Emergent Properties in <named-content content-type="genus-species">Streptococcus mutans</named-content> Biofilms Are Controlled through Adhesion Force Sensing by Initial Colonizers

ABSTRACT Bacterial adhesion is accompanied by altered gene expression, leading to “emergent” properties of biofilm bacteria that are alien to planktonic ones. With the aim of revealing the role of environmental adhesion forces in emergent biofilm properties, genes in Streptococcus mutans UA159 and a...

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Autores principales:	Can Wang, Jiapeng Hou, Henny C. van der Mei, Henk J. Busscher, Yijin Ren
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	OCT atomic force microscopy quorum sensing regulation of gene expression surface sensing Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/b19810dcfb614b4f8ecb72e45c2e76f8
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spelling	oai:doaj.org-article:b19810dcfb614b4f8ecb72e45c2e76f82021-11-15T15:59:41ZEmergent Properties in <named-content content-type="genus-species">Streptococcus mutans</named-content> Biofilms Are Controlled through Adhesion Force Sensing by Initial Colonizers10.1128/mBio.01908-192150-7511https://doaj.org/article/b19810dcfb614b4f8ecb72e45c2e76f82019-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01908-19https://doaj.org/toc/2150-7511ABSTRACT Bacterial adhesion is accompanied by altered gene expression, leading to “emergent” properties of biofilm bacteria that are alien to planktonic ones. With the aim of revealing the role of environmental adhesion forces in emergent biofilm properties, genes in Streptococcus mutans UA159 and a quorum-sensing-deficient mutant were identified that become expressed after adhesion to substratum surfaces. Using atomic force microscopy, adhesion forces of initial S. mutans colonizers on four different substrata were determined and related to gene expression. Adhesion forces upon initial contact were similarly low across different substrata, ranging between 0.2 and 1.2 nN regardless of the strain considered. Bond maturation required up to 21 s, depending on the strain and substratum surface involved, but stationary adhesion forces also were similar in the parent and in the mutant strain. However, stationary adhesion forces were largest on hydrophobic silicone rubber (19 to 20 nN), while being smallest on hydrophilic glass (3 to 4 nN). brpA gene expression in thin (34 to 48 μm) 5-h S. mutans UA159 biofilms was most sensitive to adhesion forces, while expression of gbpB and comDE expressions was weakly sensitive. ftf, gtfB, vicR, and relA expression was insensitive to adhesion forces. In thicker (98 to 151 μm) 24-h biofilms, adhesion-force-induced gene expression and emergent extracellular polymeric substance (EPS) production were limited to the first 20 to 30 μm above a substratum surface. In the quorum-sensing-deficient S. mutans, adhesion-force-controlled gene expression was absent in both 5- and 24-h biofilms. Thus, initial colonizers of substratum surfaces sense adhesion forces that externally trigger emergent biofilm properties over a limited distance above a substratum surface through quorum sensing. IMPORTANCE A new concept in biofilm science is introduced: “adhesion force sensitivity of genes,” defining the degree up to which expression of different genes in adhering bacteria is controlled by the environmental adhesion forces they experience. Analysis of gene expression as a function of height in a biofilm showed that the information about the substratum surface to which initially adhering bacteria adhere is passed up to a biofilm height of 20 to 30 μm above a substratum surface, highlighting the importance and limitations of cell-to-cell communication in a biofilm. Bacteria in a biofilm mode of growth, as opposed to planktonic growth, are responsible for the great majority of human infections, predicted to become the number one cause of death in 2050. The concept of adhesion force sensitivity of genes provides better understanding of bacterial adaptation in biofilms, direly needed for the design of improved therapeutic measures that evade the recalcitrance of biofilm bacteria to antimicrobials.Can WangJiapeng HouHenny C. van der MeiHenk J. BusscherYijin RenAmerican Society for MicrobiologyarticleOCTatomic force microscopyquorum sensingregulation of gene expressionsurface sensingMicrobiologyQR1-502ENmBio, Vol 10, Iss 5 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	OCT atomic force microscopy quorum sensing regulation of gene expression surface sensing Microbiology QR1-502
