1887

Abstract

The cariogenic bacterium has two paralogues of the YidC/Oxa1/Alb3 family of membrane protein insertases/chaperones. Disruption of results in loss of genetic competence, decreased membrane-associated ATPase activity and stress sensitivity (acid, osmotic and oxidative). Elimination of has less severe effects, with little observable effect on growth or stress sensitivity. To examine the respective roles of YidC1 and YidC2, a conditional expression system was developed allowing simultaneous elimination of both endogenous YidCs. The function of the YidC C-terminal tails was also investigated and a chimeric YidC1 protein appended with the C terminus of YidC2 enabled YidC1 to complement a Δ mutant for stress tolerance, ATP hydrolysis activity and extracellular glyceraldehyde-3-phosphate dehydrogenase (GAPDH) activity. Elimination of or affected levels of extracellular proteins, including GtfB, GtfC and adhesin P1 (AgI/II, PAc), which were increased without YidC1 but decreased in the absence of YidC2. Both and were shown to contribute to biofilm formation and to cariogenicity in a rat model. Collectively, these results provide evidence that YidC1 and YidC2 contribute to cell surface biogenesis and protein secretion in and that differences in stress sensitivity between the Δ and Δ mutants stem from a functional difference in the C-termini of these two proteins.

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2012-07-01
2019-10-20
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References

  1. Banas J. A., Vickerman M. M.. ( 2003;). Glucan-binding proteins of the oral streptococci. . Crit Rev Oral Biol Med 14:, 89–99. [CrossRef][PubMed]
    [Google Scholar]
  2. Belli W. A., Marquis R. E.. ( 1991;). Adaptation of Streptococcus mutans and Enterococcus hirae to acid stress in continuous culture. . Appl Environ Microbiol 57:, 1134–1138.[PubMed]
    [Google Scholar]
  3. Biswas S., Biswas I.. ( 2005;). Role of HtrA in surface protein expression and biofilm formation by Streptococcus mutans. . Infect Immun 73:, 6923–6934. [CrossRef][PubMed]
    [Google Scholar]
  4. Bonnefoy N., Fiumera H. L., Dujardin G., Fox T. D.. ( 2009;). Roles of Oxa1-related inner-membrane translocases in assembly of respiratory chain complexes. . Biochim Biophys Acta 1793:, 60–70. [CrossRef][PubMed]
    [Google Scholar]
  5. Brady L. J., Piacentini D. A., Crowley P. J., Oyston P. C., Bleiweis A. S.. ( 1992;). Differentiation of salivary agglutinin-mediated adherence and aggregation of mutans streptococci by use of monoclonal antibodies against the major surface adhesin P1. . Infect Immun 60:, 1008–1017.[PubMed]
    [Google Scholar]
  6. Buckley N. D., Lee L. N., LeBlanc D. J.. ( 1995;). Use of a novel mobilizable vector to inactivate the scrA gene of Streptococcus sobrinus by allelic replacement. . J Bacteriol 177:, 5028–5034.[PubMed]
    [Google Scholar]
  7. Crowley P. J., Brady L. J., Michalek S. M., Bleiweis A. S.. ( 1999;). Virulence of a spaP mutant of Streptococcus mutans in a gnotobiotic rat model. . Infect Immun 67:, 1201–1206.[PubMed]
    [Google Scholar]
  8. Crowley P. J., Svensäter G., Snoep J. L., Bleiweis A. S., Brady L. J.. ( 2004;). An ffh mutant of Streptococcus mutans is viable and able to physiologically adapt to low pH in continuous culture. . FEMS Microbiol Lett 234:, 315–324. [CrossRef][PubMed]
    [Google Scholar]
  9. Dong Y., Palmer S. R., Hasona A., Nagamori S., Kaback H. R., Dalbey R. E., Brady L. J.. ( 2008;). Functional overlap but lack of complete cross-complementation of Streptococcus mutans and Escherichia coli YidC orthologs. . J Bacteriol 190:, 2458–2469. [CrossRef][PubMed]
    [Google Scholar]
  10. Funes S., Hasona A., Bauerschmitt H., Grubbauer C., Kauff F., Collins R., Crowley P. J., Palmer S. R., Brady L. J., Herrmann J. M.. ( 2009;). Independent gene duplications of the YidC/Oxa/Alb3 family enabled a specialized cotranslational function. . Proc Natl Acad Sci U S A 106:, 6656–6661. [CrossRef][PubMed]
    [Google Scholar]
