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Zinc tolerance through glutathione import strikes a fine balance between protection and damage in Streptococcus mutans.

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Τίτλος: Zinc tolerance through glutathione import strikes a fine balance between protection and damage in Streptococcus mutans.
Συγγραφείς: Carter MC; Department of Oral Biology, College of Dentistry, University of Florida, Gainesville, FL, USA., Womack E; Department of Oral Biology, College of Dentistry, University of Florida, Gainesville, FL, USA., Khatib M; Department of Oral Biology, College of Dentistry, University of Florida, Gainesville, FL, USA., Peterson AM; Department of Oral Biology, College of Dentistry, University of Florida, Gainesville, FL, USA., Saengpet IS; Department of Oral Biology, College of Dentistry, University of Florida, Gainesville, FL, USA., Lemos JA; Department of Oral Biology, College of Dentistry, University of Florida, Gainesville, FL, USA.
Πηγή: Microbiology (Reading, England) [Microbiology (Reading)] 2026 Aug; Vol. 172 (8).
Τύπος έκδοσης: Journal Article
Γλώσσα: English
Στοιχεία περιοδικού: Publisher: Microbiology Society Country of Publication: England NLM ID: 9430468 Publication Model: Print Cited Medium: Internet ISSN: 1465-2080 (Electronic) Linking ISSN: 13500872 NLM ISO Abbreviation: Microbiology (Reading) Subsets: MEDLINE
Imprint Name(s): Publication: 2015- : London : Microbiology Society
Original Publication: Reading, U.K. : Society for General Microbiology, c1994-
Ιατρικοί όροι (MeSH): Glutathione*/metabolism , Streptococcus mutans*/metabolism , Streptococcus mutans*/genetics , Streptococcus mutans*/drug effects , Streptococcus mutans*/growth & development , Zinc*/metabolism , Zinc*/toxicity, Bacterial Proteins/genetics ; Bacterial Proteins/metabolism ; Membrane Transport Proteins/genetics ; Membrane Transport Proteins/metabolism ; Gene Expression Regulation, Bacterial ; Gene Deletion ; Stress, Physiological ; Biological Transport
Περίληψη: Recently, our group showed that the dental pathogen Streptococcus mutans is inherently more tolerant to high zinc stress than other streptococci, a phenotype associated with the presence of a P-type ATPase exporter named ZccE, virtually unique to S. mutans. In addition to zccE, a previous transcriptome analysis revealed that S. mutans upregulates genes involved in glutathione uptake during initial exposure to zinc stress. Glutathione, a major supplier of organic sulphur that also plays key roles in antioxidant defence and xenobiotic detoxification, forms coordination complexes with a variety of metals, including zinc, thereby functioning as a buffer that protects cells from metal intoxication. To investigate the contribution of glutathione zinc tolerance in S. mutans, the gshT gene, which encodes the substrate-binding subunit of a glutathione transporter, was deleted in both the parent and ΔzccE strains, and the ability of these mutants to overcome zinc stress through intracellular glutathione accumulation was determined. Targeted metabolomics revealed that S. mutans accumulates glutathione in a GshT-dependent manner following zinc stress, a response that was strikingly amplified in the ΔzccE strain. Although glutathione supplementation had a minimal impact on the growth of either parent or mutant strains in sub-inhibitory zinc concentrations, the ΔgshT strain exhibited increased zinc sensitivity in a plate-based assay. However, the ΔzccEΔgshT mutant displayed enhanced zinc tolerance compared to the ΔzccE single mutant. While glutathione alone did not alter zinc levels in the UA159 or ΔzccE strains, the combination of zinc and glutathione nearly doubled intracellular zinc levels in ΔzccE compared to cells grown in zinc only. We conclude that while glutathione may play a minor role in S. mutans zinc tolerance, enhanced glutathione uptake observed in ΔzccE facilitates zinc entry, as glutathione:Zn2+ complexes inadvertently promote zinc intoxication via a Trojan horse mechanism.
