The Pel and Psl polysaccharides provide Pseudomonas aeruginosa structural redundancy within the biofilm matrix
Summary Extracellular polysaccharides comprise a major component of the biofilm matrix. Many species that are adept at biofilm formation have the capacity to produce multiple types of polysaccharides. Pseudomonas aeruginosa produces at least three extracellular polysaccharides, alginate, Pel and Psl...
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Published in | Environmental microbiology Vol. 14; no. 8; pp. 1913 - 1928 |
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Main Authors | , , , , , , , , |
Format | Journal Article |
Language | English |
Published |
Oxford, UK
Blackwell Publishing Ltd
01.08.2012
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Subjects | |
Online Access | Get full text |
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Abstract | Summary
Extracellular polysaccharides comprise a major component of the biofilm matrix. Many species that are adept at biofilm formation have the capacity to produce multiple types of polysaccharides. Pseudomonas aeruginosa produces at least three extracellular polysaccharides, alginate, Pel and Psl, that have been implicated in biofilm development. Non‐mucoid strains can use either Pel or Psl as the primary matrix structural polysaccharide. In this study, we evaluated a range of clinical and environmental P. aeruginosa isolates for their dependence on Pel and Psl for biofilm development. Mutational analysis demonstrates that Psl plays an important role in surface attachment for most isolates. However, there was significant strain‐to‐strain variability in the contribution of Pel and Psl to mature biofilm structure. This analysis led us to propose four classes of strains based upon their Pel and Psl functional and expression profiles. Our data also suggest that Pel and Psl can serve redundant functions as structural scaffolds in mature biofilms. We propose that redundancy could help preserve the capacity to produce a biofilm when exopolysaccharide genes are subjected to mutation. To test this, we used PAO1, a common lab strain that primarily utilizes Psl in the matrix. As expected, a psl mutant strain initially produced a poor biofilm. After extended cultivation, we demonstrate that this strain acquired mutations that upregulated expression of the Pel polysaccharide, demonstrating the utility of having a redundant scaffold exopolysaccharide. Collectively, our studies revealed both unique and redundant roles for two distinct biofilm exopolysaccharides. |
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AbstractList | Extracellular polysaccharides comprise a major component of the biofilm matrix. Many species that are adept at biofilm formation have the capacity to produce multiple types of polysaccharides.
Pseudomonas aeruginosa
produces at least three extracellular polysaccharides, alginate, Pel and Psl, that have been implicated in biofilm development. Non‐mucoid strains can use either Pel or Psl as the primary matrix structural polysaccharide. In this study, we evaluated a range of clinical and environmental
P. aeruginosa
isolates for their dependence on Pel and Psl for biofilm development. Mutational analysis demonstrates that Psl plays an important role in surface attachment for most isolates. However, there was significant strain‐to‐strain variability in the contribution of Pel and Psl to mature biofilm structure. This analysis led us to propose four classes of strains based upon their Pel and Psl functional and expression profiles. Our data also suggest that Pel and Psl can serve redundant functions as structural scaffolds in mature biofilms. We propose that redundancy could help preserve the capacity to produce a biofilm when exopolysaccharide genes are subjected to mutation. To test this, we used PAO1, a common lab strain that primarily utilizes Psl in the matrix. As expected, a
psl
