1887

Abstract

, one of the primary causative agents of dental caries in humans, ferments dietary sugars in the mouth to produce organic acids. These acids lower local pH values, resulting in demineralization of the tooth enamel, leading to caries. To survive acidic environments, employs several adaptive mechanisms, including a shift from saturated to unsaturated fatty acids in membrane phospholipids. PlsX is an acyl-ACP : phosphate transacylase that links the fatty acid synthase II (FASII) pathway to the phospholipid synthesis pathway, and is therefore central to the movement of unsaturated fatty acids into the membrane. Recently, we discovered that is not essential in A deletion mutant was not a fatty acid or phospholipid auxotroph. Gas chromatography of fatty acid methyl esters indicated that membrane fatty acid chain length in the deletion strain differed from those detected in the parent strain, UA159. The deletion strain displayed a fatty acid shift similar to WT, but had a higher percentage of unsaturated fatty acids at low pH. The deletion strain survived significantly longer than the parent strain when cultures were subjected to an acid challenge of pH 2.5.The Δ strain also exhibited elevated F-ATPase activity at pH 5.2, compared with the parent. These results indicate that the loss of affects both the fatty acid synthesis pathway and the acid-adaptive response of .

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2016-04-01
2019-12-13
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References

  1. Abranches J., Candella M. M., Wen Z. T., Baker H. V., Burne R. A.. 2006; Different roles of EIIABMan and EIIGlc in regulation of energy metabolism, biofilm development, and competence in Streptococcus mutans. J Bacteriol188:3748–3756 [CrossRef][PubMed]
    [Google Scholar]
  2. Ajdić D., McShan W. M., McLaughlin R. E., Savić G., Chang J., Carson M. B., Primeaux C., Tian R., Kenton S., other authors. 2002; Genome sequence of Streptococcus mutans UA159, a cariogenic dental pathogen. Proc Natl Acad Sci U S A99:14434–14439 [CrossRef][PubMed]
    [Google Scholar]
  3. Argimón S., Caufield P. W.. 2011; Distribution of putative virulence genes in Streptococcus mutans strains does not correlate with caries experience. J Clin Microbiol49:984–992 [CrossRef][PubMed]
    [Google Scholar]
  4. Baker J. L., Derr A. M., Karuppaiah K., MacGilvray M. E., Kajfasz J. K., Faustoferri R. C., Rivera-Ramos I., Bitoun J. P., Lemos J. A., other authors. 2014; Streptococcus mutans NADH oxidase lies at the intersection of overlapping regulons controlled by oxygen and NAD+ levels. J Bacteriol196:2166–2177 [CrossRef][PubMed]
    [Google Scholar]
  5. Banas J. A.. 2004; Virulence properties of Streptococcus mutans. Front Biosci9:1267–1277 [CrossRef][PubMed]
    [Google Scholar]
  6. Brinster S., Lamberet G., Staels B., Trieu-Cuot P., Gruss A., Poyart C.. 2009; Type II fatty acid synthesis is not a suitable antibiotic target for Gram-positive pathogens. Nature458:83–86 [CrossRef][PubMed]
    [Google Scholar]
  7. Buckley A. A., Faustoferri R. C., Quivey R. G. Jr.. 2014; β-Phosphoglucomutase contributes to aciduricity in Streptococcus mutans. Microbiology160:818–827 [CrossRef][PubMed]
    [Google Scholar]
  8. de Soet J. J., Nyvad B., Kilian M.. 2000; Strain-related acid production by oral streptococci. Caries Res34:486–490 [CrossRef][PubMed]
    [Google Scholar]
  9. Derr A. M., Faustoferri R. C., Betzenhauser M. J., Gonzalez K., Marquis R. E., Quivey R. G. Jr.. 2012; Mutation of the NADH oxidase gene (nox) reveals an overlap of the oxygen- and acid-mediated stress responses in Streptococcus mutans. Appl Environ Microbiol78:1215–1227 [CrossRef][PubMed]
    [Google Scholar]
  10. Faustoferri R. C., Hubbard C. J., Santiago B., Buckley A. A., Seifert T. B., Quivey R. G. Jr.. 2015; Regulation of fatty acid biosynthesis by the global regulator CcpA and the local regulator FabT in Streptococcus mutans. Mol Oral Microbiol30:128–146 [CrossRef][PubMed]
