Physico-chemistry from initial bacterial adhesion to surface-programmed biofilm growth.
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| Title: | Physico-chemistry from initial bacterial adhesion to surface-programmed biofilm growth. |
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| Authors: | Carniello, Vera1, Peterson, Brandon W.1, van der Mei, Henny C.1 h.c.van.der.mei@umcg.nl, Busscher, Henk J.1 |
| Source: | Advances in Colloid & Interface Science. Nov2018, Vol. 261, p1-14. 14p. |
| Subjects: | Biofilms testing, Bacterial adhesion, Quorum sensing, Surface properties, Thermodynamics |
| Abstract: | Abstract Biofilm formation is initiated by adhesion of individual bacteria to a surface. However, surface adhesion alone is not sufficient to form the complex community architecture of a biofilm. Surface-sensing creates bacterial awareness of their adhering state on the surface and is essential to initiate the phenotypic and genotypic changes that characterize the transition from initial bacterial adhesion to a biofilm. Physico-chemistry has been frequently applied to explain initial bacterial adhesion phenomena, including bacterial mass transport, role of substratum surface properties in initial adhesion and the transition from reversible to irreversible adhesion. However, also emergent biofilm properties, such as production of extracellular-polymeric-substances (EPS), can be surface-programmed. This review presents a four-step, comprehensive description of the role of physico-chemistry from initial bacterial adhesion to surface-programmed biofilm growth: (1) bacterial mass transport towards a surface, (2) reversible bacterial adhesion and (3) transition to irreversible adhesion and (4) cell wall deformation and associated emergent properties. Bacterial transport mostly occurs from sedimentation or convective-diffusion, while initial bacterial adhesion can be described by surface thermodynamic and Derjaguin−Landau−Verwey−Overbeek (DLVO)-analyses, considering bacteria as smooth, inert colloidal particles. DLVO-analyses however, require precise indication of the bacterial cell surface, which is impossible due to the presence of bacterial surface tethers, creating a multi-scale roughness that impedes proper definition of the interaction distance in DLVO-analyses. Application of surface thermodynamics is also difficult, because initial bacterial adhesion is only an equilibrium phenomenon for a short period of time, when bacteria are attached to a substratum surface through few surface tethers. Physico-chemical bond-strengthening occurs in several minutes leading to irreversible adhesion due to progressive removal of interfacial water, conformational changes in cell surface proteins, re-orientation of bacteria on a surface and the progressive involvement of more tethers in adhesion. After initial bond-strengthening, adhesion forces arising from a substratum surface cause nanoscopic deformation of the bacterial cell wall against the elasticity of the rigid peptidoglycan layer positioned in the cell wall and the intracellular pressure of the cytoplasm. Cell wall deformation not only increases the contact area with a substratum surface, presenting another physico-chemical bond-strengthening mechanism, but is also accompanied by membrane surface tension changes. Membrane-located sensor molecules subsequently react to control emergent phenotypic and genotypic properties in biofilms, most notably adhesion-associated ones like EPS production. Moreover, also bacterial efflux pump systems may be activated or mechano-sensitive channels may be opened upon adhesion-induced cell wall deformation. The physico-chemical properties of the substratum surface thus control the response of initially adhering bacteria and through excretion of autoinducer molecules extend the awareness of their adhering state to other biofilm inhabitants who subsequently respond with similar emergent properties. Herewith, physico-chemistry is not only involved in initial bacterial adhesion to surfaces but also in what we here propose to call "surface-programmed" biofilm growth. This conclusion is pivotal for the development of new strategies to control biofilm formation on substratum surfaces, that have hitherto been largely confined to the initial bacterial adhesion phenomena. Graphical abstract Unlabelled Image Highlights • Physico-chemistry dictates initial bacterial adhesion to substratum surfaces • Bond-strengthening leads to irreversible adhesion of bacteria (and inert colloids) • Through quorum-sensing, bacteria share information on substratum surface properties • Substratum surface properties program emergent biofilm properties • Regarding bacteria as inert colloids, does not yield a generalized biofilm model [ABSTRACT FROM AUTHOR] |
