Matrix Polysaccharides and SiaD Diguanylate Cyclase Alter Community Structure and Competitiveness of <italic toggle="yes">Pseudomonas aeruginosa</italic> during Dual-Species Biofilm Development with <italic toggle="yes">Staphylococcus aureus</italic>

ABSTRACT Mixed-species biofilms display a number of emergent properties, including enhanced antimicrobial tolerance and communal metabolism. These properties may depend on interspecies relationships and the structure of the biofilm. However, the contribution of specific matrix components to emergent...

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Autores principales:	Su Chuen Chew, Joey Kuok Hoong Yam, Artur Matysik, Zi Jing Seng, Janosch Klebensberger, Michael Givskov, Patrick Doyle, Scott A. Rice, Liang Yang, Staffan Kjelleberg
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	Pseudomonas aeruginosa SiaD Staphylococcus aureus biofilms cyclic di-GMP exopolysaccharide Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/d11b5ff79333434889f67fa47593faae
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spelling	oai:doaj.org-article:d11b5ff79333434889f67fa47593faae2021-11-15T15:52:19ZMatrix Polysaccharides and SiaD Diguanylate Cyclase Alter Community Structure and Competitiveness of <italic toggle="yes">Pseudomonas aeruginosa</italic> during Dual-Species Biofilm Development with <italic toggle="yes">Staphylococcus aureus</italic>10.1128/mBio.00585-182150-7511https://doaj.org/article/d11b5ff79333434889f67fa47593faae2018-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00585-18https://doaj.org/toc/2150-7511ABSTRACT Mixed-species biofilms display a number of emergent properties, including enhanced antimicrobial tolerance and communal metabolism. These properties may depend on interspecies relationships and the structure of the biofilm. However, the contribution of specific matrix components to emergent properties of mixed-species biofilms remains poorly understood. Using a dual-species biofilm community formed by the opportunistic pathogens Pseudomonas aeruginosa and Staphylococcus aureus, we found that whilst neither Pel nor Psl polysaccharides, produced by P. aeruginosa, affect relative species abundance in mature P. aeruginosa and S. aureus biofilms, Psl production is associated with increased P. aeruginosa abundance and reduced S. aureus aggregation in the early stages of biofilm formation. Our data suggest that the competitive effect of Psl is not associated with its structural role in cross-linking the matrix and adhering to P. aeruginosa cells but is instead mediated through the activation of the diguanylate cyclase SiaD. This regulatory control was also found to be independent of the siderophore pyoverdine and Pseudomonas quinolone signal, which have previously been proposed to reduce S. aureus viability by inducing lactic acid fermentation-based growth. In contrast to the effect mediated by Psl, Pel reduced the effective crosslinking of the biofilm matrix and facilitated superdiffusivity in microcolony regions. These changes in matrix cross-linking enhance biofilm surface spreading and expansion of microcolonies in the later stages of biofilm development, improving overall dual-species biofilm growth and increasing biovolume severalfold. Thus, the biofilm matrix and regulators associated with matrix production play essential roles in mixed-species biofilm interactions. IMPORTANCE Bacteria in natural and engineered environments form biofilms that include many different species. Microorganisms rely on a number of different strategies to manage social interactions with other species and to access resources, build biofilm consortia, and optimize growth. For example, Pseudomonas aeruginosa and Staphylococcus aureus are biofilm-forming bacteria that coinfect the lungs of cystic fibrosis patients and diabetic and chronic wounds. P. aeruginosa is known to antagonize S. aureus growth. However, many of the factors responsible for mixed-species interactions and outcomes such as infections are poorly understood. Biofilm bacteria are encased in a self-produced extracellular matrix that facilitates interspecies behavior and biofilm development. In this study, we examined the poorly understood roles of the major matrix biopolymers and their regulators in mixed-species biofilm interactions and development.Su Chuen ChewJoey Kuok Hoong YamArtur MatysikZi Jing SengJanosch KlebensbergerMichael GivskovPatrick DoyleScott A. RiceLiang YangStaffan KjellebergAmerican Society for MicrobiologyarticlePseudomonas aeruginosaSiaDStaphylococcus aureusbiofilmscyclic di-GMPexopolysaccharideMicrobiologyQR1-502ENmBio, Vol 9, Iss 6 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	Pseudomonas aeruginosa SiaD Staphylococcus aureus biofilms cyclic di-GMP exopolysaccharide Microbiology QR1-502
spellingShingle	Pseudomonas aeruginosa SiaD Staphylococcus aureus biofilms cyclic di-GMP exopolysaccharide Microbiology QR1-502 Su Chuen Chew Joey Kuok Hoong Yam Artur Matysik Zi Jing Seng Janosch Klebensberger Michael Givskov Patrick Doyle Scott A. Rice Liang Yang Staffan Kjelleberg Matrix Polysaccharides and SiaD Diguanylate Cyclase Alter Community Structure and Competitiveness of <italic toggle="yes">Pseudomonas aeruginosa</italic> during Dual-Species Biofilm Development with <italic toggle="yes">Staphylococcus aureus</italic>
