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Staphylococcus epidermidis biofilms undergo metabolic and matrix remodeling under nitrosative stress

dc.contributor.authorOliveira, Ana S.
dc.contributor.authorSaraiva, Lígia M.
dc.contributor.authorCarvalho, Sandra M.
dc.contributor.institutionInstituto de Tecnologia Química e Biológica António Xavier (ITQB)
dc.contributor.pblFrontiers Media
dc.date.accessioned2023-09-30T22:18:50Z
dc.date.available2023-09-30T22:18:50Z
dc.date.issued2023
dc.descriptionFunding Information: This work was financially supported by Fundação para a Ciência e Tecnologia (FCT) Project – PTDC/BIA-MIC/31566/2017, R&D unit MOSTMICRO-ITQB (UIDB/04612/2020 and UIDP/04612/2020) and LS4FUTURE Associated Laboratory (LA/P/0087/2020). AO has a fellowship UI/BD/153389/2022 from FCT. The NMR data were acquired from CERMAX, ITQB-NOVA, Oeiras, Portugal, with equipment funded by FCT, project AAC 01/SAICT/2016. The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. Acknowledgments Publisher Copyright: Copyright © 2023 Oliveira, Saraiva and Carvalho.
dc.description.abstractStaphylococcus epidermidis is a commensal skin bacterium that forms host- and antibiotic-resistant biofilms that are a major cause of implant-associated infections. Most research has focused on studying the responses to host-imposed stresses on planktonic bacteria. In this work, we addressed the open question of how S. epidermidis thrives on toxic concentrations of nitric oxide (NO) produced by host innate immune cells during biofilm assembly. We analyzed alterations of gene expression, metabolism, and matrix structure of biofilms of two clinical isolates of S. epidermidis, namely, 1457 and RP62A, formed under NO stress conditions. In both strains, NO lowers the amount of biofilm mass and causes increased production of lactate and decreased acetate excretion from biofilm glucose metabolism. Transcriptional analysis revealed that NO induces icaA, which is directly involved in polysaccharide intercellular adhesion (PIA) production, and genes encoding proteins of the amino sugar pathway (glmM and glmU) that link glycolysis to PIA synthesis. However, the strains seem to have distinct regulatory mechanisms to boost lactate production, as NO causes a substantial upregulation of ldh gene in strain RP62A but not in strain 1457. The analysis of the matrix components of the staphylococcal biofilms, assessed by confocal laser scanning microscopy (CLSM), showed that NO stimulates PIA and protein production and interferes with biofilm structure in a strain-dependent manner, but independently of the Ldh level. Thus, NO resistance is attained by remodeling the staphylococcal matrix architecture and adaptation of main metabolic processes, likely providing in vivo fitness of S. epidermidis biofilms contacting NO-proficient macrophages.en
dc.description.versionpublishersversion
dc.description.versionpublished
dc.format.extent8605792
dc.identifier.doi10.3389/fcimb.2023.1200923
dc.identifier.issn2235-2988
dc.identifier.otherPURE: 72373157
dc.identifier.otherPURE UUID: 7cedfb34-fcdb-416e-a404-b291ba170296
dc.identifier.otherScopus: 85165136857
dc.identifier.otherPubMed: 37469594
dc.identifier.urihttp://hdl.handle.net/10362/158524
dc.identifier.urlhttps://www.scopus.com/pages/publications/85165136857
dc.language.isoeng
dc.peerreviewedyes
dc.subjectbiofilm metabolism
dc.subjectconfocal laser scanning microscopy (CLSM)
dc.subjectnitrosative stress
dc.subjectnuclear magnetic resonance (NMR)
dc.subjectStaphylococcus epidermidis
dc.subjectMicrobiology
dc.subjectImmunology
dc.subjectMicrobiology (medical)
dc.subjectInfectious Diseases
dc.subjectSDG 3 - Good Health and Well-being
dc.titleStaphylococcus epidermidis biofilms undergo metabolic and matrix remodeling under nitrosative stressen
dc.typejournal article
degois.publication.titleFrontiers in Cellular and Infection Microbiology
degois.publication.volume13
dspace.entity.typePublication
rcaap.rightsopenAccess

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