spellingShingle	OCT atomic force microscopy quorum sensing regulation of gene expression surface sensing Microbiology QR1-502 Can Wang Jiapeng Hou Henny C. van der Mei Henk J. Busscher Yijin Ren Emergent Properties in <named-content content-type="genus-species">Streptococcus mutans</named-content> Biofilms Are Controlled through Adhesion Force Sensing by Initial Colonizers
description	ABSTRACT Bacterial adhesion is accompanied by altered gene expression, leading to “emergent” properties of biofilm bacteria that are alien to planktonic ones. With the aim of revealing the role of environmental adhesion forces in emergent biofilm properties, genes in Streptococcus mutans UA159 and a quorum-sensing-deficient mutant were identified that become expressed after adhesion to substratum surfaces. Using atomic force microscopy, adhesion forces of initial S. mutans colonizers on four different substrata were determined and related to gene expression. Adhesion forces upon initial contact were similarly low across different substrata, ranging between 0.2 and 1.2 nN regardless of the strain considered. Bond maturation required up to 21 s, depending on the strain and substratum surface involved, but stationary adhesion forces also were similar in the parent and in the mutant strain. However, stationary adhesion forces were largest on hydrophobic silicone rubber (19 to 20 nN), while being smallest on hydrophilic glass (3 to 4 nN). brpA gene expression in thin (34 to 48 μm) 5-h S. mutans UA159 biofilms was most sensitive to adhesion forces, while expression of gbpB and comDE expressions was weakly sensitive. ftf, gtfB, vicR, and relA expression was insensitive to adhesion forces. In thicker (98 to 151 μm) 24-h biofilms, adhesion-force-induced gene expression and emergent extracellular polymeric substance (EPS) production were limited to the first 20 to 30 μm above a substratum surface. In the quorum-sensing-deficient S. mutans, adhesion-force-controlled gene expression was absent in both 5- and 24-h biofilms. Thus, initial colonizers of substratum surfaces sense adhesion forces that externally trigger emergent biofilm properties over a limited distance above a substratum surface through quorum sensing. IMPORTANCE A new concept in biofilm science is introduced: “adhesion force sensitivity of genes,” defining the degree up to which expression of different genes in adhering bacteria is controlled by the environmental adhesion forces they experience. Analysis of gene expression as a function of height in a biofilm showed that the information about the substratum surface to which initially adhering bacteria adhere is passed up to a biofilm height of 20 to 30 μm above a substratum surface, highlighting the importance and limitations of cell-to-cell communication in a biofilm. Bacteria in a biofilm mode of growth, as opposed to planktonic growth, are responsible for the great majority of human infections, predicted to become the number one cause of death in 2050. The concept of adhesion force sensitivity of genes provides better understanding of bacterial adaptation in biofilms, direly needed for the design of improved therapeutic measures that evade the recalcitrance of biofilm bacteria to antimicrobials.
format	article
author	Can Wang Jiapeng Hou Henny C. van der Mei Henk J. Busscher Yijin Ren
author_facet	Can Wang Jiapeng Hou Henny C. van der Mei Henk J. Busscher Yijin Ren
author_sort	Can Wang
title	Emergent Properties in <named-content content-type="genus-species">Streptococcus mutans</named-content> Biofilms Are Controlled through Adhesion Force Sensing by Initial Colonizers
title_short	Emergent Properties in <named-content content-type="genus-species">Streptococcus mutans</named-content> Biofilms Are Controlled through Adhesion Force Sensing by Initial Colonizers
title_full	Emergent Properties in <named-content content-type="genus-species">Streptococcus mutans</named-content> Biofilms Are Controlled through Adhesion Force Sensing by Initial Colonizers
title_fullStr	Emergent Properties in <named-content content-type="genus-species">Streptococcus mutans</named-content> Biofilms Are Controlled through Adhesion Force Sensing by Initial Colonizers
title_full_unstemmed	Emergent Properties in <named-content content-type="genus-species">Streptococcus mutans</named-content> Biofilms Are Controlled through Adhesion Force Sensing by Initial Colonizers
title_sort	emergent properties in <named-content content-type="genus-species">streptococcus mutans</named-content> biofilms are controlled through adhesion force sensing by initial colonizers
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/b19810dcfb614b4f8ecb72e45c2e76f8
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Emergent Properties in <named-content content-type="genus-species">Streptococcus mutans</named-content> Biofilms Are Controlled through Adhesion Force Sensing by Initial Colonizers

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