| Copyright of Advances in Colloid & Interface Science is the property of Elsevier B.V. and its content may not be copied or emailed to multiple sites without the copyright holder's express written permission. Additionally, content may not be used with any artificial intelligence tools or machine learning technologies. However, users may print, download, or email articles for individual use. This abstract may be abridged. No warranty is given about the accuracy of the copy. Users should refer to the original published version of the material for the full abstract. (Copyright applies to all Abstracts.) | |
| Database: | Engineering Source |
| FullText | Text: Availability: 0 |
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| Header | DbId: egs DbLabel: Engineering Source An: 132896505 AccessLevel: 6 PubType: Academic Journal PubTypeId: academicJournal PreciseRelevancyScore: 0 |
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| Items | – Name: Title Label: Title Group: Ti Data: Physico-chemistry from initial bacterial adhesion to surface-programmed biofilm growth. – Name: Author Label: Authors Group: Au Data: <searchLink fieldCode="AR" term="%22Carniello%2C+Vera%22">Carniello, Vera</searchLink><relatesTo>1</relatesTo><br /><searchLink fieldCode="AR" term="%22Peterson%2C+Brandon+W%2E%22">Peterson, Brandon W.</searchLink><relatesTo>1</relatesTo><br /><searchLink fieldCode="AR" term="%22van+der+Mei%2C+Henny+C%2E%22">van der Mei, Henny C.</searchLink><relatesTo>1</relatesTo><i> h.c.van.der.mei@umcg.nl</i><br /><searchLink fieldCode="AR" term="%22Busscher%2C+Henk+J%2E%22">Busscher, Henk J.</searchLink><relatesTo>1</relatesTo> – Name: TitleSource Label: Source Group: Src Data: <searchLink fieldCode="JN" term="%22Advances+in+Colloid+%26+Interface+Science%22">Advances in Colloid & Interface Science</searchLink>. Nov2018, Vol. 261, p1-14. 14p. – Name: Subject Label: Subjects Group: Su Data: <searchLink fieldCode="DE" term="%22Biofilms+testing%22">Biofilms testing</searchLink><br /><searchLink fieldCode="DE" term="%22Bacterial+adhesion%22">Bacterial adhesion</searchLink><br /><searchLink fieldCode="DE" term="%22Quorum+sensing%22">Quorum sensing</searchLink><br /><searchLink fieldCode="DE" term="%22Surface+properties%22">Surface properties</searchLink><br /><searchLink fieldCode="DE" term="%22Thermodynamics%22">Thermodynamics</searchLink> – Name: Abstract Label: Abstract Group: Ab Data: Abstract Biofilm formation is initiated by adhesion of individual bacteria to a surface. However, surface adhesion alone is not sufficient to form the complex community architecture of a biofilm. Surface-sensing creates bacterial awareness of their adhering state on the surface and is essential to initiate the phenotypic and genotypic changes that characterize the transition from initial bacterial adhesion to a biofilm. Physico-chemistry has been frequently applied to explain initial bacterial adhesion phenomena, including bacterial mass transport, role of substratum surface properties in initial adhesion and the transition from reversible to irreversible adhesion. However, also emergent biofilm properties, such as production of extracellular-polymeric-substances (EPS), can be surface-programmed. This review presents a four-step, comprehensive description of the role of physico-chemistry from initial bacterial adhesion to surface-programmed biofilm growth: (1) bacterial mass transport towards a surface, (2) reversible bacterial adhesion and (3) transition to irreversible adhesion and (4) cell wall deformation and associated emergent properties. Bacterial transport mostly occurs from sedimentation or convective-diffusion, while initial bacterial adhesion can be described by surface thermodynamic and Derjaguin−Landau−Verwey−Overbeek (DLVO)-analyses, considering bacteria as smooth, inert colloidal particles. DLVO-analyses however, require precise indication of the bacterial cell surface, which is impossible due to the presence of bacterial surface