  11. Gibbons R. J., Cohen L., Hay D. I.. ( 1986;). Strains of Streptococcus mutans and Streptococcus sobrinus attach to different pellicle receptors. . Infect Immun 52:, 555–561.[PubMed]
    [Google Scholar]
  12. Gutierrez J. A., Crowley P. J., Brown D. P., Hillman J. D., Youngman P., Bleiweis A. S.. ( 1996;). Insertional mutagenesis and recovery of interrupted genes of Streptococcus mutans by using transposon Tn917: preliminary characterization of mutants displaying acid sensitivity and nutritional requirements. . J Bacteriol 178:, 4166–4175.[PubMed]
    [Google Scholar]
  13. Hamilton I. R., Buckley N. D.. ( 1991;). Adaptation by Streptococcus mutans to acid tolerance. . Oral Microbiol Immunol 6:, 65–71. [CrossRef][PubMed]
    [Google Scholar]
  14. Hasona A., Crowley P. J., Levesque C. M., Mair R. W., Cvitkovitch D. G., Bleiweis A. S., Brady L. J.. ( 2005;). Streptococcal viability and diminished stress tolerance in mutants lacking the signal recognition particle pathway or YidC2. . Proc Natl Acad Sci U S A 102:, 17466–17471. [CrossRef][PubMed]
    [Google Scholar]
  15. Hasona A., Zuobi-Hasona K., Crowley P. J., Abranches J., Ruelf M. A., Bleiweis A. S., Brady L. J.. ( 2007;). Membrane composition changes and physiological adaptation by Streptococcus mutans signal recognition particle pathway mutants. . J Bacteriol 189:, 1219–1230. [CrossRef][PubMed]
    [Google Scholar]
  16. Heckman K. L., Pease L. R.. ( 2007;). Gene splicing and mutagenesis by PCR-driven overlap extension. . Nat Protoc 2:, 924–932. [CrossRef][PubMed]
    [Google Scholar]
  17. Henderson B., Martin A.. ( 2011;). Bacterial virulence in the moonlight: multitasking bacterial moonlighting proteins are virulence determinants in infectious disease. . Infect Immun 79:, 3476–3491. [CrossRef][PubMed]
    [Google Scholar]
  18. Honda K., Nakamura K., Nishiguchi M., Yamane K.. ( 1993;). Cloning and characterization of a Bacillus subtilis gene encoding a homolog of the 54-kilodalton subunit of mammalian signal recognition particle and Escherichia coli Ffh. . J Bacteriol 175:, 4885–4894.[PubMed]
    [Google Scholar]
  19. Jenkinson H. F., Demuth D. R.. ( 1997;). Structure, function and immunogenicity of streptococcal antigen I/II polypeptides. . Mol Microbiol 23:, 183–190. [CrossRef][PubMed]
    [Google Scholar]
  20. Jenkinson H. F., Lamont R. J.. ( 1997;). Streptococcal adhesion and colonization. . Crit Rev Oral Biol Med 8:, 175–200. [CrossRef][PubMed]
    [Google Scholar]
  21. Khalichi P., Cvitkovitch D. G., Santerre J. P.. ( 2004;). Effect of composite resin biodegradation products on oral streptococcal growth. . Biomaterials 25:, 5467–5472. [CrossRef][PubMed]
    [Google Scholar]
  22. Kiefer D., Kuhn A.. ( 2007;). YidC as an essential and multifunctional component in membrane protein assembly. . Int Rev Cytol 259:, 113–138. [CrossRef][PubMed]
    [Google Scholar]
  23. Knox K. W., Hardy L. N., Wicken A. J.. ( 1986;). Comparative studies on the protein profiles and hydrophobicity of strains of Streptococcus mutans serotype c. . J Gen Microbiol 132:, 2541–2548.[PubMed]
    [Google Scholar]
  24. Larson M. R., Rajashankar K. R., Patel M. H., Robinette R. A., Crowley P. J., Michalek S., Brady L. J., Deivanayagam C.. ( 2010;). Elongated fibrillar structure of a streptococcal adhesin assembled by the high-affinity association of α- and PPII-helices. . Proc Natl Acad Sci U S A 107:, 5983–5988. [CrossRef][PubMed]
    [Google Scholar]
  25. LeBlanc D. J., Lee L. N., Abu-Al-Jaibat A.. ( 1992;). Molecular, genetic, and functional analysis of the basic replicon of pVA380-1, a plasmid of oral streptococcal origin. . Plasmid 28:, 130–145. [CrossRef][PubMed]
    [Google Scholar]
  26. Ling E., Feldman G., Portnoi M., Dagan R., Overweg K., Mulholland F., Chalifa-Caspi V., Wells J., Mizrachi-Nebenzahl Y.. ( 2004;). Glycolytic enzymes associated with the cell surface of Streptococcus pneumoniae are antigenic in humans and elicit protective immune responses in the mouse. . Clin Exp Immunol 138:, 290–298. [CrossRef][PubMed]
    [Google Scholar]
