The pel polysaccharide can serve a structural and protective role in the biofilm matrix of Pseudomonas aeruginosa
Bacterial extracellular polysaccharides are a key constituent of the extracellular matrix material of biofilms. Pseudomonas aeruginosa is a model organism for biofilm studies and produces three extracellular polysaccharides that have been implicated in biofilm development, alginate, Psl and Pel. Sig...
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| Published in | PLoS pathogens Vol. 7; no. 1; p. e1001264 |
|---|---|
| Main Authors | , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
01.01.2011
Public Library of Science (PLoS) |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Bacterial extracellular polysaccharides are a key constituent of the extracellular matrix material of biofilms. Pseudomonas aeruginosa is a model organism for biofilm studies and produces three extracellular polysaccharides that have been implicated in biofilm development, alginate, Psl and Pel. Significant work has been conducted on the roles of alginate and Psl in biofilm development, however we know little regarding Pel. In this study, we demonstrate that Pel can serve two functions in biofilms. Using a novel assay involving optical tweezers, we demonstrate that Pel is crucial for maintaining cell-to-cell interactions in a PA14 biofilm, serving as a primary structural scaffold for the community. Deletion of pelB resulted in a severe biofilm deficiency. Interestingly, this effect is strain-specific. Loss of Pel production in the laboratory strain PAO1 resulted in no difference in attachment or biofilm development; instead Psl proved to be the primary structural polysaccharide for biofilm maturity. Furthermore, we demonstrate that Pel plays a second role by enhancing resistance to aminoglycoside antibiotics. This protection occurs only in biofilm populations. We show that expression of the pel gene cluster and PelF protein levels are enhanced during biofilm growth compared to liquid cultures. Thus, we propose that Pel is capable of playing both a structural and a protective role in P. aeruginosa biofilms. |
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| AbstractList | Bacterial extracellular polysaccharides are a key constituent of the extracellular matrix material of biofilms. Pseudomonas aeruginosa is a model organism for biofilm studies and produces three extracellular polysaccharides that have been implicated in biofilm development, alginate, Psl and Pel. Significant work has been conducted on the roles of alginate and Psl in biofilm development, however we know little regarding Pel. In this study, we demonstrate that Pel can serve two functions in biofilms. Using a novel assay involving optical tweezers, we demonstrate that Pel is crucial for maintaining cell-to-cell interactions in a PA14 biofilm, serving as a primary structural scaffold for the community. Deletion of pelB resulted in a severe biofilm deficiency. Interestingly, this effect is strain-specific. Loss of Pel production in the laboratory strain PAO1 resulted in no difference in attachment or biofilm development; instead Psl proved to be the primary structural polysaccharide for biofilm maturity. Furthermore, we demonstrate that Pel plays a second role by enhancing resistance to aminoglycoside antibiotics. This protection occurs only in biofilm populations. We show that expression of the pel gene cluster and PelF protein levels are enhanced during biofilm growth compared to liquid cultures. Thus, we propose that Pel is capable of playing both a structural and a protective role in P. aeruginosa biofilms. Most bacteria live within biofilm communities, which are a complex population of microorganisms that attach to surfaces and produce copious amounts of extracellular matrix material. Exopolysaccharides are a key feature of the extracellular matrix and are found in many forms, ranging from structurally simple linear homopolymers to structurally complex branched heteropolymers. Exopolysaccharides carry out a wide range of functions involving adherence to surfaces and other cells, structural support and protection against host and environmental stress. The goal of our study was to examine the functional importance of polysaccharide production in the model biofilm organism, Pseudomonas aeruginosa. Using a deletion and over expression strategy, we characterized the function of one polysaccharide, Pel, and demonstrated that this polysaccharide has two roles, a structural role and a protective role, against an important class of antibiotics, aminioglycosides. Bacterial