description	ABSTRACT Mixed-species biofilms display a number of emergent properties, including enhanced antimicrobial tolerance and communal metabolism. These properties may depend on interspecies relationships and the structure of the biofilm. However, the contribution of specific matrix components to emergent properties of mixed-species biofilms remains poorly understood. Using a dual-species biofilm community formed by the opportunistic pathogens Pseudomonas aeruginosa and Staphylococcus aureus, we found that whilst neither Pel nor Psl polysaccharides, produced by P. aeruginosa, affect relative species abundance in mature P. aeruginosa and S. aureus biofilms, Psl production is associated with increased P. aeruginosa abundance and reduced S. aureus aggregation in the early stages of biofilm formation. Our data suggest that the competitive effect of Psl is not associated with its structural role in cross-linking the matrix and adhering to P. aeruginosa cells but is instead mediated through the activation of the diguanylate cyclase SiaD. This regulatory control was also found to be independent of the siderophore pyoverdine and Pseudomonas quinolone signal, which have previously been proposed to reduce S. aureus viability by inducing lactic acid fermentation-based growth. In contrast to the effect mediated by Psl, Pel reduced the effective crosslinking of the biofilm matrix and facilitated superdiffusivity in microcolony regions. These changes in matrix cross-linking enhance biofilm surface spreading and expansion of microcolonies in the later stages of biofilm development, improving overall dual-species biofilm growth and increasing biovolume severalfold. Thus, the biofilm matrix and regulators associated with matrix production play essential roles in mixed-species biofilm interactions. IMPORTANCE Bacteria in natural and engineered environments form biofilms that include many different species. Microorganisms rely on a number of different strategies to manage social interactions with other species and to access resources, build biofilm consortia, and optimize growth. For example, Pseudomonas aeruginosa and Staphylococcus aureus are biofilm-forming bacteria that coinfect the lungs of cystic fibrosis patients and diabetic and chronic wounds. P. aeruginosa is known to antagonize S. aureus growth. However, many of the factors responsible for mixed-species interactions and outcomes such as infections are poorly understood. Biofilm bacteria are encased in a self-produced extracellular matrix that facilitates interspecies behavior and biofilm development. In this study, we examined the poorly understood roles of the major matrix biopolymers and their regulators in mixed-species biofilm interactions and development.
format	article
author	Su Chuen Chew Joey Kuok Hoong Yam Artur Matysik Zi Jing Seng Janosch Klebensberger Michael Givskov Patrick Doyle Scott A. Rice Liang Yang Staffan Kjelleberg
author_facet	Su Chuen Chew Joey Kuok Hoong Yam Artur Matysik Zi Jing Seng Janosch Klebensberger Michael Givskov Patrick Doyle Scott A. Rice Liang Yang Staffan Kjelleberg
author_sort	Su Chuen Chew
title	Matrix Polysaccharides and SiaD Diguanylate Cyclase Alter Community Structure and Competitiveness of <italic toggle="yes">Pseudomonas aeruginosa</italic> during Dual-Species Biofilm Development with <italic toggle="yes">Staphylococcus aureus</italic>
title_short	Matrix Polysaccharides and SiaD Diguanylate Cyclase Alter Community Structure and Competitiveness of <italic toggle="yes">Pseudomonas aeruginosa</italic> during Dual-Species Biofilm Development with <italic toggle="yes">Staphylococcus aureus</italic>
title_full	Matrix Polysaccharides and SiaD Diguanylate Cyclase Alter Community Structure and Competitiveness of <italic toggle="yes">Pseudomonas aeruginosa</italic> during Dual-Species Biofilm Development with <italic toggle="yes">Staphylococcus aureus</italic>
title_fullStr	Matrix Polysaccharides and SiaD Diguanylate Cyclase Alter Community Structure and Competitiveness of <italic toggle="yes">Pseudomonas aeruginosa</italic> during Dual-Species Biofilm Development with <italic toggle="yes">Staphylococcus aureus</italic>
title_full_unstemmed	Matrix Polysaccharides and SiaD Diguanylate Cyclase Alter Community Structure and Competitiveness of <italic toggle="yes">Pseudomonas aeruginosa</italic> during Dual-Species Biofilm Development with <italic toggle="yes">Staphylococcus aureus</italic>
title_sort	matrix polysaccharides and siad diguanylate cyclase alter community structure and competitiveness of <italic toggle="yes">pseudomonas aeruginosa</italic> during dual-species biofilm development with <italic toggle="yes">staphylococcus aureus</italic>
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/d11b5ff79333434889f67fa47593faae
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Matrix Polysaccharides and SiaD Diguanylate Cyclase Alter Community Structure and Competitiveness of <italic toggle="yes">Pseudomonas aeruginosa</italic> during Dual-Species Biofilm Development with <italic toggle="yes">Staphylococcus aureus</italic>

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