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Quorum sensing rewires membrane vesicle protein cargo to promote antibiotic persistence in Streptococcus mutans.

Λεπτομέρειες βιβλιογραφικής εγγραφής
Τίτλος: Quorum sensing rewires membrane vesicle protein cargo to promote antibiotic persistence in Streptococcus mutans.
Συγγραφείς: Dufour D; Faculty of Dentistry, University of Toronto, Toronto, Ontario, Canada., Leiva-Sabadini C; Institute for Biological and Medical Engineering, Pontificia Universidad Católica de Chile, Santiago, Chile., Aguayo S; Institute for Biological and Medical Engineering, Pontificia Universidad Católica de Chile, Santiago, Chile.; School of Dentistry, Faculty of Medicine, Pontificia Universidad Católica de Chile, Santiago, Chile., Lévesque CM; Faculty of Dentistry, University of Toronto, Toronto, Ontario, Canada.
Πηγή: Journal of bacteriology [J Bacteriol] 2026 Aug 20; Vol. 208 (8), pp. e0032326. Date of Electronic Publication: 2026 Jul 14.
Τύπος έκδοσης: Journal Article
Γλώσσα: English
Στοιχεία περιοδικού: Publisher: American Society for Microbiology Country of Publication: United States NLM ID: 2985120R Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1098-5530 (Electronic) Linking ISSN: 00219193 NLM ISO Abbreviation: J Bacteriol Subsets: MEDLINE
Imprint Name(s): Original Publication: Washington, DC : American Society for Microbiology
Ιατρικοί όροι (MeSH): Quorum Sensing*/physiology , Streptococcus mutans*/drug effects , Streptococcus mutans*/physiology , Streptococcus mutans*/genetics , Streptococcus mutans*/metabolism , Anti-Bacterial Agents*/pharmacology , Bacterial Proteins*/metabolism , Bacterial Proteins*/genetics , Membrane Proteins*/metabolism
Περίληψη: Quorum sensing (QS) plays a central role in the adaptive biology of Streptococcus mutans, yet the extent to which competence-stimulating peptide (CSP) signaling intersects with membrane vesicle production and function remained unclear. In this study, CSP activation markedly increased membrane vesicle output during the stationary phase and drove extensive changes in vesicle protein composition. Proteomic analysis revealed broad remodeling of vesicle cargo, including shifts in subcellular origin, and enrichment of multiple functional protein classes. Notably, CSP-induced vesicles carried the persistence-associated peptide Pep299, suggesting a link between QS-dependent cargo loading and antibiotic survival. To examine the functional consequences of this remodeling, S. mutans cells were pre-exposed to vesicles prior to antibiotic challenge. Vesicles derived from CSP-induced cultures promoted persister formation in a concentration-dependent manner, whereas vesicles from non-induced cultures exhibited minimal activity. Wild-type vesicles increased persistence, and vesicles from Pep299-overexpressing cells further enhanced this phenotype at lower vesicle concentrations. In contrast, vesicles derived from a Δ299 mutant failed to promote persistence, demonstrating that Pep299 is a key determinant of this activity. At higher vesicle abundance, the responses of wild-type and Pep299-enriched vesicles converged, consistent with endogenous CSP-dependent Pep299 loading. Fusion assays using R18 dequenching showed that vesicles from wild-type, Pep299-overexpressing, and Δ299 strains fused with comparable efficiency, indicating that differences in persistence arise from cargo composition rather than altered delivery efficiency. Together, these findings reveal that CSP QS coordinates biogenesis and selective cargo remodeling in S. mutans and identify Pep299-containing vesicles as a quorum-regulated mechanism promoting antibiotic persistence.IMPORTANCEQuorum sensing enables bacterial populations to coordinate adaptive behaviors, yet its influence on membrane vesicle biology is not fully understood. This study shows that competence-stimulating peptide (CSP) signaling in Streptococcus mutans not only increases vesicle production but also remodels vesicle protein cargo, including enrichment of the persistence-associated peptide Pep299. CSP-induced vesicles enhance the formation of persister cells through a cargo-dependent mechanism rather than through changes in vesicle-cell fusion. These findings uncover a previously unrecognized connection between quorum sensing and vesicle-mediated persistence and reveal a strategy through which S. mutans modulates community behavior and resilience within the oral biofilm environment.
