many of the genes are involved in the synthesis of secondary metabolites, including antibiotics, that are more typically associated with Streptomyces species. The genome contains at least ten prophages or remnants of prophages, indicating that bacteriophage infection has played an important evolutionary role in horizontal gene transfer, in particular in the propagation of bacterial pathogenesis.
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                Author and article information

                Contributors
                toyofuku.masanori.gf@u.tsukuba.ac.jp
                pilhofer@biol.ethz.ch
                leberl@botinst.uzh.ch
                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group UK (London )
                2041-1723
                7 September 2017
                7 September 2017
                2017
                : 8
                Affiliations
                [1 ]ISNI 0000 0001 2369 4728, GRID grid.20515.33, Department of Life and Environmental Sciences, , University of Tsukuba, ; Tennoudai 1-1-1, Tsukuba, Ibaraki 305-8572 Japan
                [2 ]ISNI 0000 0004 1937 0650, GRID grid.7400.3, Department of Plant and Microbial Biology, , University of Zürich, ; Zollikerstrasse 107, Zürich, 8008 Switzerland
                [3 ]ISNI 0000 0001 2156 2780, GRID grid.5801.c, Department of Biology, , Institute of Molecular Biology and Biophysics, ; ETH Zürich, Otto-Stern-Weg 5, Zürich, 8093 Switzerland
                [4 ]ISNI 0000 0004 1937 0650, GRID grid.7400.3, Department of Chemistry, , University of Zürich, ; Winterthurerstrasse 190, Zürich, 8057 Switzerland
                [5 ]ISNI 0000 0001 2341 2786, GRID grid.116068.8, Present Address: Department of Biological Engineering, , Massachusetts Institute of Technology, ; Cambridge, MA 02139 USA
                Article
                492
                10.1038/s41467-017-00492-w
                5589764
                28883390
                © The Author(s) 2017

                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/.

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