Σχόλια: Update of: bioRxiv. 2026 Jun 02:2026.06.01.728743. doi: 10.64898/2026.06.01.728743.. (PMID: 42282517)
References: Nat Rev Microbiol. 2012 Jul 16;10(8):525-37. (PMID: 22796883)
J Dent Res. 2013 Sep;92(9):819-24. (PMID: 23872989)
Mol Microbiol. 2013 Jul;89(2):288-303. (PMID: 23701283)
J Bacteriol. 2021 Mar 23;203(8):. (PMID: 33526613)
Nat Rev Microbiol. 2017 Jun;15(6):338-350. (PMID: 28344348)
Mol Oral Microbiol. 2023 Jun;38(3):198-211. (PMID: 36622758)
Trends Biochem Sci. 2019 Dec;44(12):1041-1056. (PMID: 31326221)
mBio. 2020 Dec 1;11(6):. (PMID: 33262259)
J Bacteriol. 2008 Aug;190(15):5431-8. (PMID: 18539744)
J Bacteriol. 2019 Sep 20;201(20):. (PMID: 31331978)
PLoS Pathog. 2011 Nov;7(11):e1002357. (PMID: 22072971)
J Bacteriol. 1998 Mar;180(6):1454-9. (PMID: 9515913)
Medicina (Kaunas). 2023 Nov 28;59(12):. (PMID: 38138191)
Microorganisms. 2024 Jan 07;12(1):. (PMID: 38257948)
Acta Biochim Pol. 1999;46(3):567-80. (PMID: 10698265)
PLoS Genet. 2016 Dec 9;12(12):e1006515. (PMID: 27935957)
J Bacteriol. 2022 Nov 15;204(11):e0025722. (PMID: 36286512)
J Microbiol Methods. 2015 Dec;119:134-41. (PMID: 26481669)
J Microbiol Methods. 2002 Apr;49(2):193-205. (PMID: 11830305)
Nutrients. 2017 Dec 24;10(1):. (PMID: 29295546)
J Bacteriol. 1999 Nov;181(22):6876-81. (PMID: 10559151)
mSphere. 2020 Jan 8;5(1):. (PMID: 31915219)
Nutrients. 2026 Feb 07;18(4):. (PMID: 41754074)
J Bacteriol. 2008 Jul;190(13):4632-40. (PMID: 18441055)
J Bacteriol. 1996 Apr;178(7):1990-5. (PMID: 8606174)
PLoS One. 2014 Feb 18;9(2):e89427. (PMID: 24558498)
Microbiol Spectr. 2019 Jan;7(1):. (PMID: 30657107)
BMC Public Health. 2024 Nov 21;24(1):3239. (PMID: 39574014)
Nat Rev Microbiol. 2022 Nov;20(11):657-670. (PMID: 35641670)
J Bacteriol. 1996 Apr;178(7):2131-5. (PMID: 8606194)
J Bacteriol. 2008 Aug;190(15):5439-54. (PMID: 18539742)
Methods. 2001 Dec;25(4):402-8. (PMID: 11846609)
Arch Oral Biol. 2005 Aug;50(8):747-57. (PMID: 15958206)
Mol Aspects Med. 2009 Feb-Apr;30(1-2):1-12. (PMID: 18796312)
Metallomics. 2021 Apr 30;13(5):. (PMID: 33770183)
Antioxid Redox Signal. 2006 May-Jun;8(5-6):753-62. (PMID: 16771667)
Arch Biochem Biophys. 2016 Dec 1;611:58-65. (PMID: 27021581)
Mol Oral Microbiol. 2021 Jun;36(3):214-224. (PMID: 33819383)
Pediatrics. 2008 Feb;121(2):326-36. (PMID: 18245424)
J Bacteriol. 2012 Nov;194(22):6248-54. (PMID: 22984260)
Nat Methods. 2009 May;6(5):343-5. (PMID: 19363495)
PLoS Pathog. 2022 Aug 8;18(8):e1010477. (PMID: 35939512)
J Clin Periodontol. 1975 Feb;2(1):33-43. (PMID: 1094034)
Grant Information: F31 DE032899 United States DE NIDCR NIH HHS; R01 DE032555 United States DE NIDCR NIH HHS; T90 DE021990 United States DE NIDCR NIH HHS
Contributed Indexing: Keywords: Streptococcus mutans; ZccE; glutathione; metal stress; zinc mismetallation
Substance Nomenclature: GAN16C9B8O (Glutathione)
J41CSQ7QDS (Zinc)
0 (Bacterial Proteins)
0 (glutathione transporter)
0 (Membrane Transport Proteins)
Entry Date(s): Date Created: 20260810 Date Completed: 20260810 Latest Revision: 20260826
Update Code: 20260826
PubMed Central ID: PMC13456638
DOI: 10.1099/mic.0.001754
PMID: 42574064
Βάση Δεδομένων: MEDLINE
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  Data: Zinc tolerance through glutathione import strikes a fine balance between protection and damage in Streptococcus mutans.