mutant strain initially produced a poor biofilm. After extended cultivation, we demonstrate that this strain acquired mutations that upregulated expression of the Pel polysaccharide, demonstrating the utility of having a redundant scaffold exopolysaccharide. Collectively, our studies revealed both unique and redundant roles for two distinct biofilm exopolysaccharides. Extracellular polysaccharides comprise a major component of the biofilm matrix. Many species that are adept at biofilm formation have the capacity to produce multiple types of polysaccharides. Pseudomonas aeruginosa produces at least three extracellular polysaccharides, alginate, Pel and Psl, that have been implicated in biofilm development. Non-mucoid strains can use either Pel or Psl as the primary matrix structural polysaccharide. In this study, we evaluated a range of clinical and environmental P. aeruginosa isolates for their dependence on Pel and Psl for biofilm development. Mutational analysis demonstrates that Psl plays an important role in surface attachment for most isolates. However, there was significant strain-to-strain variability in the contribution of Pel and Psl to mature biofilm structure. This analysis led us to propose four classes of strains based upon their Pel and Psl functional and expression profiles. Our data also suggest that Pel and Psl can serve a redundant function as a structural scaffold in mature biofilms. We propose that redundancy could help preserve the capacity to produce a biofilm when exopolysaccharide genes are subjected to mutation. To test this we used PAO1, a common lab strain that primarily utilizes Psl in the matrix. As expected, a psl mutant strain initially produced a poor biofilm. After extended cultivation, we demonstrate that this strain acquired mutations that up-regulated expression of the Pel polysaccharide, demonstrating the utility of having a redundant scaffold exopolysaccharide. Collectively, our studies revealed both unique and functionally redundant roles for two distinct biofilm exopolysaccharides. Summary Extracellular polysaccharides comprise a major component of the biofilm matrix. Many species that are adept at biofilm formation have the capacity to produce multiple types of polysaccharides. Pseudomonas aeruginosa produces at least three extracellular polysaccharides, alginate, Pel and Psl, that have been implicated in biofilm development. Non‐mucoid strains can use either Pel or Psl as the primary matrix structural polysaccharide. In this study, we evaluated a range of clinical and environmental P. aeruginosa isolates for their dependence on Pel and Psl for biofilm development. Mutational analysis demonstrates that Psl plays an important role in surface attachment for most isolates. However, there was significant strain‐to‐strain variability in the contribution of Pel and Psl to mature biofilm structure. This analysis led us to propose four classes of strains based upon their Pel and Psl functional and expression profiles. Our data also suggest that Pel and Psl can serve redundant functions as structural scaffolds in mature biofilms. We propose that redundancy could help preserve the capacity to produce a biofilm when exopolysaccharide genes are subjected to mutation. To test this, we used PAO1, a common lab strain that primarily utilizes Psl in the matrix. As expected, a psl mutant strain initially produced a poor biofilm. After extended cultivation, we demonstrate that this strain acquired mutations that upregulated expression of the Pel polysaccharide, demonstrating the utility of having a redundant scaffold exopolysaccharide. Collectively, our studies revealed both unique and redundant roles for two distinct biofilm exopolysaccharides. Extracellular polysaccharides comprise a major component of the biofilm matrix. Many species that are adept at biofilm formation have the capacity to produce multiple types of polysaccharides. Pseudomonas aeruginosa produces at least three extracellular polysaccharides, alginate, Pel and Psl, that have been implicated in biofilm development. Non-mucoid strains can use either Pel or Psl as the primary matrix structural polysaccharide. In this study, we evaluated a range of clinical and environmental P.aeruginosa isolates for their dependence on Pel and Psl for biofilm development. Mutational analysis demonstrates that Psl plays an important role in surface attachment for most isolates. However, there was significant strain-to-strain variability in the contribution of Pel and Psl to mature biofilm structure. This analysis led us to propose four classes of strains based upon their Pel and Psl functional and expression profiles. Our data also suggest that Pel and Psl can serve redundant functions as structural scaffolds in mature biofilms. We propose that redundancy could help preserve the capacity to produce a biofilm when exopolysaccharide genes are subjected to mutation. To test this, we used PAO1, a common lab strain that primarily utilizes Psl in the matrix. As expected, a psl mutant strain initially produced a poor biofilm. After extended cultivation, we demonstrate that this strain acquired mutations that upregulated expression of the Pel polysaccharide, demonstrating the utility of having a redundant scaffold exopolysaccharide. Collectively, our studies revealed both unique and redundant roles for two distinct biofilm exopolysaccharides. |