    [Google Scholar]
  11. Fiske C. H., Subbarow Y.. 1925; The colorimetric determination of phosphorus. J Biol Chem66:375–400
    [Google Scholar]
  12. Fozo E. M., Quivey R. G. Jr.. 2004a; The fabM gene product of Streptococcus mutans is responsible for the synthesis of monounsaturated fatty acids and is necessary for survival at low pH. J Bacteriol186:4152–4158 [CrossRef][PubMed]
    [Google Scholar]
  13. Fozo E. M., Quivey R. G. Jr.. 2004b; Shifts in the membrane fatty acid profile of Streptococcus mutans enhance survival in acidic environments. Appl Environ Microbiol70:929–936 [CrossRef][PubMed]
    [Google Scholar]
  14. Fozo E. M., Scott-Anne K., Koo H., Quivey R. G. Jr.. 2007; Role of unsaturated fatty acid biosynthesis in virulence of Streptococcus mutans. Infect Immun75:1537–1539 [CrossRef][PubMed]
    [Google Scholar]
  15. Grimes K. D., Lu Y.-J., Zhang Y.-M., Luna V. A., Hurdle J. G., Carson E. I., Qi J., Kudrimoti S., Rock C. O., Lee R. E.. 2008; Novel acyl phosphate mimics that target PlsY, an essential acyltransferase in Gram-positive bacteria. ChemMedChem3:1936–1945 [CrossRef][PubMed]
    [Google Scholar]
  16. Heipieper H. J., Neumann G., Cornelissen S., Meinhardt F.. 2007; Solvent-tolerant bacteria for biotransformations in two-phase fermentation systems. Appl Microbiol Biotechnol74:961–973 [CrossRef][PubMed]
    [Google Scholar]
  17. Jerga A., Rock C. O.. 2009; Acyl-acyl carrier protein regulates transcription of fatty acid biosynthetic genes via the FabT repressor in Streptococcus pneumoniae. J Biol Chem284:15364–15368 [CrossRef][PubMed]
    [Google Scholar]
  18. Jiang P., Cronan J.E., Jr. 1994; Inhibition of fatty acid synthesis in Escherichia coli in the absence of phospholipid synthesis and release of inhibition by thioesterase action. J Bacteriol176:2814–2821[PubMed]
    [Google Scholar]
  19. Koo H., Xiao J., Klein M. I., Jeon J. G.. 2010; Exopolysaccharides produced by Streptococcus mutans glucosyltransferases modulate the establishment of microcolonies within multispecies biofilms. J Bacteriol192:3024–3032 [CrossRef][PubMed]
    [Google Scholar]
  20. Kuhnert W. L., Zheng G., Faustoferri R. C., Quivey R.G., Jr. 2004; F-ATPase operon promoter of Streptococcus mutans is transcriptionally regulated in response to external pH. J Bacteriol186:8524–8528 [CrossRef][PubMed]
    [Google Scholar]
  21. Lemos J. A., Burne R. A.. 2008; A model of efficiency: stress tolerance by Streptococcus mutans. Microbiology154:3247–3255 [CrossRef][PubMed]
    [Google Scholar]
  22. Lu H., Tonge P. J.. 2008; Inhibitors of FabI, an enzyme drug target in the bacterial fatty acid biosynthesis pathway. Acc Chem Res41:11–20 [CrossRef][PubMed]
    [Google Scholar]
  23. Lu Y.-J., Zhang Y.-M., Grimes K. D., Qi J., Lee R. E., Rock C. O.. 2006; Acyl-phosphates initiate membrane phospholipid synthesis in Gram-positive pathogens. Mol Cell23:765–772 [CrossRef][PubMed]
    [Google Scholar]
  24. Lundbaek J. A., Collingwood S. A., Ingólfsson H. I., Kapoor R., Andersen O. S.. 2010; Lipid bilayer regulation of membrane protein function: gramicidin channels as molecular force probes. J R Soc Interface7:373–395 [CrossRef][PubMed]
    [Google Scholar]
  25. MacGilvray M. E., Lapek J. D. Jr, Friedman A. E., Quivey R.G., Jr.. 2012; Cardiolipin biosynthesis in Streptococcus mutans is regulated in response to external pH. Microbiology158:2133–2143 [CrossRef][PubMed]
    [Google Scholar]
  26. Paoletti L., Lu Y.-J., Schujman G. E., de Mendoza D., Rock C. O.. 2007; Coupling of fatty acid and phospholipid synthesis in Bacillus subtilis. J Bacteriol189:5816–5824 [CrossRef][PubMed]
    [Google Scholar]
  27. Parsons J. B., Frank M. W., Subramanian C., Saenkham P., Rock C. O.. 2011; Metabolic basis for the differential susceptibility of Gram-positive pathogens to fatty acid synthesis inhibitors. Proc Natl Acad Sci U S A108:15378–15383 [CrossRef][PubMed]
