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Regulation of biofilm formation by BpfA, BpfD, and BpfG in Shewanella oneidensis

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Frontiers in Microbiology

Frontiers Media S.A.

biofilm, bpfA bpfG, bpfD, regulation mechanism, S. oneidensis

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      Abstract

      Bacteria switch between two distinct life styles – planktonic (free living) and biofilm forming – in keeping with their ever-changing environment. Such switch involves sophisticated signaling and tight regulation, which provides a fascinating portal for studying gene function and orchestrated protein interactions. In this work, we investigated the molecular mechanism underlying biofilm formation in Shewanella oneidensis MR-1, an environmentally important model bacterium renowned for respiratory diversities, and uncovered a gene cluster coding for seven proteins involved in this process. The three key proteins, BpfA, BpfG, and BpfD, were studied in detail for the first time. BpfA directly participates in biofilm formation as extracellular “glue” BpfG is not only indispensable for BpfA export during biofilm forming but also functions to turn BpfA into active form for biofilm dispersing. BpfD regulates biofilm development by interacting with both BpfA and BpfG, likely in response to signal molecule c-di-GMP. In addition, we found that 1:1 stoichiometry between BpfD and BpfG is critical for biofilm formation. Furthermore, we demonstrated that a biofilm over-producing phenotype can be induced by C116S mutation but not loss of BpfG.

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      Most cited references 45

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      Bacterial biofilms: from the natural environment to infectious diseases.

      Biofilms--matrix-enclosed microbial accretions that adhere to biological or non-biological surfaces--represent a significant and incompletely understood mode of growth for bacteria. Biofilm formation appears early in the fossil record (approximately 3.25 billion years ago) and is common throughout a diverse range of organisms in both the Archaea and Bacteria lineages, including the 'living fossils' in the most deeply dividing branches of the phylogenetic tree. It is evident that biofilm formation is an ancient and integral component of the prokaryotic life cycle, and is a key factor for survival in diverse environments. Recent advances show that biofilms are structurally complex, dynamic systems with attributes of both primordial multicellular organisms and multifaceted ecosystems. Biofilm formation represents a protected mode of growth that allows cells to survive in hostile environments and also disperse to colonize new niches. The implications of these survival and propagative mechanisms in the context of both the natural environment and infectious diseases are discussed in this review.
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        The biofilm matrix.

        The microorganisms in biofilms live in a self-produced matrix of hydrated extracellular polymeric substances (EPS) that form their immediate environment. EPS are mainly polysaccharides, proteins, nucleic acids and lipids; they provide the mechanical stability of biofilms, mediate their adhesion to surfaces and form a cohesive, three-dimensional polymer network that interconnects and transiently immobilizes biofilm cells. In addition, the biofilm matrix acts as an external digestive system by keeping extracellular enzymes close to the cells, enabling them to metabolize dissolved, colloidal and solid biopolymers. Here we describe the functions, properties and constituents of the EPS matrix that make biofilms the most successful forms of life on earth.
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          SMART: recent updates, new developments and status in 2015

          SMART (Simple Modular Architecture Research Tool) is a web resource (http://smart.embl.de/) providing simple identification and extensive annotation of protein domains and the exploration of protein domain architectures. In the current version, SMART contains manually curated models for more than 1200 protein domains, with ∼200 new models since our last update article. The underlying protein databases were synchronized with UniProt, Ensembl and STRING, bringing the total number of annotated domains and other protein features above 100 million. SMART's ‘Genomic’ mode, which annotates proteins from completely sequenced genomes was greatly expanded and now includes 2031 species, compared to 1133 in the previous release. SMART analysis results pages have been completely redesigned and include links to several new information sources. A new, vector-based display engine has been developed for protein schematics in SMART, which can also be exported as high-resolution bitmap images for easy inclusion into other documents. Taxonomic tree displays in SMART have been significantly improved, and can be easily navigated using the integrated search engine.
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            Author and article information

            Affiliations
            Institute of Microbiology, College of Life Sciences, Zijingang Campus, Zhejiang University Hangzhou, China
            Author notes

            Edited by: Biswarup Mukhopadhyay, Virginia Tech, USA

            Reviewed by: Kenneth Nealson, University of Southern California, USA; Atsushi Kouzuma, Tokyo University of Pharmacy and Life Sciences, Japan

            *Correspondence: Jie Yuan and Haichun Gao, Institute of Microbiology, College of Life Sciences, Zijingang Campus, Zhejiang University, Room 235, Hangzhou, Zhejiang 310058, China, jieyuan@ 123456zju.edu.cn ; haichung@ 123456zju.edu.cn

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

            Contributors
            Journal
            Front Microbiol
            Front Microbiol
            Front. Microbiol.
            Frontiers in Microbiology
            Frontiers Media S.A.
            1664-302X
            04 August 2015
            2015
            : 6
            4523816
            10.3389/fmicb.2015.00790
            Copyright © 2015 Zhou, Yuan and Gao.

            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.

            Counts
            Figures: 6, Tables: 1, Equations: 0, References: 45, Pages: 11, Words: 0
            Funding
            Funded by: National Natural Science Foundation of China
            Award ID: 31270097
            Award ID: 41476105
            Award ID: 31100600
            Funded by: Fundamental Research Funds for the Central Universities
            Award ID: 2014FZA6002
            Funded by: Ministry of Education Science and Technology Development Center
            Award ID: 20120541
            Categories
            Microbiology
            Original Research

            Microbiology & Virology

            s. oneidensis, regulation mechanism, bpfd, bpfa bpfg, biofilm

            Comments

            added an editorial note to Shewanella

            What biochemical mechanisms underlie the formation of Shewanella biofilms? Zhou et al provide initial information and offer a model for biofilm formation, dispersion and regulation thereof.

            2016-03-21 11:59 UTC
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