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Dynamic Remodeling of Microbial Biofilms by Functionally Distinct Exopolysaccharides
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| Zeitschriftentitel: | mBio |
|---|---|
| Personen und Körperschaften: | , , , , , , , |
| In: | mBio, 5, 2014, 4 |
| Format: | E-Article |
| Sprache: | Englisch |
| veröffentlicht: |
American Society for Microbiology
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| Schlagwörter: |
| author_facet |
Chew, Su Chuen Kundukad, Binu Seviour, Thomas van der Maarel, Johan R. C. Yang, Liang Rice, Scott A. Doyle, Patrick Kjelleberg, Staffan Chew, Su Chuen Kundukad, Binu Seviour, Thomas van der Maarel, Johan R. C. Yang, Liang Rice, Scott A. Doyle, Patrick Kjelleberg, Staffan |
|---|---|
| author |
Chew, Su Chuen Kundukad, Binu Seviour, Thomas van der Maarel, Johan R. C. Yang, Liang Rice, Scott A. Doyle, Patrick Kjelleberg, Staffan |
| spellingShingle |
Chew, Su Chuen Kundukad, Binu Seviour, Thomas van der Maarel, Johan R. C. Yang, Liang Rice, Scott A. Doyle, Patrick Kjelleberg, Staffan mBio Dynamic Remodeling of Microbial Biofilms by Functionally Distinct Exopolysaccharides Virology Microbiology |
| author_sort |
chew, su chuen |
| spelling |
Chew, Su Chuen Kundukad, Binu Seviour, Thomas van der Maarel, Johan R. C. Yang, Liang Rice, Scott A. Doyle, Patrick Kjelleberg, Staffan 2161-2129 2150-7511 American Society for Microbiology Virology Microbiology http://dx.doi.org/10.1128/mbio.01536-14 <jats:title>ABSTRACT</jats:title> <jats:p> Biofilms are densely populated communities of microbial cells protected and held together by a matrix of extracellular polymeric substances. The structure and rheological properties of the matrix at the microscale influence the retention and transport of molecules and cells in the biofilm, thereby dictating population and community behavior. Despite its importance, quantitative descriptions of the matrix microstructure and microrheology are limited. Here, particle-tracking microrheology in combination with genetic approaches was used to spatially and temporally study the rheological contributions of the major exopolysaccharides Pel and Psl in <jats:named-content content-type="genus-species">Pseudomonas aeruginosa</jats:named-content> biofilms. Psl increased the elasticity and effective cross-linking within the matrix, which strengthened its scaffold and appeared to facilitate the formation of microcolonies. Conversely, Pel reduced effective cross-linking within the matrix. Without Psl, the matrix becomes more viscous, which facilitates biofilm spreading. The wild-type biofilm decreased in effective cross-linking over time, which would be advantageous for the spreading and colonization of new surfaces. This suggests that there are regulatory mechanisms to control production of the exopolysaccharides that serve to remodel the matrix of developing biofilms. The exopolysaccharides were also found to have profound effects on the spatial organization and integration of <jats:named-content content-type="genus-species">P. aeruginosa</jats:named-content> in a mixed-species biofilm model of <jats:italic>P. aeruginosa</jats:italic> - <jats:named-content content-type="genus-species">Staphylococcus aureus</jats:named-content> . Pel was required for close association of the two species in mixed-species microcolonies. In contrast, Psl was important for <jats:named-content content-type="genus-species">P. aeruginosa</jats:named-content> to form single-species biofilms on top of <jats:named-content content-type="genus-species">S. aureus</jats:named-content> biofilms. Our results demonstrate that Pel and Psl have distinct physical properties and functional roles during biofilm formation. </jats:p> <jats:p> <jats:bold>IMPORTANCE</jats:bold> Most bacteria grow as biofilms in the environment or in association with eukaryotic hosts. Removal of biofilms that form on surfaces is a challenge in clinical and industrial settings. One of the defining features of a biofilm is its extracellular matrix. The matrix has a heterogeneous structure and is formed from a secretion of various biopolymers, including proteins, extracellular DNA, and polysaccharides. It is generally known to interact with biofilm cells, thus affecting cell physiology and cell-cell communication. Despite the fact that the matrix may comprise up to 90% of the biofilm dry weight, how the matrix properties affect biofilm structure, maturation, and interspecies interactions remain largely unexplored. This study reveals that bacteria can use specific extracellular polymers to modulate the physical properties of their microenvironment. This in turn impacts biofilm structure, differentiation, and interspecies interactions. </jats:p> Dynamic Remodeling of Microbial Biofilms by Functionally Distinct Exopolysaccharides mBio |