extracellular polysaccharides are a key constituent of the extracellular matrix material of biofilms. Pseudomonas aeruginosa is a model organism for biofilm studies and produces three extracellular polysaccharides that have been implicated in biofilm development, alginate, Psl and Pel. Significant work has been conducted on the roles of alginate and Psl in biofilm development, however we know little regarding Pel. In this study, we demonstrate that Pel can serve two functions in biofilms. Using a novel assay involving optical tweezers, we demonstrate that Pel is crucial for maintaining cell-to-cell interactions in a PA14 biofilm, serving as a primary structural scaffold for the community. Deletion of pelB resulted in a severe biofilm deficiency. Interestingly, this effect is strain-specific. Loss of Pel production in the laboratory strain PAO1 resulted in no difference in attachment or biofilm development; instead Psl proved to be the primary structural polysaccharide for biofilm maturity. Furthermore, we demonstrate that Pel plays a second role by enhancing resistance to aminoglycoside antibiotics. This protection occurs only in biofilm populations. We show that expression of the pel gene cluster and PelF protein levels are enhanced during biofilm growth compared to liquid cultures. Thus, we propose that Pel is capable of playing both a structural and a protective role in P. aeruginosa biofilms. Most bacteria live within biofilm communities, which are a complex population of microorganisms that attach to surfaces and produce copious amounts of extracellular matrix material. Exopolysaccharides are a key feature of the extracellular matrix and are found in many forms, ranging from structurally simple linear homopolymers to structurally complex branched heteropolymers. Exopolysaccharides carry out a wide range of functions involving adherence to surfaces and other cells, structural support and protection against host and environmental stress. The goal of our study was to examine the functional importance of polysaccharide production in the model biofilm organism, Pseudomonas aeruginosa . Using a deletion and over expression strategy, we characterized the function of one polysaccharide, Pel, and demonstrated that this polysaccharide has two roles, a structural role and a protective role, against an important class of antibiotics, aminioglycosides. Bacterial extracellular polysaccharides are a key constituent of the extracellular matrix material of biofilms. Pseudomonas aeruginosa is a model organism for biofilm studies and produces three extracellular polysaccharides that have been implicated in biofilm development, alginate, Psl and Pel. Significant work has been conducted on the roles of alginate and Psl in biofilm development, however we know little regarding Pel. In this study, we demonstrate that Pel can serve two functions in biofilms. Using a novel assay involving optical tweezers, we demonstrate that Pel is crucial for maintaining cell-to-cell interactions in a PA14 biofilm, serving as a primary structural scaffold for the community. Deletion of pelB resulted in a severe biofilm deficiency. Interestingly, this effect is strain-specific. Loss of Pel production in the laboratory strain PAO1 resulted in no difference in attachment or biofilm development; instead Psl proved to be the primary structural polysaccharide for biofilm maturity. Furthermore, we demonstrate that Pel plays a second role by enhancing resistance to aminoglycoside antibiotics. This protection occurs only in biofilm populations. We show that expression of the pel gene cluster and PelF protein levels are enhanced during biofilm growth compared to liquid cultures. Thus, we propose that Pel is capable of playing both a structural and a protective role in P. aeruginosa biofilms. Bacterial extracellular polysaccharides are a key constituent of the extracellular matrix material of biofilms. Pseudomonas aeruginosa is a model organism for biofilm studies and produces three extracellular polysaccharides that have been implicated in biofilm development, alginate, Psl and Pel. Significant work has been conducted on the roles of alginate and Psl in biofilm development, however we know little regarding Pel. In this study, we demonstrate that Pel can serve two functions in biofilms. Using a novel assay involving optical tweezers, we demonstrate that Pel is crucial for maintaining cell-to-cell interactions in a PA14 biofilm, serving as a primary structural scaffold for the community. Deletion of pelB resulted in a severe biofilm deficiency. Interestingly, this effect is strain-specific. Loss of Pel production in the laboratory strain PAO1 resulted in no difference in attachment or biofilm development; instead Psl proved to be the primary structural polysaccharide for biofilm maturity. Furthermore, we demonstrate that Pel plays a second role by enhancing resistance to aminoglycoside antibiotics. This protection occurs only in biofilm populations. We show that expression of the pel gene cluster and PelF protein levels are enhanced during biofilm growth compared to liquid cultures. Thus, we propose that Pel is capable of playing both a structural and a protective role in P. aeruginosa biofilms. |
