Low Concentrations of Vitamin C Reduce the Synthesis of Extracellular Polymers and Destabilize Bacterial Biofilms

Handle URI:
http://hdl.handle.net/10754/626444
Title:
Low Concentrations of Vitamin C Reduce the Synthesis of Extracellular Polymers and Destabilize Bacterial Biofilms
Authors:
Pandit, Santosh; Ravikumar, Vaishnavi; Abdel-Haleem, Alyaa M.; Derouiche, Abderahmane; Mokkapati, V. R. S. S.; Sihlbom, Carina; Mineta, Katsuhiko ( 0000-0002-4727-045X ) ; Gojobori, Takashi ( 0000-0001-7850-1743 ) ; Gao, Xin ( 0000-0002-7108-3574 ) ; Westerlund, Fredrik; Mijakovic, Ivan
Abstract:
Extracellular polymeric substances (EPS) produced by bacteria form a matrix supporting the complex three-dimensional architecture of biofilms. This EPS matrix is primarily composed of polysaccharides, proteins and extracellular DNA. In addition to supporting the community structure, the EPS matrix protects bacterial biofilms from the environment. Specifically, it shields the bacterial cells inside the biofilm, by preventing antimicrobial agents from getting in contact with them, thereby reducing their killing effect. New strategies for disrupting the formation of the EPS matrix can therefore lead to a more efficient use of existing antimicrobials. Here we examined the mechanism of the known effect of vitamin C (sodium ascorbate) on enhancing the activity of various antibacterial agents. Our quantitative proteomics analysis shows that non-lethal concentrations of vitamin C inhibit bacterial quorum sensing and other regulatory mechanisms underpinning biofilm development. As a result, the EPS biosynthesis in reduced, and especially the polysaccharide component of the matrix is depleted. Once the EPS content is reduced beyond a critical point, bacterial cells get fully exposed to the medium. At this stage, the cells are more susceptible to killing, either by vitamin C-induced oxidative stress as reported here, or by other antimicrobials or treatments.
KAUST Department:
Biological and Environmental Sciences and Engineering (BESE) Division; Computational Bioscience Research Center (CBRC)
Citation:
Pandit S, Ravikumar V, Abdel-Haleem AM, Derouiche A, Mokkapati VRSS, et al. (2017) Low Concentrations of Vitamin C Reduce the Synthesis of Extracellular Polymers and Destabilize Bacterial Biofilms. Frontiers in Microbiology 8. Available: http://dx.doi.org/10.3389/fmicb.2017.02599.
Publisher:
Frontiers Media SA
Journal:
Frontiers in Microbiology
Issue Date:
26-Dec-2017
DOI:
10.3389/fmicb.2017.02599
Type:
Article
ISSN:
1664-302X
Sponsors:
This work was funded by grants from the Chalmers University of Technology and VINNOVA to IM and FW, and ÅForsk to IM.
Additional Links:
https://www.frontiersin.org/articles/10.3389/fmicb.2017.02599/full
Appears in Collections:
Articles; Computational Bioscience Research Center (CBRC); Biological and Environmental Sciences and Engineering (BESE) Division

Full metadata record

DC FieldValue Language
dc.contributor.authorPandit, Santoshen
dc.contributor.authorRavikumar, Vaishnavien
dc.contributor.authorAbdel-Haleem, Alyaa M.en
dc.contributor.authorDerouiche, Abderahmaneen
dc.contributor.authorMokkapati, V. R. S. S.en
dc.contributor.authorSihlbom, Carinaen
dc.contributor.authorMineta, Katsuhikoen
dc.contributor.authorGojobori, Takashien
dc.contributor.authorGao, Xinen
dc.contributor.authorWesterlund, Fredriken
dc.contributor.authorMijakovic, Ivanen
dc.date.accessioned2017-12-27T13:11:16Z-
dc.date.available2017-12-27T13:11:16Z-
dc.date.issued2017-12-26en
dc.identifier.citationPandit S, Ravikumar V, Abdel-Haleem AM, Derouiche A, Mokkapati VRSS, et al. (2017) Low Concentrations of Vitamin C Reduce the Synthesis of Extracellular Polymers and Destabilize Bacterial Biofilms. Frontiers in Microbiology 8. Available: http://dx.doi.org/10.3389/fmicb.2017.02599.en
dc.identifier.issn1664-302Xen
dc.identifier.doi10.3389/fmicb.2017.02599en
dc.identifier.urihttp://hdl.handle.net/10754/626444-
dc.description.abstractExtracellular polymeric substances (EPS) produced by bacteria form a matrix supporting the complex three-dimensional architecture of biofilms. This EPS matrix is primarily composed of polysaccharides, proteins and extracellular DNA. In addition to supporting the community structure, the EPS matrix protects bacterial biofilms from the environment. Specifically, it shields the bacterial cells inside the biofilm, by preventing antimicrobial agents from getting in contact with them, thereby reducing their killing effect. New strategies for disrupting the formation of the EPS matrix can therefore lead to a more efficient use of existing antimicrobials. Here we examined the mechanism of the known effect of vitamin C (sodium ascorbate) on enhancing the activity of various antibacterial agents. Our quantitative proteomics analysis shows that non-lethal concentrations of vitamin C inhibit bacterial quorum sensing and other regulatory mechanisms underpinning biofilm development. As a result, the EPS biosynthesis in reduced, and especially the polysaccharide component of the matrix is depleted. Once the EPS content is reduced beyond a critical point, bacterial cells get fully exposed to the medium. At this stage, the cells are more susceptible to killing, either by vitamin C-induced oxidative stress as reported here, or by other antimicrobials or treatments.en
dc.description.sponsorshipThis work was funded by grants from the Chalmers University of Technology and VINNOVA to IM and FW, and ÅForsk to IM.en
dc.publisherFrontiers Media SAen
dc.relation.urlhttps://www.frontiersin.org/articles/10.3389/fmicb.2017.02599/fullen
dc.rightsThis is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.en
dc.rights.urihttp://creativecommons.org/licenses/by/4.0/en
dc.titleLow Concentrations of Vitamin C Reduce the Synthesis of Extracellular Polymers and Destabilize Bacterial Biofilmsen
dc.typeArticleen
dc.contributor.departmentBiological and Environmental Sciences and Engineering (BESE) Divisionen
dc.contributor.departmentComputational Bioscience Research Center (CBRC)en
dc.identifier.journalFrontiers in Microbiologyen
dc.eprint.versionPublisher's Version/PDFen
dc.contributor.institutionSystems and Synthetic Biology Division, Department of Biology and Biological Engineering, Chalmers University of Technology, Gothenburg, Swedenen
dc.contributor.institutionProteomics Core Facility, Sahlgrenska Academy, University of Gothenburg, Gothenburg, Swedenen
dc.contributor.institutionNovo Nordisk Foundation Center for Biosustainability, Technical University of Denmark, Kongens Lyngby, Denmarken
kaust.authorAbdel-Haleem, Alyaa M.en
kaust.authorMineta, Katsuhikoen
kaust.authorGojobori, Takashien
kaust.authorGao, Xinen
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