    [Google Scholar]
  28. Parsons J. B., Frank M. W., Eleveld M. J., Schalkwijk J., Broussard T. C., de Jonge M. I., Rock C. O.. 2015; A thioesterase bypasses the requirement for exogenous fatty acids in the plsX deletion of Streptococcus pneumoniae. Mol Microbiol96:28–41 [CrossRef][PubMed]
    [Google Scholar]
  29. Pereira-Cenci T., Deng D. M., Kraneveld E. A., Manders E.M.M., Del Bel Cury A. A., Ten Cate J. M., Crielaard W.. 2008; The effect of Streptococcus mutans and Candida glabrata on Candida albicans biofilms formed on different surfaces. Arch Oral Biol53:755–764 [CrossRef][PubMed]
    [Google Scholar]
  30. Petersen P. E., Bourgeois D., Ogawa H., Estupinan-Day S., Ndiaye C.. 2005; The global burden of oral diseases and risks to oral health. Bull World Health Organ83:661–669[PubMed]
    [Google Scholar]
  31. Quivey R. G. Jr, Faustoferri R. C., Clancy K. A., Marquis R. E.. 1995; Acid adaptation in Streptococcus mutans UA159 alleviates sensitization to environmental stress due to RecA deficiency. FEMS Microbiol Lett126:257–261 [CrossRef][PubMed]
    [Google Scholar]
  32. Quivey R. G. Jr, Faustoferri R., Monahan K., Marquis R.. 2000a; Shifts in membrane fatty acid profiles associated with acid adaptation of Streptococcus mutans. FEMS Microbiol Lett189:89–92 [CrossRef][PubMed]
    [Google Scholar]
  33. Quivey R. G., Kuhnert W. L., Hahn K.. 2000b; Adaptation of oral streptococci to low pH. Adv Microb Physiol239–274 [CrossRef]
    [Google Scholar]
  34. Quivey R. G. Jr, Grayhack E. J., Faustoferri R. C., Hubbard C. J., Baldeck J. D., Wolf A. S., MacGilvray M. E., Rosalen P. L., Scott-Anne K., other authors. 2015; Functional profiling in Streptococcus mutans: construction and examination of a genomic collection of gene deletion mutants. Mol Oral Microbiol30:474–495 [CrossRef][PubMed]
    [Google Scholar]
  35. Santiago B., MacGilvray M., Faustoferri R. C., Quivey R. G. Jr.. 2012; The branched-chain amino acid aminotransferase encoded by ilvE is involved in acid tolerance in Streptococcus mutans. J Bacteriol194:2010–2019 [CrossRef][PubMed]
    [Google Scholar]
  36. Sardessai Y., Bhosle S.. 2002; Tolerance of bacteria to organic solvents. Res Microbiol153:263–268 [CrossRef][PubMed]
    [Google Scholar]
  37. Sheng J., Marquis R. E.. 2007; Malolactic fermentation by Streptococcus mutans. FEMS Microbiol Lett272:196–201 [CrossRef][PubMed]
    [Google Scholar]
  38. Sikkema J., de Bont J. A., Poolman B.. 1995; Mechanisms of membrane toxicity of hydrocarbons. Microbiol Rev59:201–222[PubMed]
    [Google Scholar]
  39. Sturr M. G., Marquis R. E.. 1992; Comparative acid tolerances and inhibitor sensitivities of isolated F-ATPases of oral lactic acid bacteria. Appl Environ Microbiol58:2287–2291[PubMed]
    [Google Scholar]
  40. Takahashi N., Nyvad B.. 2011; The role of bacteria in the caries process: ecological perspectives. J Dent Res90:294–303 [CrossRef][PubMed]
    [Google Scholar]
  41. Tanzer J. M., Livingston J., Thompson A. M.. 2001; The microbiology of primary dental caries in humans. J Dent Educ65:1028–1037[PubMed]
    [Google Scholar]
  42. Terleckyj B., Willett N. P., Shockman G. D.. 1975; Growth of several cariogenic strains of oral streptococci in a chemically defined medium. Infect Immun11:649–655[PubMed]
    [Google Scholar]
  43. Yoshimura M., Oshima T., Ogasawara N.. 2007; Involvement of the YneS/YgiH and PlsX proteins in phospholipid biosynthesis in both Bacillus subtilis and Escherichia coli. BMC Microbiol7:69 [CrossRef][PubMed]
    [Google Scholar]
  44. Zhang Y.-M., Rock C. O.. 2008a; Membrane lipid homeostasis in bacteria. Nat Rev Microbiol6:222–233 [CrossRef][PubMed]
    [Google Scholar]
  45. Zhang Y.-M., Rock C. O.. 2008b; Thematic review series: glycerolipids. Acyltransferases in bacterial glycerophospholipid synthesis. J Lipid Res49:1867–1874 [CrossRef][PubMed]
    [Google Scholar]
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