| Audience | Academic |
| Author | Gordon, Vernita D Wong, Gerard C L Wozniak, Daniel J Borlee, Bradley R Parsek, Matthew R Murakami, Keiji Colvin, Kelly M |
| AuthorAffiliation | 3 Department of Microbiology, Ohio State University, Columbus, Ohio, United States of America Massachusetts General Hospital and Harvard Medical School, United States of America 4 Department of Bioengineering, University of California, Los Angeles, Los Angeles, California, United States of America 1 Department of Microbiology, University of Washington, Seattle, Washington, United States of America 2 Department of Physics, University of Texas, Austin, Austin, Texas, United States of America |
| AuthorAffiliation_xml | – name: 1 Department of Microbiology, University of Washington, Seattle, Washington, United States of America – name: 4 Department of Bioengineering, University of California, Los Angeles, Los Angeles, California, United States of America – name: 2 Department of Physics, University of Texas, Austin, Austin, Texas, United States of America – name: 3 Department of Microbiology, Ohio State University, Columbus, Ohio, United States of America – name: Massachusetts General Hospital and Harvard Medical School, United States of America |
| Author_xml | – sequence: 1 givenname: Kelly M surname: Colvin fullname: Colvin, Kelly M organization: Department of Microbiology, University of Washington, Seattle, Washington, United States of America – sequence: 2 givenname: Vernita D surname: Gordon fullname: Gordon, Vernita D – sequence: 3 givenname: Keiji surname: Murakami fullname: Murakami, Keiji – sequence: 4 givenname: Bradley R surname: Borlee fullname: Borlee, Bradley R – sequence: 5 givenname: Daniel J surname: Wozniak fullname: Wozniak, Daniel J – sequence: 6 givenname: Gerard C L surname: Wong fullname: Wong, Gerard C L – sequence: 7 givenname: Matthew R surname: Parsek fullname: Parsek, Matthew R |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/21298031$$D View this record in MEDLINE/PubMed |
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| Copyright | COPYRIGHT 2011 Public Library of Science 2011 Colvin et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Colvin KM, Gordon VD, Murakami K, Borlee BR, Wozniak DJ, et al. (2011) The Pel Polysaccharide Can Serve a Structural and Protective Role in the Biofilm Matrix of Pseudomonas aeruginosa. PLoS Pathog 7(1): e1001264. doi:10.1371/journal.ppat.1001264 Colvin et al. 2011 |
| Copyright_xml | – notice: COPYRIGHT 2011 Public Library of Science – notice: 2011 Colvin et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Colvin KM, Gordon VD, Murakami K, Borlee BR, Wozniak DJ, et al. (2011) The Pel Polysaccharide Can Serve a Structural and Protective Role in the Biofilm Matrix of Pseudomonas aeruginosa. PLoS Pathog 7(1): e1001264. doi:10.1371/journal.ppat.1001264 – notice: Colvin et al. 2011 |
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| SubjectTerms | Alginates Anti-Bacterial Agents - pharmacology Antimicrobial agents Bacterial Adhesion Bacterial Proteins - genetics Bacterial Proteins - metabolism Bacteriology Biofilms Biofilms - growth & development Experiments Extracellular Matrix - physiology Gene Expression Regulation, Bacterial Genetic aspects Microbial mats Microbial polysaccharides Microbial Sensitivity Tests Microbial Viability - drug effects Microbiology Microbiology/Medical Microbiology Microbiology/Microbial Growth and Development Operons Physiological aspects Polysaccharides, Bacterial - genetics Polysaccharides, Bacterial - metabolism Pseudomonas aeruginosa Pseudomonas aeruginosa - drug effects Pseudomonas aeruginosa - growth & development Pseudomonas aeruginosa - physiology Tobramycin - pharmacology |
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| Title | The pel polysaccharide can serve a structural and protective role in the biofilm matrix of Pseudomonas aeruginosa |
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