Dynamic remodeling of microbial biofilms by functionally distinct exopolysaccharides

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 d...

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Main Authors: Chew, Su Chuen, Kundukad, Binu, Seviour, Thomas, Van der Maarel, Johan R. C., Yang, Liang, Rice, Scott A., Doyle, Patrick, Kjelleberg, Staffan
Other Authors: School of Biological Sciences
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Language:English
Published: 2014
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Online Access:https://hdl.handle.net/10356/101844
http://hdl.handle.net/10220/24214
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spelling sg-ntu-dr.10356-1018442022-02-16T16:27:51Z Dynamic remodeling of microbial biofilms by functionally distinct exopolysaccharides Chew, Su Chuen Kundukad, Binu Seviour, Thomas Van der Maarel, Johan R. C. Yang, Liang Rice, Scott A. Doyle, Patrick Kjelleberg, Staffan School of Biological Sciences Singapore Centre for Environmental Life Sciences Engineering DRNTU::Science::Biological sciences 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 Pseudomonas aeruginosa 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 P. aeruginosa in a mixed-species biofilm model of P. aeruginosa-Staphylococcus aureus. Pel was required for close association of the two species in mixed-species microcolonies. In contrast, Psl was important for P. aeruginosa to form single-species biofilms on top of S. aureus biofilms. Our results demonstrate that Pel and Psl have distinct physical properties and functional roles during biofilm formation. IMPORTANCE: 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. Published version 2014-11-11T01:05:14Z 2019-12-06T20:45:30Z 2014-11-11T01:05:14Z 2019-12-06T20:45:30Z 2014 2014 Journal Article Chew, S. C., Kundukad, B., Seviour, T., van der Maarel, J. R. C., Yang, L., Rice, S. A., et al. (2014). Dynamic remodeling of microbial biofilms by functionally distinct exopolysaccharides. mBio, 5(4), 1-11. 2150-7511 https://hdl.handle.net/10356/101844 http://hdl.handle.net/10220/24214 10.1128/mBio.01536-14 25096883 en mBio © 2014 Chew et al. This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited. 12 p. application/pdf
institution Nanyang Technological University
building NTU Library
continent Asia
country Singapore
Singapore
content_provider NTU Library
collection DR-NTU
language English
topic DRNTU::Science::Biological sciences
spellingShingle DRNTU::Science::Biological sciences
Chew, Su Chuen
Kundukad, Binu
Seviour, Thomas
Van der Maarel, Johan R. C.
Yang, Liang
Rice, Scott A.
Doyle, Patrick
Kjelleberg, Staffan
Dynamic remodeling of microbial biofilms by functionally distinct exopolysaccharides
description 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 Pseudomonas aeruginosa 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 P. aeruginosa in a mixed-species biofilm model of P. aeruginosa-Staphylococcus aureus. Pel was required for close association of the two species in mixed-species microcolonies. In contrast, Psl was important for P. aeruginosa to form single-species biofilms on top of S. aureus biofilms. Our results demonstrate that Pel and Psl have distinct physical properties and functional roles during biofilm formation. IMPORTANCE: 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.
author2 School of Biological Sciences
author_facet School of Biological Sciences
Chew, Su Chuen
Kundukad, Binu
Seviour, Thomas
Van der Maarel, Johan R. C.
Yang, Liang
Rice, Scott A.
Doyle, Patrick
Kjelleberg, Staffan
format Article
author Chew, Su Chuen
Kundukad, Binu
Seviour, Thomas
Van der Maarel, Johan R. C.
Yang, Liang
Rice, Scott A.
Doyle, Patrick
Kjelleberg, Staffan
author_sort Chew, Su Chuen
title Dynamic remodeling of microbial biofilms by functionally distinct exopolysaccharides
title_short 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_sort dynamic remodeling of microbial biofilms by functionally distinct exopolysaccharides
publishDate 2014
url https://hdl.handle.net/10356/101844
http://hdl.handle.net/10220/24214
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