Competing Interests: The authors declare no conflict of interest.
Σχόλια: Erratum in: J Bacteriol. 2026 Sep 18:e0046826. doi: 10.1128/jb.00468-26.. (PMID: 42757964)
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Microbiologyopen. 2025 Mar;14(1):e70016. (PMID: 40159675)
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Bioinformatics. 2010 Jul 1;26(13):1608-15. (PMID: 20472543)
Protein Sci. 2022 Jan;31(1):47-53. (PMID: 34423492)
J Extracell Vesicles. 2022 Apr;11(4):e12212. (PMID: 35384360)
J Bacteriol. 2005 Jul;187(13):4451-6. (PMID: 15968054)
J Bacteriol. 2009 May;191(9):2973-84. (PMID: 19251860)
Nat Rev Microbiol. 2019 Jul;17(7):441-448. (PMID: 30980069)
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Biofilm. 2024 Jul 25;8:100216. (PMID: 39184814)
J Bacteriol. 2018 Dec 7;201(1):. (PMID: 30322852)
Infect Immun. 2020 Nov 16;88(12):. (PMID: 32989035)
Nat Commun. 2026 Apr 16;17(1):. (PMID: 41991528)
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FEMS Microbiol Lett. 2006 Feb;255(2):240-6. (PMID: 16448501)
J Bacteriol. 2025 Sep 18;207(9):e0010025. (PMID: 40788091)
Mol Cell Proteomics. 2011 Sep;10(9):M111.011015. (PMID: 21642640)
Front Microbiol. 2015 Oct 23;6:1176. (PMID: 26557114)
ISME J. 2023 Sep;17(9):1430-1444. (PMID: 37355741)
Annu Rev Cell Dev Biol. 2005;21:319-46. (PMID: 16212498)
mBio. 2018 May 22;9(3):. (PMID: 29789364)
J Bacteriol. 2012 May;194(9):2265-74. (PMID: 22366415)
Appl Microbiol Biotechnol. 2020 Nov;104(22):9733-9748. (PMID: 33064184)
Mol Oral Microbiol. 2021 Feb;36(1):12-24. (PMID: 33040492)
Int J Mol Sci. 2025 May 23;26(11):. (PMID: 40507835)
PLoS Pathog. 2021 May 13;17(5):e1009508. (PMID: 33984071)
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Arch Microbiol. 2026 Feb 02;208(4):157. (PMID: 41627464)
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Microorganisms. 2026 Mar 18;14(3):. (PMID: 41900446)
Nat Rev Microbiol. 2019 Jan;17(1):13-24. (PMID: 30397270)
Biochemistry. 1984 Nov 20;23(24):5675-81. (PMID: 6098295)
J Bacteriol. 1970 Oct;104(1):313-22. (PMID: 5473898)
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Annu Rev Genet. 2009;43:197-222. (PMID: 19686078)
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Grant Information: RGPIN-2019-06454 Natural Sciences and Engineering Research Council of Canada
Contributed Indexing: Keywords: Streptococcus mutans; antibiotic tolerance; membrane vesicles; peptide signaling; persister cells; quorum sensing
Substance Nomenclature: 0 (Anti-Bacterial Agents)
0 (Bacterial Proteins)
0 (Membrane Proteins)
0 (competence factor, Streptococcus)
Entry Date(s): Date Created: 20260714 Date Completed: 20260820 Latest Revision: 20260918
Update Code: 20260918
PubMed Central ID: PMC13492114
DOI: 10.1128/jb.00323-26
PMID: 42447300
Βάση Δεδομένων: MEDLINE
FullText Text:
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DbLabel: MEDLINE
An: 42447300
AccessLevel: 3
PubType: Academic Journal
PubTypeId: academicJournal
PreciseRelevancyScore: 0
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  Data: Quorum sensing rewires membrane vesicle protein cargo to promote antibiotic persistence in Streptococcus mutans.
