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      Protein Secretion Systems in Pseudomonas aeruginosa: An Essay on Diversity, Evolution, and Function

      review-article
      1
      Frontiers in Microbiology
      Frontiers Research Foundation
      cell envelope, nanomachine, macromolecular complex, channel, targeting

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          Abstract

          Protein secretion systems are molecular nanomachines used by Gram-negative bacteria to thrive within their environment. They are used to release enzymes that hydrolyze complex carbon sources into usable compounds, or to release proteins that capture essential ions such as iron. They are also used to colonize and survive within eukaryotic hosts, causing acute or chronic infections, subverting the host cell response and escaping the immune system. In this article, the opportunistic human pathogen Pseudomonas aeruginosa is used as a model to review the diversity of secretion systems that bacteria have evolved to achieve these goals. This diversity may result from a progressive transformation of cell envelope complexes that initially may not have been dedicated to secretion. The striking similarities between secretion systems and type IV pili, flagella, bacteriophage tail, or efflux pumps is a nice illustration of this evolution. Differences are also needed since various secretion configurations call for diversity. For example, some proteins are released in the extracellular medium while others are directly injected into the cytosol of eukaryotic cells. Some proteins are folded before being released and transit into the periplasm. Other proteins cross the whole cell envelope at once in an unfolded state. However, the secretion system requires conserved basic elements or features. For example, there is a need for an energy source or for an outer membrane channel. The structure of this review is thus quite unconventional. Instead of listing secretion types one after each other, it presents a melting pot of concepts indicating that secretion types are in constant evolution and use basic principles. In other words, emergence of new secretion systems could be predicted the way Mendeleïev had anticipated characteristics of yet unknown elements.

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          Most cited references229

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          Type IV pili and twitching motility.

          Twitching motility is a flagella-independent form of bacterial translocation over moist surfaces. It occurs by the extension, tethering, and then retraction of polar type IV pili, which operate in a manner similar to a grappling hook. Twitching motility is equivalent to social gliding motility in Myxococcus xanthus and is important in host colonization by a wide range of plant and animal pathogens, as well as in the formation of biofilms and fruiting bodies. The biogenesis and function of type IV pili is controlled by a large number of genes, almost 40 of which have been identified in Pseudomonas aeruginosa. A number of genes required for pili assembly are homologous to genes involved in type II protein secretion and competence for DNA uptake, suggesting that these systems share a common architecture. Twitching motility is also controlled by a range of signal transduction systems, including two-component sensor-regulators and a complex chemosensory system.
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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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              Bacterial invasion: the paradigms of enteroinvasive pathogens.

              Invasive bacteria actively induce their own uptake by phagocytosis in normally nonphagocytic cells and then either establish a protected niche within which they survive and replicate, or disseminate from cell to cell by means of an actin-based motility process. The mechanisms underlying bacterial entry, phagosome maturation, and dissemination reveal common strategies as well as unique tactics evolved by individual species to establish infection.
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                Author and article information

                Journal
                Front Microbiol
                Front. Microbio.
                Frontiers in Microbiology
                Frontiers Research Foundation
                1664-302X
                25 May 2011
                18 July 2011
                2011
                : 2
                : 155
                Affiliations
                [1] 1simpleDivision of Cell and Molecular Biology, Centre for Molecular Microbiology and Infection, Imperial College London London, UK
                Author notes

                Edited by: Dara Frank, Medical College of Wisconsin, USA

                Reviewed by: Maria Sandkvist, University of Michigan, USA; Katrina Forest, University of Wisconsin-Madison, USA

                *Correspondence: Alain Filloux, Division of Cell and Molecular Biology, Centre for Molecular Microbiology and Infection, Imperial College London, South Kensington Campus, Flowers Building, SW72AZ London, UK. e-mail: a.filloux@ 123456imperial.ac.uk

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

                Article
                10.3389/fmicb.2011.00155
                3140646
                21811488
                99abac91-31e8-4a98-915c-3d0e66d44746
                Copyright © 2011 Filloux.

                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
                : 26 April 2011
                : 01 July 2011
                Page count
                Figures: 7, Tables: 1, Equations: 0, References: 250, Pages: 21, Words: 20465
                Categories
                Microbiology
                Review Article

                Microbiology & Virology
                nanomachine,channel,macromolecular complex,targeting,cell envelope
                Microbiology & Virology
                nanomachine, channel, macromolecular complex, targeting, cell envelope

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