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10.1128/mbio.01536-14 |
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Medizin Biologie |
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American Society for Microbiology, 2014 |
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American Society for Microbiology, 2014 |
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2161-2129 2150-7511 |
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2161-2129 2150-7511 |
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2014 |
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American Society for Microbiology |
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| title |
Dynamic Remodeling of Microbial Biofilms by Functionally Distinct Exopolysaccharides |
| title_unstemmed |
Dynamic Remodeling of Microbial Biofilms by Functionally Distinct Exopolysaccharides |
| title_full |
Dynamic Remodeling of Microbial Biofilms by Functionally Distinct Exopolysaccharides |
| title_fullStr |
Dynamic Remodeling of Microbial Biofilms by Functionally Distinct Exopolysaccharides |
| title_full_unstemmed |
Dynamic Remodeling of Microbial Biofilms by Functionally Distinct Exopolysaccharides |
| title_short |
Dynamic Remodeling of Microbial Biofilms by Functionally Distinct Exopolysaccharides |
| title_sort |
dynamic remodeling of microbial biofilms by functionally distinct exopolysaccharides |
| topic |
Virology Microbiology |
| url |
http://dx.doi.org/10.1128/mbio.01536-14 |
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2014 |
| physical |
|
| description |
<jats:title>ABSTRACT</jats:title>
<jats:p>
Biofilms are densely populated communities of microbial cells protected and held together by a matrix of extracellular polymeric substances. The structure and rheological properties of the matrix at the microscale influence the retention and transport of molecules and cells in the biofilm, thereby dictating population and community behavior. Despite its importance, quantitative descriptions of the matrix microstructure and microrheology are limited. Here, particle-tracking microrheology in combination with genetic approaches was used to spatially and temporally study the rheological contributions of the major exopolysaccharides Pel and Psl in
<jats:named-content content-type="genus-species">Pseudomonas aeruginosa</jats:named-content>
biofilms. Psl increased the elasticity and effective cross-linking within the matrix, which strengthened its scaffold and appeared to facilitate the formation of microcolonies. Conversely, Pel reduced effective cross-linking within the matrix. Without Psl, the matrix becomes more viscous, which facilitates biofilm spreading. The wild-type biofilm decreased in effective cross-linking over time, which would be advantageous for the spreading and colonization of new surfaces. This suggests that there are regulatory mechanisms to control production of the exopolysaccharides that serve to remodel the matrix of developing biofilms. The exopolysaccharides were also found to have profound effects on the spatial organization and integration of
<jats:named-content content-type="genus-species">P. aeruginosa</jats:named-content>
in a mixed-species biofilm model of
<jats:italic>P. aeruginosa</jats:italic>
-
<jats:named-content content-type="genus-species">Staphylococcus aureus</jats:named-content>
. Pel was required for close association of the two species in mixed-species microcolonies. In contrast, Psl was important for
<jats:named-content content-type="genus-species">P. aeruginosa</jats:named-content>
to form single-species biofilms on top of
<jats:named-content content-type="genus-species">S. aureus</jats:named-content>
biofilms. Our results demonstrate that Pel and Psl have distinct physical properties and functional roles during biofilm formation.