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  Data: Recently, our group showed that the dental pathogen Streptococcus mutans is inherently more tolerant to high zinc stress than other streptococci, a phenotype associated with the presence of a P-type ATPase exporter named ZccE, virtually unique to S. mutans. In addition to zccE, a previous transcriptome analysis revealed that S. mutans upregulates genes involved in glutathione uptake during initial exposure to zinc stress. Glutathione, a major supplier of organic sulphur that also plays key roles in antioxidant defence and xenobiotic detoxification, forms coordination complexes with a variety of metals, including zinc, thereby functioning as a buffer that protects cells from metal intoxication. To investigate the contribution of glutathione zinc tolerance in S. mutans, the gshT gene, which encodes the substrate-binding subunit of a glutathione transporter, was deleted in both the parent and ΔzccE strains, and the ability of these mutants to overcome zinc stress through intracellular glutathione accumulation was determined. Targeted metabolomics revealed that S. mutans accumulates glutathione in a GshT-dependent manner following zinc stress, a response that was strikingly amplified in the ΔzccE strain. Although glutathione supplementation had a minimal impact on the growth of either parent or mutant strains in sub-inhibitory zinc concentrations, the ΔgshT strain exhibited increased zinc sensitivity in a plate-based assay. However, the ΔzccEΔgshT mutant displayed enhanced zinc tolerance compared to the ΔzccE single mutant. While glutathione alone did not alter zinc levels in the UA159 or ΔzccE strains, the combination of zinc and glutathione nearly doubled intracellular zinc levels in ΔzccE compared to cells grown in zinc only. We conclude that while glutathione may play a minor role in S. mutans zinc tolerance, enhanced glutathione uptake observed in ΔzccE facilitates zinc entry, as glutathione:Zn<superscript>2+</superscript> complexes inadvertently promote zinc intoxication via a Trojan horse mechanism.
