Literature DB >> 23175784

Self-produced exopolysaccharide is a signal that stimulates biofilm formation in Pseudomonas aeruginosa.

Yasuhiko Irie1, Bradley R Borlee, Jennifer R O'Connor, Preston J Hill, Caroline S Harwood, Daniel J Wozniak, Matthew R Parsek.   

Abstract

Bacteria have a tendency to attach to surfaces and grow as structured communities called biofilms. Chronic biofilm infections are a problem because they tend to resist antibiotic treatment and are difficult to eradicate. Bacterial biofilms have an extracellular matrix that is usually composed of a mixture of polysaccharides, proteins, and nucleic acids. This matrix has long been assumed to play a passive structural and protective role for resident biofilm cells. Here we show that this view is an oversimplification and that the biofilm matrix can play an active role in stimulating its own synthesis. Working with the model biofilm bacterium Pseudomonas aeruginosa, we found that Psl, a major biofilm matrix polysaccharide for this species, acts as a signal to stimulate two diguanylate cyclases, SiaD and SadC, to produce the intracellular secondary messenger molecule c-di-GMP. Elevated intracellular concentrations of c-di-GMP then lead to the increased production of Psl and other components of the biofilm. This mechanism represents a unique positive feedback regulatory circuit, where the expression of an extracellular polysaccharide promotes biofilm growth in a manner analogous to autocrine signaling in eukaryotes.

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Year:  2012        PMID: 23175784      PMCID: PMC3528562          DOI: 10.1073/pnas.1217993109

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  30 in total

Review 1.  The biofilm matrix--an immobilized but dynamic microbial environment.

Authors:  I W Sutherland
Journal:  Trends Microbiol       Date:  2001-05       Impact factor: 17.079

2.  Cell-cell signaling in Xanthomonas campestris involves an HD-GYP domain protein that functions in cyclic di-GMP turnover.

Authors:  Robert P Ryan; Yvonne Fouhy; Jean F Lucey; Lisa C Crossman; Stephen Spiro; Ya-Wen He; Lian-Hui Zhang; Stephan Heeb; Miguel Cámara; Paul Williams; J Maxwell Dow
Journal:  Proc Natl Acad Sci U S A       Date:  2006-04-12       Impact factor: 11.205

Review 3.  c-di-GMP-mediated regulation of virulence and biofilm formation.

Authors:  Peggy A Cotter; Scott Stibitz
Journal:  Curr Opin Microbiol       Date:  2007-01-08       Impact factor: 7.934

4.  A chemosensory system that regulates biofilm formation through modulation of cyclic diguanylate levels.

Authors:  Jason W Hickman; Delia F Tifrea; Caroline S Harwood
Journal:  Proc Natl Acad Sci U S A       Date:  2005-09-26       Impact factor: 11.205

5.  Analysis of Pseudomonas aeruginosa conditional psl variants reveals roles for the psl polysaccharide in adhesion and maintaining biofilm structure postattachment.

Authors:  Luyan Ma; Kara D Jackson; Rebecca M Landry; Matthew R Parsek; Daniel J Wozniak
Journal:  J Bacteriol       Date:  2006-09-15       Impact factor: 3.490

6.  Subcellular location characteristics of the Pseudomonas aeruginosa GGDEF protein, WspR, indicate that it produces cyclic-di-GMP in response to growth on surfaces.

Authors:  Zehra Tüzün Güvener; Caroline S Harwood
Journal:  Mol Microbiol       Date:  2007-11-19       Impact factor: 3.501

7.  SadC reciprocally influences biofilm formation and swarming motility via modulation of exopolysaccharide production and flagellar function.

Authors:  Judith H Merritt; Kimberly M Brothers; Sherry L Kuchma; George A O'Toole
Journal:  J Bacteriol       Date:  2007-06-22       Impact factor: 3.490

8.  Analysis of Pseudomonas aeruginosa diguanylate cyclases and phosphodiesterases reveals a role for bis-(3'-5')-cyclic-GMP in virulence.

Authors:  Hemantha Kulasakara; Vincent Lee; Anja Brencic; Nicole Liberati; Jonathan Urbach; Sachiko Miyata; Daniel G Lee; Alice N Neely; Mamoru Hyodo; Yoshihiro Hayakawa; Frederick M Ausubel; Stephen Lory
Journal:  Proc Natl Acad Sci U S A       Date:  2006-02-13       Impact factor: 11.205

9.  Surface sensing and lateral subcellular localization of WspA, the receptor in a chemosensory-like system leading to c-di-GMP production.