</jats:p>
<jats:p>
<jats:bold>IMPORTANCE</jats:bold>
Most bacteria grow as biofilms in the environment or in association with eukaryotic hosts. Removal of biofilms that form on surfaces is a challenge in clinical and industrial settings. One of the defining features of a biofilm is its extracellular matrix. The matrix has a heterogeneous structure and is formed from a secretion of various biopolymers, including proteins, extracellular DNA, and polysaccharides. It is generally known to interact with biofilm cells, thus affecting cell physiology and cell-cell communication. Despite the fact that the matrix may comprise up to 90% of the biofilm dry weight, how the matrix properties affect biofilm structure, maturation, and interspecies interactions remain largely unexplored. This study reveals that bacteria can use specific extracellular polymers to modulate the physical properties of their microenvironment. This in turn impacts biofilm structure, differentiation, and interspecies interactions.
</jats:p> |
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| author | Chew, Su Chuen, Kundukad, Binu, Seviour, Thomas, van der Maarel, Johan R. C., Yang, Liang, Rice, Scott A., Doyle, Patrick, Kjelleberg, Staffan |
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| description | <jats:title>ABSTRACT</jats:title> <jats:p> Biofilms are densely populated communities of microbial cells protected and held together by a matrix of extracellular polymeric substances. The structure and rheological properties of the matrix at the microscale influence the retention and transport of molecules and cells in the biofilm, thereby dictating population and community behavior. Despite its importance, quantitative descriptions of the matrix microstructure and microrheology are limited. Here, particle-tracking microrheology in combination with genetic approaches was used to spatially and temporally study the rheological contributions of the major exopolysaccharides Pel and Psl in <jats:named-content content-type="genus-species">Pseudomonas aeruginosa</jats:named-content> biofilms. Psl increased the elasticity and effective cross-linking within the matrix, which strengthened its scaffold and appeared to facilitate the formation of microcolonies. Conversely, Pel reduced effective cross-linking within the matrix. Without Psl, the matrix becomes more viscous, which facilitates biofilm spreading. The wild-type biofilm decreased in effective cross-linking over time, which would be advantageous for the spreading and colonization of new surfaces. This suggests that there are regulatory mechanisms to control production of the exopolysaccharides that serve to remodel the matrix of developing biofilms. The exopolysaccharides were also found to have profound effects on the spatial organization and integration of <jats:named-content content-type="genus-species">P. aeruginosa</jats:named-content> in a mixed-species biofilm model of <jats:italic>P. aeruginosa</jats:italic> - <jats:named-content content-type="genus-species">Staphylococcus aureus</jats:named-content> . Pel was required for close association of the two species in mixed-species microcolonies. In contrast, Psl was important for <jats:named-content content-type="genus-species">P. aeruginosa</jats:named-content> to form single-species biofilms on top of <jats:named-content content-type="genus-species">S. aureus</jats:named-content> biofilms. Our results demonstrate that Pel and Psl have distinct physical properties and functional roles during biofilm formation. </jats:p> <jats:p> <jats:bold>IMPORTANCE</jats:bold> Most bacteria grow as biofilms in the environment or in association with eukaryotic hosts. Removal of biofilms that form on surfaces is a challenge in clinical and industrial settings. One of the defining features of a biofilm is its extracellular matrix. The matrix has a heterogeneous structure and is formed from a secretion of various biopolymers, including proteins, extracellular DNA, and polysaccharides. It is generally known to interact with biofilm cells, thus affecting cell physiology and cell-cell communication. Despite the fact that the matrix may comprise up to 90% of the biofilm dry weight, how the matrix properties affect biofilm structure, maturation, and interspecies interactions remain largely unexplored. This study reveals that bacteria can use specific extracellular polymers to modulate the physical properties of their microenvironment. This in turn impacts biofilm structure, differentiation, and interspecies interactions. </jats:p> |