Author | Tart, Catherine S. Wozniak, Daniel J. Howell, P. Lynne Ryder, Cynthia Urbano, Rodolfo Colvin, Kelly M. Irie, Yasuhiko Whitney, John C. Parsek, Matthew R. |
AuthorAffiliation | 4 Departments of Medicine (Infectious Disease) and Microbiology, Center for Microbial Interface Biology, Ohio State University, 484 W. 12 th Ave, Columbus, OH 43210 3 Department of Biochemistry, University of Toronto, 1 Kings College Circle, Toronto, ON, M5S 1A8 1 Department of Microbiology, University of Washington, 1959 NE Pacific St, Box number 357242, Seattle, WA 98195 2 Program in Molecular Structure & Function, Hospital for Sick Children, 555 University Ave, Toronto, Ontario MSG 1X8, Canada |
AuthorAffiliation_xml | – name: 1 Department of Microbiology, University of Washington, 1959 NE Pacific St, Box number 357242, Seattle, WA 98195 – name: 2 Program in Molecular Structure & Function, Hospital for Sick Children, 555 University Ave, Toronto, Ontario MSG 1X8, Canada – name: 3 Department of Biochemistry, University of Toronto, 1 Kings College Circle, Toronto, ON, M5S 1A8 – name: 4 Departments of Medicine (Infectious Disease) and Microbiology, Center for Microbial Interface Biology, Ohio State University, 484 W. 12 th Ave, Columbus, OH 43210 |
Author_xml | – sequence: 1 givenname: Kelly M. surname: Colvin fullname: Colvin, Kelly M. organization: Department of Microbiology, University of Washington, 1959 NE Pacific St, Box number 357242, Seattle, WA 98195, USA – sequence: 2 givenname: Yasuhiko surname: Irie fullname: Irie, Yasuhiko organization: Department of Microbiology, University of Washington, 1959 NE Pacific St, Box number 357242, Seattle, WA 98195, USA – sequence: 3 givenname: Catherine S. surname: Tart fullname: Tart, Catherine S. organization: Department of Microbiology, University of Washington, 1959 NE Pacific St, Box number 357242, Seattle, WA 98195, USA – sequence: 4 givenname: Rodolfo surname: Urbano fullname: Urbano, Rodolfo organization: Department of Microbiology, University of Washington, 1959 NE Pacific St, Box number 357242, Seattle, WA 98195, USA – sequence: 5 givenname: John C. surname: Whitney fullname: Whitney, John C. organization: Program in Molecular Structure & Function, Hospital for Sick Children, 555 University Ave, Toronto, ON, MSG 1X8, Canada – sequence: 6 givenname: Cynthia surname: Ryder fullname: Ryder, Cynthia organization: Department of Biology, Lincoln Memorial University, 206 Farr-Chinnock Hall, Harrogate, TN 37752, USA – sequence: 7 givenname: P. Lynne surname: Howell fullname: Howell, P. Lynne organization: Program in Molecular Structure & Function, Hospital for Sick Children, 555 University Ave, Toronto, ON, MSG 1X8, Canada – sequence: 8 givenname: Daniel J. surname: Wozniak fullname: Wozniak, Daniel J. organization: Departments of Medicine (Infectious Disease) and Microbiology, Center for Microbial Interface Biology, Ohio State University, 484 W. 12th Ave, Columbus, OH 43210, USA – sequence: 9 givenname: Matthew R. surname: Parsek fullname: Parsek, Matthew R. email: parsem@u.washington.edu organization: Department of Microbiology, University of Washington, 1959 NE Pacific St, Box number 357242, Seattle, WA 98195, USA |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/22176658$$D View this record in MEDLINE/PubMed |
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Extracellular polysaccharides comprise a major component of the biofilm matrix. Many species that are adept at biofilm formation have the capacity to... Extracellular polysaccharides comprise a major component of the biofilm matrix. Many species that are adept at biofilm formation have the capacity to produce... |
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SubjectTerms | Biofilms Gene Expression Profiling Gene Expression Regulation, Bacterial Mutation Polysaccharides, Bacterial - biosynthesis Polysaccharides, Bacterial - chemistry Polysaccharides, Bacterial - genetics Pseudomonas aeruginosa Pseudomonas aeruginosa - genetics Pseudomonas aeruginosa - isolation & purification Pseudomonas aeruginosa - metabolism Pseudomonas aeruginosa - physiology Species Specificity |
Title | The Pel and Psl polysaccharides provide Pseudomonas aeruginosa structural redundancy within the biofilm matrix |
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