A Distinguishable Role of eDNA in the Viscoelastic Relaxation of Biofilms

ABSTRACT Bacteria in the biofilm mode of growth are protected against chemical and mechanical stresses. Biofilms are composed, for the most part, of extracellular polymeric substances (EPSs). The extracellular matrix is composed of different chemical constituents, such as proteins, polysaccharides,...

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Autores principales:	Brandon W. Peterson, Henny C. van der Mei, Jelmer Sjollema, Henk J. Busscher, Prashant K. Sharma
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2013
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/7a8501b3d3ee4c4a861f74c3528fe468
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spelling	oai:doaj.org-article:7a8501b3d3ee4c4a861f74c3528fe4682021-11-15T15:42:48ZA Distinguishable Role of eDNA in the Viscoelastic Relaxation of Biofilms10.1128/mBio.00497-132150-7511https://doaj.org/article/7a8501b3d3ee4c4a861f74c3528fe4682013-11-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00497-13https://doaj.org/toc/2150-7511ABSTRACT Bacteria in the biofilm mode of growth are protected against chemical and mechanical stresses. Biofilms are composed, for the most part, of extracellular polymeric substances (EPSs). The extracellular matrix is composed of different chemical constituents, such as proteins, polysaccharides, and extracellular DNA (eDNA). Here we aimed to identify the roles of different matrix constituents in the viscoelastic response of biofilms. Staphylococcus aureus, Staphylococcus epidermidis, Streptococcus mutans, and Pseudomonas aeruginosa biofilms were grown under different conditions yielding distinct matrix chemistries. Next, biofilms were subjected to mechanical deformation and stress relaxation was monitored over time. A Maxwell model possessing an average of four elements for an individual biofilm was used to fit the data. Maxwell elements were defined by a relaxation time constant and their relative importance. Relaxation time constants varied widely over the 104 biofilms included and were divided into seven ranges (<1, 1 to 5, 5 to 10, 10 to 50, 50 to 100, 100 to 500, and >500 s). Principal-component analysis was carried out to eliminate related time constant ranges, yielding three principal components that could be related to the known matrix chemistries. The fastest relaxation component (<3 s) was due to the presence of water and soluble polysaccharides, combined with the absence of bacteria, i.e., the heaviest masses in a biofilm. An intermediate component (3 to 70 s) was related to other EPSs, while a distinguishable role was assigned to intact eDNA, which possesses a unique principal component with a time constant range (10 to 25 s) between those of EPS constituents. This implies that eDNA modulates its interaction with other matrix constituents to control its contribution to viscoelastic relaxation under mechanical stress. IMPORTANCE The protection offered by biofilms to organisms that inhabit it against chemical and mechanical stresses is due in part to its matrix of extracellular polymeric substances (EPSs) in which biofilm organisms embed themselves. Mechanical stresses lead to deformation and possible detachment of biofilm organisms, and hence, rearrangement processes occur in a biofilm to relieve it from these stresses. Maxwell analysis of stress relaxation allows the determination of characteristic relaxation time constants, but the biofilm components and matrix constituents associated with different stress relaxation processes have never been identified. Here we grew biofilms with different matrix constituents and used principal-component analysis to reveal that the presence of water and soluble polysaccharides, together with the absence of bacteria, is associated with the fastest relaxation, while other EPSs control a second, slower relaxation. Extracellular DNA, as a matrix constituent, had a distinguishable role with its own unique principal component in stress relaxation with a time constant range between those of other EPSs.Brandon W. PetersonHenny C. van der MeiJelmer SjollemaHenk J. BusscherPrashant K. SharmaAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 4, Iss 5 (2013)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Brandon W. Peterson Henny C. van der Mei Jelmer Sjollema Henk J. Busscher Prashant K. Sharma A Distinguishable Role of eDNA in the Viscoelastic Relaxation of Biofilms
description	ABSTRACT Bacteria in the biofilm mode of growth are protected against chemical and mechanical stresses. Biofilms are composed, for the most part, of extracellular polymeric substances (EPSs). The extracellular matrix is composed of different chemical constituents, such as proteins, polysaccharides, and extracellular DNA (eDNA). Here we aimed to identify the roles of different matrix constituents in the viscoelastic response of biofilms. Staphylococcus aureus, Staphylococcus epidermidis, Streptococcus mutans, and Pseudomonas aeruginosa biofilms were grown under different conditions yielding distinct matrix chemistries. Next, biofilms were subjected to mechanical deformation and stress relaxation was monitored over time. A Maxwell model possessing an average of four elements for an individual biofilm was used to fit the data. Maxwell elements were defined by a relaxation time constant and their relative importance. Relaxation time constants varied widely over the 104 biofilms included and were divided into seven ranges (<1, 1 to 5, 5 to 10, 10 to 50, 50 to 100, 100 to 500, and >500 s). Principal-component analysis was carried out to eliminate related time constant ranges, yielding three principal components that could be related to the known matrix chemistries. The fastest relaxation component (<3 s) was due to the presence of water and soluble polysaccharides, combined with the absence of bacteria, i.e., the heaviest masses in a biofilm. An intermediate component (3 to 70 s) was related to other EPSs, while a distinguishable role was assigned to intact eDNA, which possesses a unique principal component with a time constant range (10 to 25 s) between those of EPS constituents. This implies that eDNA modulates its interaction with other matrix constituents to control its contribution to viscoelastic relaxation under mechanical stress. IMPORTANCE The protection offered by biofilms to organisms that inhabit it against chemical and mechanical stresses is due in part to its matrix of extracellular polymeric substances (EPSs) in which biofilm organisms embed themselves. Mechanical stresses lead to deformation and possible detachment of biofilm organisms, and hence, rearrangement processes occur in a biofilm to relieve it from these stresses. Maxwell analysis of stress relaxation allows the determination of characteristic relaxation time constants, but the biofilm components and matrix constituents associated with different stress relaxation processes have never been identified. Here we grew biofilms with different matrix constituents and used principal-component analysis to reveal that the presence of water and soluble polysaccharides, together with the absence of bacteria, is associated with the fastest relaxation, while other EPSs control a second, slower relaxation. Extracellular DNA, as a matrix constituent, had a distinguishable role with its own unique principal component in stress relaxation with a time constant range between those of other EPSs.
format	article
author	Brandon W. Peterson Henny C. van der Mei Jelmer Sjollema Henk J. Busscher Prashant K. Sharma
author_facet	Brandon W. Peterson Henny C. van der Mei Jelmer Sjollema Henk J. Busscher Prashant K. Sharma
author_sort	Brandon W. Peterson
title	A Distinguishable Role of eDNA in the Viscoelastic Relaxation of Biofilms
title_short	A Distinguishable Role of eDNA in the Viscoelastic Relaxation of Biofilms
title_full	A Distinguishable Role of eDNA in the Viscoelastic Relaxation of Biofilms
title_fullStr	A Distinguishable Role of eDNA in the Viscoelastic Relaxation of Biofilms
title_full_unstemmed	A Distinguishable Role of eDNA in the Viscoelastic Relaxation of Biofilms
title_sort	distinguishable role of edna in the viscoelastic relaxation of biofilms
publisher	American Society for Microbiology
publishDate	2013
url	https://doaj.org/article/7a8501b3d3ee4c4a861f74c3528fe468
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A Distinguishable Role of eDNA in the Viscoelastic Relaxation of Biofilms

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