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| spelling | Chew, Su Chuen Kundukad, Binu Seviour, Thomas van der Maarel, Johan R. C. Yang, Liang Rice, Scott A. Doyle, Patrick Kjelleberg, Staffan 2161-2129 2150-7511 American Society for Microbiology Virology Microbiology http://dx.doi.org/10.1128/mbio.01536-14 <jats:title>ABSTRACT</jats:title> <jats:p> Biofilms are densely populated communities of microbial cells protected and held together by a matrix of extracellular polymeric substances. The structure and rheological properties of the matrix at the microscale influence the retention and transport of molecules and cells in the biofilm, thereby dictating population and community behavior. Despite its importance, quantitative descriptions of the matrix microstructure and microrheology are limited. Here, particle-tracking microrheology in combination with genetic approaches was used to spatially and temporally study the rheological contributions of the major exopolysaccharides Pel and Psl in <jats:named-content content-type="genus-species">Pseudomonas aeruginosa</jats:named-content> biofilms. Psl increased the elasticity and effective cross-linking within the matrix, which strengthened its scaffold and appeared to facilitate the formation of microcolonies. Conversely, Pel reduced effective cross-linking within the matrix. Without Psl, the matrix becomes more viscous, which facilitates biofilm spreading. The wild-type biofilm decreased in effective cross-linking over time, which would be advantageous for the spreading and colonization of new surfaces. This suggests that there are regulatory mechanisms to control production of the exopolysaccharides that serve to remodel the matrix of developing biofilms. The exopolysaccharides were also found to have profound effects on the spatial organization and integration of <jats:named-content content-type="genus-species">P. aeruginosa</jats:named-content> in a mixed-species biofilm model of <jats:italic>P. aeruginosa</jats:italic> - <jats:named-content content-type="genus-species">Staphylococcus aureus</jats:named-content> . Pel was required for close association of the two species in mixed-species microcolonies. In contrast, Psl was important for <jats:named-content content-type="genus-species">P. aeruginosa</jats:named-content> to form single-species biofilms on top of <jats:named-content content-type="genus-species">S. aureus</jats:named-content> biofilms. Our results demonstrate that Pel and Psl have distinct physical properties and functional roles during biofilm formation. </jats:p> <jats:p> <jats:bold>IMPORTANCE</jats:bold> Most bacteria grow as biofilms in the environment or in association with eukaryotic hosts. Removal of biofilms that form on surfaces is a challenge in clinical and industrial settings. One of the defining features of a biofilm is its extracellular matrix. The matrix has a heterogeneous structure and is formed from a secretion of various biopolymers, including proteins, extracellular DNA, and polysaccharides. It is generally known to interact with biofilm cells, thus affecting cell physiology and cell-cell communication. Despite the fact that the matrix may comprise up to 90% of the biofilm dry weight, how the matrix properties affect biofilm structure, maturation, and interspecies interactions remain largely unexplored. This study reveals that bacteria can use specific extracellular polymers to modulate the physical properties of their microenvironment. This in turn impacts biofilm structure, differentiation, and interspecies interactions. </jats:p> Dynamic Remodeling of Microbial Biofilms by Functionally Distinct Exopolysaccharides mBio |
| spellingShingle | Chew, Su Chuen, Kundukad, Binu, Seviour, Thomas, van der Maarel, Johan R. C., Yang, Liang, Rice, Scott A., Doyle, Patrick, Kjelleberg, Staffan, mBio, Dynamic Remodeling of Microbial Biofilms by Functionally Distinct Exopolysaccharides, Virology, Microbiology |
| title | Dynamic Remodeling of Microbial Biofilms by Functionally Distinct Exopolysaccharides |
| title_full | Dynamic Remodeling of Microbial Biofilms by Functionally Distinct Exopolysaccharides |
| title_fullStr | Dynamic Remodeling of Microbial Biofilms by Functionally Distinct Exopolysaccharides |
| title_full_unstemmed | Dynamic Remodeling of Microbial Biofilms by Functionally Distinct Exopolysaccharides |
| title_short | Dynamic Remodeling of Microbial Biofilms by Functionally Distinct Exopolysaccharides |
| title_sort | dynamic remodeling of microbial biofilms by functionally distinct exopolysaccharides |
| title_unstemmed | Dynamic Remodeling of Microbial Biofilms by Functionally Distinct Exopolysaccharides |
| topic | Virology, Microbiology |
| url | http://dx.doi.org/10.1128/mbio.01536-14 |