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  Data: <searchLink fieldCode="AU" term="%22Dufour+D%22">Dufour D</searchLink>; Faculty of Dentistry, University of Toronto, Toronto, Ontario, Canada.<br /><searchLink fieldCode="AU" term="%22Leiva-Sabadini+C%22">Leiva-Sabadini C</searchLink>; Institute for Biological and Medical Engineering, Pontificia Universidad Católica de Chile, Santiago, Chile.<br /><searchLink fieldCode="AU" term="%22Aguayo+S%22">Aguayo S</searchLink>; Institute for Biological and Medical Engineering, Pontificia Universidad Católica de Chile, Santiago, Chile.; School of Dentistry, Faculty of Medicine, Pontificia Universidad Católica de Chile, Santiago, Chile.<br /><searchLink fieldCode="AU" term="%22Lévesque+CM%22">Lévesque CM</searchLink>; Faculty of Dentistry, University of Toronto, Toronto, Ontario, Canada.
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  Data: <searchLink fieldCode="JN" term="%222985120R%22">Journal of bacteriology</searchLink> [J Bacteriol] 2026 Aug 20; Vol. 208 (8), pp. e0032326. <i>Date of Electronic Publication: </i>2026 Jul 14.
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  Data: <i>Publisher: </i><searchLink fieldCode="PB" term="%22American+Society+for+Microbiology%22">American Society for Microbiology </searchLink><i>Country of Publication: </i>United States <i>NLM ID: </i>2985120R <i>Publication Model: </i>Print-Electronic <i>Cited Medium: </i>Internet <i>ISSN: </i>1098-5530 (Electronic) <i>Linking ISSN: </i><searchLink fieldCode="IS" term="%2200219193%22">00219193 </searchLink><i>NLM ISO Abbreviation: </i>J Bacteriol <i>Subsets: </i>MEDLINE
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  Data: <i>Original Publication</i>: Washington, DC : American Society for Microbiology
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  Data: <searchLink fieldCode="MM" term="%22Quorum+Sensing%22">Quorum Sensing*</searchLink>/<searchLink fieldCode="MM" term="%22Quorum+Sensing+physiology%22">physiology</searchLink> <br /><searchLink fieldCode="MM" term="%22Streptococcus+mutans%22">Streptococcus mutans*</searchLink>/<searchLink fieldCode="MM" term="%22Streptococcus+mutans+drug+effects%22">drug effects</searchLink> <br /><searchLink fieldCode="MM" term="%22Streptococcus+mutans%22">Streptococcus mutans*</searchLink>/<searchLink fieldCode="MM" term="%22Streptococcus+mutans+physiology%22">physiology</searchLink> <br /><searchLink fieldCode="MM" term="%22Streptococcus+mutans%22">Streptococcus mutans*</searchLink>/<searchLink fieldCode="MM" term="%22Streptococcus+mutans+genetics%22">genetics</searchLink> <br /><searchLink fieldCode="MM" term="%22Streptococcus+mutans%22">Streptococcus mutans*</searchLink>/<searchLink fieldCode="MM" term="%22Streptococcus+mutans+metabolism%22">metabolism</searchLink> <br /><searchLink fieldCode="MM" term="%22Anti-Bacterial+Agents%22">Anti-Bacterial Agents*</searchLink>/<searchLink fieldCode="MM" term="%22Anti-Bacterial+Agents+pharmacology%22">pharmacology</searchLink> <br /><searchLink fieldCode="MM" term="%22Bacterial+Proteins%22">Bacterial Proteins*</searchLink>/<searchLink fieldCode="MM" term="%22Bacterial+Proteins+metabolism%22">metabolism</searchLink> <br /><searchLink fieldCode="MM" term="%22Bacterial+Proteins%22">Bacterial Proteins*</searchLink>/<searchLink fieldCode="MM" term="%22Bacterial+Proteins+genetics%22">genetics</searchLink> <br /><searchLink fieldCode="MM" term="%22Membrane+Proteins%22">Membrane Proteins*</searchLink>/<searchLink fieldCode="MM" term="%22Membrane+Proteins+metabolism%22">metabolism</searchLink>