  27. McArthur W. P., Rhodin N. R., Seifert T. B., Oli M. W., Robinette R. A., Demuth D. R., Brady L. J.. ( 2007;). Characterization of epitopes recognized by anti-Streptococcus mutans P1 monoclonal antibodies. . FEMS Immunol Med Microbiol 50:, 342–353. [CrossRef][PubMed]
    [Google Scholar]
  28. Michalek S. M., McGhee J. R., Navia J. M.. ( 1975;). Virulence of Streptococcus mutans: a sensitive method for evaluating cariogenicity in young gnotobiotic rats. . Infect Immun 12:, 69–75.[PubMed]
    [Google Scholar]
  29. Oli M. W., McArthur W. P., Brady L. J.. ( 2006;). A whole cell BIAcore assay to evaluate P1-mediated adherence of Streptococcus mutans to human salivary agglutinin and inhibition by specific antibodies. . J Microbiol Methods 65:, 503–511. [CrossRef][PubMed]
    [Google Scholar]
  30. Phillips G. J., Silhavy T. J.. ( 1992;). The E. coli ffh gene is necessary for viability and efficient protein export. . Nature 359:, 744–746. [CrossRef][PubMed]
    [Google Scholar]
  31. Robinette R. A., Oli M. W., McArthur W. P., Brady L. J.. ( 2011;). A therapeutic anti-Streptococcus mutans monoclonal antibody used in human passive protection trials influences the adaptive immune response. . Vaccine 29:, 6292–6300. [CrossRef][PubMed]
    [Google Scholar]
  32. Seifert K. N., McArthur W. P., Bleiweis A. S., Brady L. J.. ( 2003;). Characterization of group B streptococcal glyceraldehyde-3-phosphate dehydrogenase: surface localization, enzymatic activity, and protein–protein interactions. . Can J Microbiol 49:, 350–356. [CrossRef][PubMed]
    [Google Scholar]
  33. Seifert T. B., Bleiweis A. S., Brady L. J.. ( 2004;). Contribution of the alanine-rich region of Streptococcus mutans P1 to antigenicity, surface expression, and interaction with the proline-rich repeat domain. . Infect Immun 72:, 4699–4706. [CrossRef][PubMed]
    [Google Scholar]
  34. Severin A., Nickbarg E., Wooters J., Quazi S. A., Matsuka Y. V., Murphy E., Moutsatsos I. K., Zagursky R. J., Olmsted S. B.. ( 2007;). Proteomic analysis and identification of Streptococcus pyogenes surface-associated proteins. . J Bacteriol 189:, 1514–1522. [CrossRef][PubMed]
    [Google Scholar]
  35. Suntharalingam P., Senadheera M. D., Mair R. W., Lévesque C. M., Cvitkovitch D. G.. ( 2009;). The LiaFSR system regulates the cell envelope stress response in Streptococcus mutans. . J Bacteriol 191:, 2973–2984. [CrossRef][PubMed]
    [Google Scholar]
  36. Terleckyj B., Willett N. P., Shockman G. D.. ( 1975;). Growth of several cariogenic strains of oral streptococci in a chemically defined medium. . Infect Immun 11:, 649–655.[PubMed]
    [Google Scholar]
  37. Vadeboncoeur C., Brochu D., Reizer J.. ( 1991;). Quantitative determination of the intracellular concentration of the various forms of HPr, a phosphocarrier protein of the phosphoenolpyruvate: sugar phosphotransferase system in growing cells of oral streptococci. . Anal Biochem 196:, 24–30. [CrossRef][PubMed]
    [Google Scholar]
  38. van der Laan M., Urbanus M. L., Ten Hagen-Jongman C. M., Nouwen N., Oudega B., Harms N., Driessen A. J., Luirink J.. ( 2003;). A conserved function of YidC in the biogenesis of respiratory chain complexes. . Proc Natl Acad Sci U S A 100:, 5801–5806. [CrossRef][PubMed]
    [Google Scholar]
  39. Wen Z. T., Burne R. A.. ( 2001;). Construction of a new integration vector for use in Streptococcus mutans. . Plasmid 45:, 31–36. [CrossRef][PubMed]
    [Google Scholar]
  40. Wunder D., Bowen W. H.. ( 2000;). Effects of antibodies to glucosyltransferase on soluble and insolubilized enzymes. . Oral Dis 6:, 289–296. [CrossRef][PubMed]
    [Google Scholar]
  41. Zeng L., Burne R. A.. ( 2009;). Transcriptional regulation of the cellobiose operon of Streptococcus mutans. . J Bacteriol 191:, 2153–2162. [CrossRef][PubMed]
    [Google Scholar]
  42. Zhang Y. J., Tian H. F., Wen J. F.. ( 2009;). The evolution of YidC/Oxa/Alb3 family in the three domains of life: a phylogenomic analysis. . BMC Evol Biol 9:, 137. [CrossRef][PubMed]
    [Google Scholar]
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