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Streptococcus mutans copes with heat stress by multiple transcriptional regulons modulating virulence and energy metabolism

Liu, Chengcheng, Niu, Yulong, Zhou, Xuedong, Zheng, Xin, Wang, Shida, Guo, Qiang, Li, Yuqing, Li, Mingyun, Li, Jiyao, Yang, Yi, Ding, Yi, Lamont, Richard J., Xu, Xin·2015·Scientific Reports

Abstract

Dental caries is closely associated with the virulence of Streptococcus mutans. The virulence expression of S. mutans is linked to its stress adaptation to the changes in the oral environment. In this work we used whole-genome microarrays to profile the dynamic transcriptomic responses of S. mutans during physiological heat stress. In addition, we evaluated the phenotypic changes, including, eDNA release, initial biofilm formation, extracellular polysaccharides generation, acid production/acid tolerance and ATP turnover of S. mutans during heat stress. There were distinct patterns observed in the way that S. mutans responded to heat stress that included 66 transcription factors for the expression of functional genes being differentially expressed. Especially, response regulators of two component systems (TCSs), the repressors of heat shock proteins and regulators involved in sugar transporting and metabolism co-ordinated to enhance the cell’s survival and energy generation against heat stress in S. mutans.

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  1. Decker, E. M., Klein, C., Schwindt, D. & von Ohle, C. Metabolic activity of Streptococcus mutans biofilms and gene expression during exposure to xylitol and sucrose. Int J Oral Sci. 6(4):195–204 (2014). · DOI
  2. Lemos, J. A., Quivey, R. G., Jr., Koo, H. & Abranches, J. Streptococcus mutans: a new Gram-positive paradigm? Microbiology. 159, 436–445 (2013). · DOI
  3. Lemos, J. A., Abranches, J. & Burne, R. A. Responses of cariogenic streptococci to environmental stresses. Curr Issues Mol Biol. 7, 95–107 (2005).
  4. Narberhaus, F. Translational control of bacterial heat shock and virulence genes by temperature-sensing mRNAs. RNA Biol. 7, 84–89 (2010). · DOI
  5. Kotte, O., Zaugg, J. B. & Heinemann, M. Bacterial adaptation through distributed sensing of metabolic fluxes. Mol Syst Biol. 6, 355 (2010). · DOI · Paper page
  6. Herrou, J., Rotskoff, G., Luo, Y., Roux, B. & Crosson, S. Structural basis of a protein partner switch that regulates the general stress response of alpha-proteobacteria. Proc Natl Acad Sci U S A. 109, E1415–1423 (2012). · DOI
  7. Elsholz, A. K., Michalik, S., Zuhlke, D., Hecker, M. & Gerth, U. CtsR, the Gram-positive master regulator of protein quality control, feels the heat. EMBO J. 29, 3621–3629 (2010). · DOI
  8. Griswold, A. R., Jameson-Lee, M. & Burne, R. A. Regulation and physiologic significance of the agmatine deiminase system of Streptococcus mutans UA159. J Bacteriol. 188, 834–841 (2006). · DOI
  9. Sheng, J. & Marquis, R. E. Enhanced acid resistance of oral streptococci at lethal pH values associated with acid-tolerant catabolism and with ATP synthase activity. FEMS Microbiol Lett. 262, 93–98 (2006). · DOI
  10. Fozo, E. M. & Quivey, R. G., Jr. Shifts in the membrane fatty acid profile of Streptococcus mutans enhance survival in acidic environments. Appl Environ Microbiol. 70, 929–936 (2004). · DOI
  11. Xu, P. et al. Genome of the opportunistic pathogen Streptococcus sanguinis. J Bacteriol. 189, 3166–3175 (2007). · DOI
  12. Smith, E. G. & Spatafora, G. A. Gene regulation in S. mutans: complex control in a complex environment. J Dent Res. 91, 133–141 (2012). · DOI
  13. Ajdic, D. et al. Genome sequence of Streptococcus mutans UA159, a cariogenic dental pathogen. Proc Natl Acad Sci U S A. 99, 14434–14439 (2002). · DOI
  14. Liang, W. D. et al. Gene expression profiling of Clostridium botulinum under heat shock stress. Biomed Res Int. 2013, 760904 (2013).
  15. Xue, X. L., Tomasch, J., Sztajer, H. & Wagner-Dobler, I. The Delta Subunit of RNA Polymerase, RpoE, Is a Global Modulator of Streptococcus mutans Environmental Adaptation. J Bacteriol. 192, 5081–5092 (2010). · DOI