– Name: Abstract
  Label: Abstract
  Group: Ab
  Data: Quorum sensing (QS) plays a central role in the adaptive biology of Streptococcus mutans, yet the extent to which competence-stimulating peptide (CSP) signaling intersects with membrane vesicle production and function remained unclear. In this study, CSP activation markedly increased membrane vesicle output during the stationary phase and drove extensive changes in vesicle protein composition. Proteomic analysis revealed broad remodeling of vesicle cargo, including shifts in subcellular origin, and enrichment of multiple functional protein classes. Notably, CSP-induced vesicles carried the persistence-associated peptide Pep299, suggesting a link between QS-dependent cargo loading and antibiotic survival. To examine the functional consequences of this remodeling, S. mutans cells were pre-exposed to vesicles prior to antibiotic challenge. Vesicles derived from CSP-induced cultures promoted persister formation in a concentration-dependent manner, whereas vesicles from non-induced cultures exhibited minimal activity. Wild-type vesicles increased persistence, and vesicles from Pep299-overexpressing cells further enhanced this phenotype at lower vesicle concentrations. In contrast, vesicles derived from a Δ299 mutant failed to promote persistence, demonstrating that Pep299 is a key determinant of this activity. At higher vesicle abundance, the responses of wild-type and Pep299-enriched vesicles converged, consistent with endogenous CSP-dependent Pep299 loading. Fusion assays using R18 dequenching showed that vesicles from wild-type, Pep299-overexpressing, and Δ299 strains fused with comparable efficiency, indicating that differences in persistence arise from cargo composition rather than altered delivery efficiency. Together, these findings reveal that CSP QS coordinates biogenesis and selective cargo remodeling in S. mutans and identify Pep299-containing vesicles as a quorum-regulated mechanism promoting antibiotic persistence.IMPORTANCEQuorum sensing enables bacterial populations to coordinate adaptive behaviors, yet its influence on membrane vesicle biology is not fully understood. This study shows that competence-stimulating peptide (CSP) signaling in Streptococcus mutans not only increases vesicle production but also remodels vesicle protein cargo, including enrichment of the persistence-associated peptide Pep299. CSP-induced vesicles enhance the formation of persister cells through a cargo-dependent mechanism rather than through changes in vesicle-cell fusion. These findings uncover a previously unrecognized connection between quorum sensing and vesicle-mediated persistence and reveal a strategy through which S. mutans modulates community behavior and resilience within the oral biofilm environment.
– Name: Abstract
  Label: Competing Interests
  Group: Ab
  Data: The authors declare no conflict of interest.
