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      Type IVB Secretion Systems of Legionella and Other Gram-Negative Bacteria

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          Abstract

          Type IV secretion systems (T4SSs) play a central role in the pathogenicity of many important pathogens, including Agrobacterium tumefaciens, Helicobacter pylori, and Legionella pneumophila. The T4SSs are related to bacterial conjugation systems, and are classified into two subgroups, type IVA (T4ASS) and type IVB (T4BSS). The T4BSS, which is closely related to conjugation systems of IncI plasmids, was originally found in human pathogen L. pneumophila; pathogenesis by L. pneumophila infection requires functional Dot/Icm T4BSS. A zoonotic pathogen, Coxiella burnetii, and an arthropod pathogen, Rickettsiella grylli – both of which carry T4BSSs highly similar to the Legionella Dot/Icm system – are evolutionarily closely related and comprise a monophyletic group. A growing body of bacterial genomic information now suggests that T4BSSs are not limited to Legionella and related bacteria and IncI plasmids. Here, we review the current knowledge on T4BSS apparatus and component proteins, gained mainly from studies on L. pneumophila Dot/Icm T4BSS. Recent structural studies, along with previous findings, suggest that the Dot/Icm T4BSS contains components with primary or higher-order structures similar to those in other types of secretion systems – types II, III, IVA, and VI, thus highlighting the mosaic nature of T4BSS architecture.

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          Biological diversity of prokaryotic type IV secretion systems.

          Type IV secretion systems (T4SS) translocate DNA and protein substrates across prokaryotic cell envelopes generally by a mechanism requiring direct contact with a target cell. Three types of T4SS have been described: (i) conjugation systems, operationally defined as machines that translocate DNA substrates intercellularly by a contact-dependent process; (ii) effector translocator systems, functioning to deliver proteins or other macromolecules to eukaryotic target cells; and (iii) DNA release/uptake systems, which translocate DNA to or from the extracellular milieu. Studies of a few paradigmatic systems, notably the conjugation systems of plasmids F, R388, RP4, and pKM101 and the Agrobacterium tumefaciens VirB/VirD4 system, have supplied important insights into the structure, function, and mechanism of action of type IV secretion machines. Information on these systems is updated, with emphasis on recent exciting structural advances. An underappreciated feature of T4SS, most notably of the conjugation subfamily, is that they are widely distributed among many species of gram-negative and -positive bacteria, wall-less bacteria, and the Archaea. Conjugation-mediated lateral gene transfer has shaped the genomes of most if not all prokaryotes over evolutionary time and also contributed in the short term to the dissemination of antibiotic resistance and other virulence traits among medically important pathogens. How have these machines adapted to function across envelopes of distantly related microorganisms? A survey of T4SS functioning in phylogenetically diverse species highlights the biological complexity of these translocation systems and identifies common mechanistic themes as well as novel adaptations for specialized purposes relating to the modulation of the donor-target cell interaction.
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            Modulation of host cell function by Legionella pneumophila type IV effectors.

            Macrophages and protozoa ingest bacteria by phagocytosis and destroy these microbes using a conserved pathway that mediates fusion of the phagosome with lysosomes. To survive within phagocytic host cells, bacterial pathogens have evolved a variety of strategies to avoid fusion with lysosomes. A virulence strategy used by the intracellular pathogen Legionella pneumophila is to manipulate host cellular processes using bacterial proteins that are delivered into the cytosolic compartment of the host cell by a specialized secretion system called Dot/Icm. The proteins delivered by the Dot/Icm system target host factors that play evolutionarily conserved roles in controlling membrane transport in eukaryotic cells, which enables L. pneumophila to create an endoplasmic reticulum-like vacuole that supports intracellular replication in both protozoan and mammalian host cells. This review focuses on intracellular trafficking of L. pneumophila and describes how bacterial proteins contribute to modulation of host processes required for survival within host cells.
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              Ankyrin repeat proteins comprise a diverse family of bacterial type IV effectors.

              Specialized secretion systems are used by many bacteria to deliver effector proteins into host cells that can either mimic or disrupt the function of eukaryotic factors. We found that the intracellular pathogens Legionella pneumophila and Coxiella burnetii use a type IV secretion system to deliver into eukaryotic cells a large number of different bacterial proteins containing ankyrin repeat homology domains called Anks. The L. pneumophila AnkX protein prevented microtubule-dependent vesicular transport to interfere with fusion of the L. pneumophila-containing vacuole with late endosomes after infection of macrophages, which demonstrates that Ank proteins have effector functions important for bacterial infection of eukaryotic host cells.
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                Author and article information

                Journal
                Front Microbiol
                Front. Microbio.
                Frontiers in Microbiology
                Frontiers Research Foundation
                1664-302X
                04 March 2011
                27 June 2011
                2011
                : 2
                : 136
                Affiliations
                [1] 1simpleResearch Institute for Microbial Diseases, Osaka University Osaka, Japan
                [2] 2simpleGraduate School of Frontier Biosciences, Osaka University Osaka, Japan
                Author notes

                Edited by: Carmen Buchrieser, Pasteur Institute, France

                Reviewed by: Christoph Dehio, Biozentrum University of Basel, Switzerland; Rémi Fronzes, CNRS/Pasteur Institute, France

                *Correspondence: Hiroki Nagai, Research Institute for Microbial Diseases, Osaka University, 3-1 Yamadaoka, Suita, Osaka 565-0871, Japan. e-mail: hnagai@ 123456biken.osaka-u.ac.jp

                This article was submitted to Frontiers in Cellular and Infection Microbiology, a specialty of Frontiers in Microbiology.

                Article
                10.3389/fmicb.2011.00136
                3127085
                21743810
                e940770d-ef35-4f90-8fdc-37f8d12e1cdb
                Copyright © 2011 Nagai and Kubori.

                This is an open-access article subject to a non-exclusive license between the authors and Frontiers Media SA, which permits use, distribution and reproduction in other forums, provided the original authors and source are credited and other Frontiers conditions are complied with.

                History
                : 15 January 2011
                : 11 June 2011
                Page count
                Figures: 5, Tables: 0, Equations: 0, References: 111, Pages: 12, Words: 10586
                Categories
                Microbiology
                Review Article

                Microbiology & Virology
                coxiella,rickettsiella,protein secretion,conjugation,legionella,type iv secretion,dot/icm,type ivb secretion

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