– Name: Comment
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  Data: Update of: bioRxiv. 2026 Jun 02:2026.06.01.728743. doi: 10.64898/2026.06.01.728743.. (PMID: <searchLink fieldCode="PM" term="%2242282517%22">42282517)</searchLink>
– Name: Ref
  Label: References
  Group: RefInfo
  Data: Nat Rev Microbiol. 2012 Jul 16;10(8):525-37. (PMID: <searchLink fieldCode="PM" term="%2222796883%22">22796883)</searchLink><br />J Dent Res. 2013 Sep;92(9):819-24. (PMID: <searchLink fieldCode="PM" term="%2223872989%22">23872989)</searchLink><br />Mol Microbiol. 2013 Jul;89(2):288-303. (PMID: <searchLink fieldCode="PM" term="%2223701283%22">23701283)</searchLink><br />J Bacteriol. 2021 Mar 23;203(8):. (PMID: <searchLink fieldCode="PM" term="%2233526613%22">33526613)</searchLink><br />Nat Rev Microbiol. 2017 Jun;15(6):338-350. (PMID: <searchLink fieldCode="PM" term="%2228344348%22">28344348)</searchLink><br />Mol Oral Microbiol. 2023 Jun;38(3):198-211. (PMID: <searchLink fieldCode="PM" term="%2236622758%22">36622758)</searchLink><br />Trends Biochem Sci. 2019 Dec;44(12):1041-1056. (PMID: <searchLink fieldCode="PM" term="%2231326221%22">31326221)</searchLink><br />mBio. 2020 Dec 1;11(6):. (PMID: <searchLink fieldCode="PM" term="%2233262259%22">33262259)</searchLink><br />J Bacteriol. 2008 Aug;190(15):5431-8. (PMID: <searchLink fieldCode="PM" term="%2218539744%22">18539744)</searchLink><br />J Bacteriol. 2019 Sep 20;201(20):. (PMID: <searchLink fieldCode="PM" term="%2231331978%22">31331978)</searchLink><br />PLoS Pathog. 2011 Nov;7(11):e1002357. (PMID: <searchLink fieldCode="PM" term="%2222072971%22">22072971)</searchLink><br />J Bacteriol. 1998 Mar;180(6):1454-9. (PMID: <searchLink fieldCode="PM" term="%229515913%22">9515913)</searchLink><br />Medicina (Kaunas). 2023 Nov 28;59(12):. (PMID: <searchLink fieldCode="PM" term="%2238138191%22">38138191)</searchLink><br />Microorganisms. 2024 Jan 07;12(1):. (PMID: <searchLink fieldCode="PM" term="%2238257948%22">38257948)</searchLink><br />Acta Biochim Pol. 1999;46(3):567-80. (PMID: <searchLink fieldCode="PM" term="%2210698265%22">10698265)</searchLink><br />PLoS Genet. 2016 Dec 9;12(12):e1006515. (PMID: <searchLink fieldCode="PM" term="%2227935957%22">27935957)</searchLink><br />J Bacteriol. 2022 Nov 15;204(11):e0025722. (PMID: <searchLink fieldCode="PM" term="%2236286512%22">36286512)</searchLink><br />J Microbiol Methods. 2015 Dec;119:134-41. (PMID: <searchLink fieldCode="PM" term="%2226481669%22">26481669)</searchLink><br />J Microbiol Methods. 2002 Apr;49(2):193-205. (PMID: <searchLink fieldCode="PM" term="%2211830305%22">11830305)</searchLink><br />Nutrients. 2017 Dec 24;10(1):. (PMID: <searchLink fieldCode="PM" term="%2229295546%22">29295546)</searchLink><br />J Bacteriol. 1999 Nov;181(22):6876-81. (PMID: <searchLink fieldCode="PM" term="%2210559151%22">10559151)</searchLink><br />mSphere. 2020 Jan 8;5(1):. (PMID: <searchLink fieldCode="PM" term="%2231915219%22">31915219)</searchLink><br />Nutrients. 2026 Feb 07;18(4):. (PMID: <searchLink fieldCode="PM" term="%2241754074%22">41754074)</searchLink><br />J Bacteriol. 2008 Jul;190(13):4632-40. (PMID: <searchLink fieldCode="PM" term="%2218441055%22">18441055)</searchLink><br />J Bacteriol. 1996 Apr;178(7):1990-5. (PMID: <searchLink fieldCode="PM" term="%228606174%22">8606174)</searchLink><br />PLoS One. 2014 Feb 18;9(2):e89427. (PMID: <searchLink fieldCode="PM" term="%2224558498%22">24558498)</searchLink><br />Microbiol Spectr. 2019 Jan;7(1):. (PMID: <searchLink fieldCode="PM" term="%2230657107%22">30657107)</searchLink><br />BMC Public Health. 2024 Nov 21;24(1):3239. (PMID: <searchLink fieldCode="PM" term="%2239574014%22">39574014)</searchLink><br />Nat Rev Microbiol. 2022 Nov;20(11):657-670. (PMID: <searchLink fieldCode="PM" term="%2235641670%22">35641670)</searchLink><br />J Bacteriol. 