– Name: Comment
  Label: Comments
  Group: Commnt
  Data: Erratum in: J Bacteriol. 2026 Sep 18:e0046826. doi: 10.1128/jb.00468-26.. (PMID: <searchLink fieldCode="PM" term="%2242757964%22">42757964)</searchLink>
– Name: Ref
  Label: References
  Group: RefInfo
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(PMID: <searchLink fieldCode="PM" term="%2230397270%22">30397270)</searchLink><br />Biochemistry. 1984 Nov 20;23(24):5675-81. (PMID: <searchLink fieldCode="PM" term="%226098295%22">6098295)</searchLink><br />J Bacteriol. 1970 Oct;104(1):313-22. (PMID: <searchLink fieldCode="PM" term="%225473898%22">5473898)</searchLink><br />Front Microbiol. 2020 Dec 09;11:600221. (PMID: <searchLink fieldCode="PM" term="%2233362747%22">33362747)</searchLink><br />Annu Rev Genet. 2009;43:197-222. (PMID: <searchLink fieldCode="PM" term="%2219686078%22">19686078)</searchLink><br />Microbiol Mol Biol Rev. 2016 Jul 27;80(3):837-90. (PMID: <searchLink fieldCode="PM" term="%2227466284%22">27466284)</searchLink><br />Mol Oral Microbiol. 2012 Apr;27(2):57-69. (PMID: <searchLink fieldCode="PM" term="%2222394465%22">22394465)</searchLink><br />J Bacteriol. 2001 Apr;183(8):2543-52. (PMID: <searchLink fieldCode="PM" term="%2211274114%22">11274114)</searchLink><br />Mol Oral Microbiol. 2026 Jun;41(3):145-157. (PMID: <searchLink fieldCode="PM" term="%2241718018%22">41718018)</searchLink><br />Database (Oxford). 2009;2009:bap021. (PMID: <searchLink fieldCode="PM" term="%2220157493%22">20157493)</searchLink><br />Genes (Basel). 2022 Aug 12;13(8):. (PMID: <searchLink fieldCode="PM" term="%2236011345%22">36011345)</searchLink><br />Microbiol Mol Biol Rev. 2024 Sep 26;88(3):e0003724. (PMID: <searchLink fieldCode="PM" term="%2238869292%22">38869292)</searchLink><br />Crit Rev Microbiol. 2016 May;42(3):339-51. (PMID: <searchLink fieldCode="PM" term="%2225198780%22">25198780)</searchLink><br />Mol Oral Microbiol. 2023 Feb;38(1):1-8. (PMID: <searchLink fieldCode="PM" term="%2236088636%22">36088636)</searchLink><br />Front Microbiol. 2025 Oct 10;16:1656926. (PMID: <searchLink fieldCode="PM" term="%2241140391%22">41140391)</searchLink><br />FEMS Microbiol Lett. 2016 Jun;363(11):. 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  Data: <i>Keywords: </i>Streptococcus mutans; antibiotic tolerance; membrane vesicles; peptide signaling; persister cells; quorum sensing
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        Value: 10.1128/jb.00323-26
    Languages:
      – Code: eng
        Text: English
    PhysicalDescription:
      Pagination:
        StartPage: e0032326
    Subjects:
      – SubjectFull: Quorum Sensing physiology
        Type: general
      – SubjectFull: Streptococcus mutans drug effects
        Type: general
      – SubjectFull: Streptococcus mutans physiology
        Type: general
      – SubjectFull: Streptococcus mutans genetics
        Type: general
      – SubjectFull: Streptococcus mutans metabolism
        Type: general
      – SubjectFull: Anti-Bacterial Agents pharmacology
        Type: general
      – SubjectFull: Bacterial Proteins metabolism
        Type: general
      – SubjectFull: Bacterial Proteins genetics
        Type: general
      – SubjectFull: Membrane Proteins metabolism
        Type: general
    Titles:
      – TitleFull: Quorum sensing rewires membrane vesicle protein cargo to promote antibiotic persistence in Streptococcus mutans.
        Type: main
  BibRelationships:
    HasContributorRelationships:
      – PersonEntity:
          Name:
            NameFull: Dufour D
      – PersonEntity:
          Name:
            NameFull: Leiva-Sabadini C
      – PersonEntity:
          Name:
            NameFull: Aguayo S
      – PersonEntity:
          Name:
            NameFull: Lévesque CM
    IsPartOfRelationships:
      – BibEntity:
          Dates:
            – D: 20
              M: 08
              Text: 2026 Aug 20
              Type: published
              Y: 2026
          Identifiers:
            – Type: issn-electronic
              Value: 1098-5530
          Numbering:
            – Type: volume
              Value: 208
            – Type: issue
              Value: 8
          Titles:
            – TitleFull: Journal of bacteriology
              Type: main
ResultId 1