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      Proteinaceous determinants of surface colonization in bacteria: bacterial adhesion and biofilm formation from a protein secretion perspective

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          Abstract

          Bacterial colonization of biotic or abiotic surfaces results from two quite distinct physiological processes, namely bacterial adhesion and biofilm formation. Broadly speaking, a biofilm is defined as the sessile development of microbial cells. Biofilm formation arises following bacterial adhesion but not all single bacterial cells adhering reversibly or irreversibly engage inexorably into a sessile mode of growth. Among molecular determinants promoting bacterial colonization, surface proteins are the most functionally diverse active components. To be present on the bacterial cell surface, though, a protein must be secreted in the first place. Considering the close association of secreted proteins with their cognate secretion systems, the secretome (which refers both to the secretion systems and their protein substrates) is a key concept to apprehend the protein secretion and related physiological functions. The protein secretion systems are here considered in light of the differences in the cell-envelope architecture between diderm-LPS (archetypal Gram-negative), monoderm (archetypal Gram-positive) and diderm-mycolate (archetypal acid-fast) bacteria. Besides, their cognate secreted proteins engaged in the bacterial colonization process are regarded from single protein to supramolecular protein structure as well as the non-classical protein secretion. This state-of-the-art on the complement of the secretome (the secretion systems and their cognate effectors) involved in the surface colonization process in diderm-LPS and monoderm bacteria paves the way for future research directions in the field.

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          Most cited references361

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          The Pfam protein families database.

          Pfam is a large collection of protein families and domains. Over the past 2 years the number of families in Pfam has doubled and now stands at 6190 (version 10.0). Methodology improvements for searching the Pfam collection locally as well as via the web are described. Other recent innovations include modelling of discontinuous domains allowing Pfam domain definitions to be closer to those found in structure databases. Pfam is available on the web in the UK (http://www.sanger.ac.uk/Software/Pfam/), the USA (http://pfam.wustl.edu/), France (http://pfam.jouy.inra.fr/) and Sweden (http://Pfam.cgb.ki.se/).
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            Genetic analysis of Escherichia coli biofilm formation: roles of flagella, motility, chemotaxis and type I pili.

            We have used Escherichia coli as a model system to investigate the initiation of biofilm formation. Here, we demonstrate that E. coli forms biofilms on multiple abiotic surfaces in a nutrient-dependent fashion. In addition, we have isolated insertion mutations that render this organism defective in biofilm formation. One-half of these mutations was found to perturb normal flagellar function. Using defined fli, flh, mot and che alleles, we show that motility, but not chemotaxis, is critical for normal biofilm formation. Microscopic analyses of these mutants suggest that motility is important for both initial interaction with the surface and for movement along the surface. In addition, we present evidence that type I pili (harbouring the mannose-specific adhesin, FimH) are required for initial surface attachment and that mannose inhibits normal attachment. In light of the observations presented here, a working model is discussed that describes the roles of both motility and type I pili in biofilm development.
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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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                Author and article information

                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                14 October 2013
                2013
                : 4
                : 303
                Affiliations
                [1] 1UR454 Microbiologie, INRA Saint-Genès Champanelle, France
                [2] 2UR370 Qualité des Produits Animaux, INRA Saint-Genès Champanelle, France
                Author notes

                Edited by: Biswarup Mukhopadhyay, Virginia Bioinformatics Institute, USA

                Reviewed by: Dirk Linke, Max Planck Society, Germany; Karl G. Wooldridge, University of Nottingham, UK

                *Correspondence: Mickaël Desvaux, UR454 Microbiology, INRA Clermont-Ferrand Research Centre, Site of Theix, F-63122 Saint-Genès Champanelle, France e-mail: mickael.desvaux@ 123456clermont.inra.fr

                This article was submitted to Microbial Physiology and Metabolism, a section of the journal Frontiers in Microbiology.

                †These authors have contributed equally to this work and share first authorship.

                Article
                10.3389/fmicb.2013.00303
                3796261
                24133488
                df6a9a80-d5ea-4fc5-9562-a3aeb2f46091
                Copyright © 2013 Chagnot, Zorgani, Astruc and Desvaux.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 18 July 2013
                : 22 September 2013
                Page count
                Figures: 4, Tables: 1, Equations: 0, References: 403, Pages: 26, Words: 24518
                Categories
                Microbiology
                Review Article

                Microbiology & Virology
                secretome,adhesin,pili/fimbriae/curli,cell surface,aggregation,secreted protein,mscramm,protein secretion system

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