1996 Apr;178(7):2131-5. (PMID: <searchLink fieldCode="PM" term="%228606194%22">8606194)</searchLink><br />J Bacteriol. 2008 Aug;190(15):5439-54. (PMID: <searchLink fieldCode="PM" term="%2218539742%22">18539742)</searchLink><br />Methods. 2001 Dec;25(4):402-8. (PMID: <searchLink fieldCode="PM" term="%2211846609%22">11846609)</searchLink><br />Arch Oral Biol. 2005 Aug;50(8):747-57. (PMID: <searchLink fieldCode="PM" term="%2215958206%22">15958206)</searchLink><br />Mol Aspects Med. 2009 Feb-Apr;30(1-2):1-12. (PMID: <searchLink fieldCode="PM" term="%2218796312%22">18796312)</searchLink><br />Metallomics. 2021 Apr 30;13(5):. (PMID: <searchLink fieldCode="PM" term="%2233770183%22">33770183)</searchLink><br />Antioxid Redox Signal. 2006 May-Jun;8(5-6):753-62. (PMID: <searchLink fieldCode="PM" term="%2216771667%22">16771667)</searchLink><br />Arch Biochem Biophys. 2016 Dec 1;611:58-65. (PMID: <searchLink fieldCode="PM" term="%2227021581%22">27021581)</searchLink><br />Mol Oral Microbiol. 2021 Jun;36(3):214-224. (PMID: <searchLink fieldCode="PM" term="%2233819383%22">33819383)</searchLink><br />Pediatrics. 2008 Feb;121(2):326-36. (PMID: <searchLink fieldCode="PM" term="%2218245424%22">18245424)</searchLink><br />J Bacteriol. 2012 Nov;194(22):6248-54. (PMID: <searchLink fieldCode="PM" term="%2222984260%22">22984260)</searchLink><br />Nat Methods. 2009 May;6(5):343-5. (PMID: <searchLink fieldCode="PM" term="%2219363495%22">19363495)</searchLink><br />PLoS Pathog. 2022 Aug 8;18(8):e1010477. (PMID: <searchLink fieldCode="PM" term="%2235939512%22">35939512)</searchLink><br />J Clin Periodontol. 1975 Feb;2(1):33-43. (PMID: <searchLink fieldCode="PM" term="%221094034%22">1094034)</searchLink>
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  Data: <i>Keywords: </i>Streptococcus mutans; ZccE; glutathione; metal stress; zinc mismetallation
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        Text: English
    Subjects:
      – SubjectFull: Bacterial Proteins genetics
        Type: general
      – SubjectFull: Bacterial Proteins metabolism
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      – SubjectFull: Membrane Transport Proteins genetics
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      – SubjectFull: Membrane Transport Proteins metabolism
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      – SubjectFull: Glutathione metabolism
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      – SubjectFull: Streptococcus mutans metabolism
        Type: general
      – SubjectFull: Streptococcus mutans genetics
        Type: general
      – SubjectFull: Streptococcus mutans drug effects
        Type: general
      – SubjectFull: Streptococcus mutans growth & development
        Type: general
      – SubjectFull: Zinc metabolism
        Type: general
      – SubjectFull: Zinc toxicity
        Type: general
    Titles:
      – TitleFull: Zinc tolerance through glutathione import strikes a fine balance between protection and damage in Streptococcus mutans.
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      – PersonEntity:
          Name:
            NameFull: Peterson AM
      – PersonEntity:
          Name:
            NameFull: Saengpet IS
      – PersonEntity:
          Name:
            NameFull: Lemos JA
    IsPartOfRelationships:
      – BibEntity:
          Dates:
            – D: 01
              M: 08
              Text: 2026 Aug
              Type: published
              Y: 2026
          Identifiers:
            – Type: issn-electronic
              Value: 1465-2080
          Numbering:
            – Type: volume
              Value: 172
            – Type: issue
              Value: 8
          Titles:
            – TitleFull: Microbiology (Reading, England)
              Type: main
ResultId 1