Authors:  Jennifer R O'Connor; Nathan J Kuwada; Varisa Huangyutitham; Paul A Wiggins; Caroline S Harwood
Journal:  Mol Microbiol       Date:  2012-09-07       Impact factor: 3.501

10.  A cyclic-di-GMP receptor required for bacterial exopolysaccharide production.

Authors:  Vincent T Lee; Jody M Matewish; Jennifer L Kessler; Mamoru Hyodo; Yoshihiro Hayakawa; Stephen Lory
Journal:  Mol Microbiol       Date:  2007-09       Impact factor: 3.501

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  110 in total

Review 1.  Innate Immune Signaling Activated by MDR Bacteria in the Airway.

Authors:  Dane Parker; Danielle Ahn; Taylor Cohen; Alice Prince
Journal:  Physiol Rev       Date:  2016-01       Impact factor: 37.312

2.  Elevated levels of the second messenger c-di-GMP contribute to antimicrobial resistance of Pseudomonas aeruginosa.

Authors:  Kajal Gupta; Julie Liao; Olga E Petrova; K E Cherny; Karin Sauer
Journal:  Mol Microbiol       Date:  2014-04-09       Impact factor: 3.501

3.  Deletion mutant library for investigation of functional outputs of cyclic diguanylate metabolism in Pseudomonas aeruginosa PA14.

Authors:  Dae-Gon Ha; Megan E Richman; George A O'Toole
Journal:  Appl Environ Microbiol       Date:  2014-03-21       Impact factor: 4.792

4.  The Matrix Reloaded: Probing the Extracellular Matrix Synchronizes Bacterial Communities.

Authors:  Nitai Steinberg; Ilana Kolodkin-Gal
Journal:  J Bacteriol       Date:  2015-03-30       Impact factor: 3.490

Review 5.  Virulence attenuating combination therapy: a potential multi-target synergy approach to treat Pseudomonas aeruginosa infections in cystic fibrosis patients.

Authors:  Elana Shaw; William M Wuest
Journal:  RSC Med Chem       Date:  2020-02-19

6.  Role of psl Genes in Antibiotic Tolerance of Adherent Pseudomonas aeruginosa.

Authors:  Keiji Murakami; Tsuneko Ono; Darija Viducic; Yoko Somiya; Reiko Kariyama; Kenji Hori; Takashi Amoh; Katsuhiko Hirota; Hiromi Kumon; Matthew R Parsek; Yoichiro Miyake
Journal:  Antimicrob Agents Chemother       Date:  2017-06-27       Impact factor: 5.191

7.  A Survival Strategy for Pseudomonas aeruginosa That Uses Exopolysaccharides To Sequester and Store Iron To Stimulate Psl-Dependent Biofilm Formation.

Authors:  Shan Yu; Qing Wei; Tianhu Zhao; Yuan Guo; Luyan Z Ma
Journal:  Appl Environ Microbiol       Date:  2016-10-14       Impact factor: 4.792

8.  Structural Basis for Translocation of a Biofilm-supporting Exopolysaccharide across the Bacterial Outer Membrane.

Authors:  Yan Wang; Archana Andole Pannuri; Dongchun Ni; Haizhen Zhou; Xiou Cao; Xiaomei Lu; Tony Romeo; Yihua Huang
Journal:  J Biol Chem       Date:  2016-03-08       Impact factor: 5.157

9.  The SiaA/B/C/D signaling network regulates biofilm formation in Pseudomonas aeruginosa.

Authors:  Gukui Chen; Jianhua Gan; Chun Yang; Yili Zuo; Juan Peng; Meng Li; Weiping Huo; Yingpeng Xie; Yani Zhang; Tietao Wang; Xin Deng; Haihua Liang
Journal:  EMBO J       Date:  2020-02-24       Impact factor: 11.598

10.  PslG, a self-produced glycosyl hydrolase, triggers biofilm disassembly by disrupting exopolysaccharide matrix.

Authors:  Shan Yu; Tiantian Su; Huijun Wu; Shiheng Liu; Di Wang; Tianhu Zhao; Zengjun Jin; Wenbin Du; Mei-Jun Zhu; Song Lin Chua; Liang Yang; Deyu Zhu; Lichuan Gu; Luyan Z Ma
Journal:  Cell Res       Date:  2015-11-27       Impact factor: 25.617

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