Dynamic Remodeling of Microbial Biofilms by Functionally Distinct Exopolysaccharides

ABSTRACT 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,...

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Autores principales:	Su Chuen Chew, Binu Kundukad, Thomas Seviour, Johan R. C. van der Maarel, Liang Yang, Scott A. Rice, Patrick Doyle, Staffan Kjelleberg
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2014
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/3654bdfab4a146c1804f8555e286353a
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spelling	oai:doaj.org-article:3654bdfab4a146c1804f8555e286353a2021-11-15T15:47:21ZDynamic Remodeling of Microbial Biofilms by Functionally Distinct Exopolysaccharides10.1128/mBio.01536-142150-7511https://doaj.org/article/3654bdfab4a146c1804f8555e286353a2014-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01536-14https://doaj.org/toc/2150-7511ABSTRACT 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.Su Chuen ChewBinu KundukadThomas SeviourJohan R. C. van der MaarelLiang YangScott A. RicePatrick DoyleStaffan KjellebergAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 5, Iss 4 (2014)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Su Chuen Chew Binu Kundukad Thomas Seviour Johan R. C. van der Maarel Liang Yang Scott A. Rice Patrick Doyle Staffan Kjelleberg Dynamic Remodeling of Microbial Biofilms by Functionally Distinct Exopolysaccharides
description	ABSTRACT 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.
format	article
author	Su Chuen Chew Binu Kundukad Thomas Seviour Johan R. C. van der Maarel Liang Yang Scott A. Rice Patrick Doyle Staffan Kjelleberg
author_facet	Su Chuen Chew Binu Kundukad Thomas Seviour Johan R. C. van der Maarel Liang Yang Scott A. Rice Patrick Doyle Staffan Kjelleberg
author_sort	Su Chuen Chew
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
publisher	American Society for Microbiology
publishDate	2014
url	https://doaj.org/article/3654bdfab4a146c1804f8555e286353a
work_keys_str_mv	AT suchuenchew dynamicremodelingofmicrobialbiofilmsbyfunctionallydistinctexopolysaccharides AT binukundukad dynamicremodelingofmicrobialbiofilmsbyfunctionallydistinctexopolysaccharides AT thomasseviour dynamicremodelingofmicrobialbiofilmsbyfunctionallydistinctexopolysaccharides AT johanrcvandermaarel dynamicremodelingofmicrobialbiofilmsbyfunctionallydistinctexopolysaccharides AT liangyang dynamicremodelingofmicrobialbiofilmsbyfunctionallydistinctexopolysaccharides AT scottarice dynamicremodelingofmicrobialbiofilmsbyfunctionallydistinctexopolysaccharides AT patrickdoyle dynamicremodelingofmicrobialbiofilmsbyfunctionallydistinctexopolysaccharides AT staffankjelleberg dynamicremodelingofmicrobialbiofilmsbyfunctionallydistinctexopolysaccharides
_version_	1718427509048999936

Dynamic Remodeling of Microbial Biofilms by Functionally Distinct Exopolysaccharides

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