tethers, creating a multi-scale roughness that impedes proper definition of the interaction distance in DLVO-analyses. Application of surface thermodynamics is also difficult, because initial bacterial adhesion is only an equilibrium phenomenon for a short period of time, when bacteria are attached to a substratum surface through few surface tethers. Physico-chemical bond-strengthening occurs in several minutes leading to irreversible adhesion due to progressive removal of interfacial water, conformational changes in cell surface proteins, re-orientation of bacteria on a surface and the progressive involvement of more tethers in adhesion. After initial bond-strengthening, adhesion forces arising from a substratum surface cause nanoscopic deformation of the bacterial cell wall against the elasticity of the rigid peptidoglycan layer positioned in the cell wall and the intracellular pressure of the cytoplasm. Cell wall deformation not only increases the contact area with a substratum surface, presenting another physico-chemical bond-strengthening mechanism, but is also accompanied by membrane surface tension changes. Membrane-located sensor molecules subsequently react to control emergent phenotypic and genotypic properties in biofilms, most notably adhesion-associated ones like EPS production. Moreover, also bacterial efflux pump systems may be activated or mechano-sensitive channels may be opened upon adhesion-induced cell wall deformation. The physico-chemical properties of the substratum surface thus control the response of initially adhering bacteria and through excretion of autoinducer molecules extend the awareness of their adhering state to other biofilm inhabitants who subsequently respond with similar emergent properties. Herewith, physico-chemistry is not only involved in initial bacterial adhesion to surfaces but also in what we here propose to call "surface-programmed" biofilm growth. This conclusion is pivotal for the development of new strategies to control biofilm formation on substratum surfaces, that have hitherto been largely confined to the initial bacterial adhesion phenomena. Graphical abstract Unlabelled Image Highlights • Physico-chemistry dictates initial bacterial adhesion to substratum surfaces • Bond-strengthening leads to irreversible adhesion of bacteria (and inert colloids) • Through quorum-sensing, bacteria share information on substratum surface properties • Substratum surface properties program emergent biofilm properties • Regarding bacteria as inert colloids, does not yield a generalized biofilm model [ABSTRACT FROM AUTHOR] – Name: AbstractSuppliedCopyright Label: Group: Ab Data: <i>Copyright of Advances in Colloid & Interface Science is the property of Elsevier B.V. and its content may not be copied or emailed to multiple sites without the copyright holder's express written permission. Additionally, content may not be used with any artificial intelligence tools or machine learning technologies. However, users may print, download, or email articles for individual use. This abstract may be abridged. No warranty is given about the accuracy of the copy. Users should refer to the original published version of the material for the full abstract.</i> (Copyright applies to all Abstracts.) |
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| RecordInfo | BibRecord: BibEntity: Identifiers: – Type: doi Value: 10.1016/j.cis.2018.10.005 Languages: – Code: eng Text: English PhysicalDescription: Pagination: PageCount: 14 StartPage: 1 Subjects: – SubjectFull: Biofilms testing Type: general – SubjectFull: Bacterial adhesion Type: general – SubjectFull: Quorum sensing Type: general – SubjectFull: Surface properties Type: general – SubjectFull: Thermodynamics Type: general Titles: – TitleFull: Physico-chemistry from initial bacterial adhesion to surface-programmed biofilm growth. Type: main BibRelationships: HasContributorRelationships: – PersonEntity: Name: NameFull: Carniello, Vera – PersonEntity: Name: NameFull: Peterson, Brandon W. – PersonEntity: Name: NameFull: van der Mei, Henny C. – PersonEntity: Name: NameFull: Busscher, Henk J. IsPartOfRelationships: – BibEntity: Dates: – D: 01 M: 11 Text: Nov2018 Type: published Y: 2018 Identifiers: – Type: issn-print Value: 00018686 Numbering: – Type: volume Value: 261 Titles: – TitleFull: Advances in Colloid & Interface Science Type: main |
| ResultId | 1 |
