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      Type VI secretion systems in plant‐associated bacteria

      review-article
      1 , , 2 , 1
      Environmental Microbiology
      John Wiley and Sons Inc.

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          Summary

          The type VI secretion system (T6SS) is a bacterial nanomachine used to inject effectors into prokaryotic or eukaryotic cells and is thus involved in both host manipulation and interbacterial competition. The T6SS is widespread among Gram‐negative bacteria, mostly within the Proteobacterium Phylum. This secretion system is commonly found in commensal and pathogenic plant‐associated bacteria. Phylogenetic analysis of phytobacterial T6SS clusters shows that they are distributed in the five main clades previously described (group 1–5). The even distribution of the system among commensal and pathogenic phytobacteria suggests that the T6SS provides fitness and colonization advantages in planta and that the role of the T6SS is not restricted to virulence. This manuscript reviews the phylogeny and biological roles of the T6SS in plant‐associated bacteria, highlighting a remarkable diversity both in terms of mechanism and function.

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          Most cited references54

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          Diverse type VI secretion phospholipases are functionally plastic antibacterial effectors

          Membranes allow the compartmentalization of biochemical processes and are therefore fundamental to life. The conservation of the cellular membrane, combined with its accessibility to secreted proteins, has made it a common target of factors mediating antagonistic interactions between diverse organisms. Here we report the discovery of a diverse superfamily of bacterial phospholipase enzymes. Within this superfamily, we defined enzymes with phospholipase A1 (PLA1) and A2 (PLA2) activity, which are common in host cell-targeting bacterial toxins and the venoms of certain insects and reptiles 1,2 . However, we find that the fundamental role of the superfamily is to mediate antagonistic bacterial interactions as effectors of the type VI secretion system (T6SS) translocation apparatus; accordingly, we name these proteins type VI lipase effectors (Tle). Our analyses indicate that PldA of Pseudomonas aeruginosa, a eukaryotic-like phospholipase D (PLD) 3 , is a member of the Tle superfamily and the founding substrate of the haemolysin co-regulated protein secretion island II T6SS (H2-T6SS). While prior studies have specifically implicated PldA and the H2-T6SS in pathogenesis 3–5 , we uncovered a specific role for the effector and its secretory machinery in intra- and inter-species bacterial interactions. Furthermore we find that this effector achieves its antibacterial activity by degrading phosphatidylethanolamine (PE), the major component of bacterial membranes. The surprising finding that virulence-associated phospholipases can serve as specific antibacterial effectors suggests that interbacterial interactions are a relevant factor driving the ongoing evolution of pathogenesis.
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            A type VI secretion-related pathway in Bacteroidetes mediates interbacterial antagonism.

            Bacteroidetes are a phylum of Gram-negative bacteria abundant in mammalian-associated polymicrobial communities, where they impact digestion, immunity, and resistance to infection. Despite the extensive competition at high cell density that occurs in these settings, cell contact-dependent mechanisms of interbacterial antagonism, such as the type VI secretion system (T6SS), have not been defined in this group of organisms. Herein we report the bioinformatic and functional characterization of a T6SS-like pathway in diverse Bacteroidetes. Using prominent human gut commensal and soil-associated species, we demonstrate that these systems localize dynamically within the cell, export antibacterial proteins, and target competitor bacteria. The Bacteroidetes system is a distinct pathway with marked differences in gene content and high evolutionary divergence from the canonical T6S pathway. Our findings offer a potential molecular explanation for the abundance of Bacteroidetes in polymicrobial environments, the observed stability of Bacteroidetes in healthy humans, and the barrier presented by the microbiota against pathogens.
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              Pyoverdine siderophores: from biogenesis to biosignificance.

              Pyoverdines are a group of structurally related siderophores produced by fluorescent Pseudomonas species. Recent genomic and biochemical data have shed new light on the complex molecular steps of pyoverdine biogenesis and explained the chemical diversity of these compounds. In the opportunistic pathogen Pseudomonas aeruginosa, pyoverdine is necessary for infection in several different disease models. The occurrence of pyoverdine-defective strains in chronic infections of patients with cystic fibrosis and the extremely high sequence diversity of genes involved in pyoverdine synthesis and uptake indicate that pyoverdine production is subject to high evolutionary pressure. Pyoverdine-dependent iron transport is also crucial for biofilm development, further expanding the importance of these siderophores in Pseudomonas biology.
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                Author and article information

                Contributors
                p.bernal@imperial.ac.uk
                Journal
                Environ Microbiol
                Environ. Microbiol
                10.1111/(ISSN)1462-2920
                EMI
                Environmental Microbiology
                John Wiley and Sons Inc. (Hoboken )
                1462-2912
                1462-2920
                10 November 2017
                January 2018
                : 20
                : 1 , Thematic Issue: Life of Microbes in rhizosphere ( doiID: 10.1111/emi.2018.20.issue-1 )
                : 1-15
                Affiliations
                [ 1 ] Department of Life Sciences, MRC Centre for Molecular Bacteriology and Infection, Flowers Building, 1st floor South Kensington Campus Imperial College London London SW7 2AZ UK
                [ 2 ] Department of Environmental Protection Estación Experimental del Zaidín‐Consejo Superior de Investigaciones Científicas 18008 Granada Spain
                Author notes
                [*] [* ]For correspondence. E‐mail p.bernal@ 123456imperial.ac.uk ; Tel. +44 (0)20 7594 3071; Fax ‐44 (0)20 7594 3069.
                Author information
                http://orcid.org/0000-0002-6228-0496
                http://orcid.org/0000-0002-9499-0492
                Article
                EMI13956
                10.1111/1462-2920.13956
                5813230
                29027348
                46e4860f-51d8-4cd7-bb09-49f277cfb564
                © 2017 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd

                This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 26 August 2017
                : 02 October 2017
                : 05 October 2017
                Page count
                Figures: 4, Tables: 1, Pages: 15, Words: 9817
                Funding
                Funded by: European Union through a Marie Curie Individual Fellowship
                Award ID: 654135 ‐ BIOCONT6SS
                Funded by: Spanish Ministry of Economy through a Ramon&Cajal
                Award ID: RYC2011‐08874
                Funded by: BBSRC
                Award ID: BB/N002539/1
                Categories
                Minireview
                Minireviews
                Custom metadata
                2.0
                emi13956
                January 2018
                Converter:WILEY_ML3GV2_TO_NLMPMC version:version=5.3.2.2 mode:remove_FC converted:15.02.2018

                Microbiology & Virology
                Microbiology & Virology

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