  16. Leung, V., Ajdic, D., Koyanagi, S. & Levesque, C. M. The formation of Streptococcus mutans persisters induced by the quorum-sensing peptide pheromone is affected by the LexA regulator. J Bacteriol. 197, 1083–1094 (2015). · DOI
  17. Wu, C. et al. Regulation of ciaXRH operon expression and identification of the CiaR regulon in Streptococcus mutans. J Bacteriol. 192, 4669–4679 (2010). · DOI
  18. Jayaraman, G. C., Penders, J. E. & Burne, R. A. Transcriptional analysis of the Streptococcus mutans hrcA, grpE and dnaK genes and regulation of expression in response to heat shock and environmental acidification. Mol Microbiol. 25, 329–341(1997). · DOI
  19. Lemos, J. A. & Burne, R. A. Regulation and Physiological Significance of ClpC and ClpP in Streptococcus mutans. J Bacteriol. 184, 6357–6366 (2002). · DOI
  20. Lemos, J. A., Chen, Y. Y. & Burne, R. A. Genetic and physiologic analysis of the groE operon and role of the HrcA repressor in stress gene regulation and acid tolerance in Streptococcus mutans. J Bacteriol. 183, 6074–6084 (2001). · DOI
  21. Lemos, J. A., Luzardo, Y. & Burne, R. A. Physiologic effects of forced down-regulation of dnaK and groEL expression in Streptococcus mutans. J Bacteriol. 189, 1582–1588 (2007). · DOI
  22. Hou, X. H., Zhang, J. Q., Song, X. Y., Ma, X. B. & Zhang, S. Y. Contribution of ClpP to stress tolerance and virulence properties of Streptococcus mutans. J Basic Microbiol. 54, 1222–1232 (2014). · DOI
  23. Svensater, G., Sjogreen, B. & Hamilton, I. R. Multiple stress responses in Streptococcus mutans and the induction of general and stress-specific proteins. Microbiology. 146, 107–117 (2000). · DOI
  24. Tremblay, Y. D., Lo, H., Li, Y. H., Halperin, S. A. & Lee, S. F. Expression of the Streptococcus mutans essential two-component regulatory system VicRK is pH and growth-phase dependent and controlled by the LiaFSR three-component regulatory system. Microbiology. 155, 2856–2865 (2009). · DOI
  25. Senadheera, M. D. et al. A VicRK signal transduction system in Streptococcus mutans affects gtfBCD, gbpB and ftf expression, biofilm formation and genetic competence development. J Bacteriol. 187, 4064–4076 (2005). · DOI
  26. Sudhakar, P. et al. Construction and verification of the transcriptional regulatory response network of Streptococcus mutans upon treatment with the biofilm inhibitor carolacton. BMC genomics. 15, 739 (2014). · DOI
  27. Kanehisa M. et al. From genomics to chemical genomics: new developments in KEGG. Nucleic Acids Res. 34, D354–357 (2006 ). Available at: http://www.genome.jp/kegg/. (Accessed: 74.0, April 2015). · DOI
  28. Vadeboncoeur, C. & Pelletier, M. The phosphoenolpyruvate:sugar phosphotransferase system of oral streptococci and its role in the control of sugar metabolism. FEMS Microbiol Rev. 19, 187–207 (1997). · DOI
  29. Ajdic, D. & Chen, Z. A novel phosphotransferase system of Streptococcus mutans is responsible for transport of carbohydrates with-1,3 linkage. Mol Oral Microbiol. 28, 114–128 (2013). · DOI
  30. dos Santos, N. Relationship among dental plaque composition, daily sugar exposure and caries in the primary dentition. Caries Res. 37, 236–236 (2003). · DOI
  31. Bowen, W. H. & Koo, H. Biology of Streptococcus mutans-derived glucosyltransferases: role in extracellular matrix formation of cariogenic biofilms. Caries Res. 45, 69–86 (2011). · DOI
  32. Loo, C. Y., Mitrakul, K., Voss, I. B., Hughes, C. V. & Ganeshkumar, N. Involvement of an inducible fructose phosphotransferase operon in Streptococcus gordonii biofilm formation. J Bacteriol. 185(21), 6241–54 (2003). · DOI
  33. Baker, J. L. et al. Streptococcus mutans NADH Oxidase Lies at the Intersection of Overlapping Regulons Controlled by Oxygen and NAD(+) Levels. J Bacteriol. 196, 2166–2177 (2014). · DOI
  34. Shenhar, Y., Rasouly, A., Biran, D. & Ron, E. Z. Adaptation of Escherichi coli to elevated temperatures involves a change in stability of heat shock gene transcripts. Environ Microbiol. 11, 2989–2997 (2009). · DOI
  35. Jozefczuk, S. et al. Metabolomic and transcriptomic stress response of Escherichia coli. Mol Syst Biol. 6, 364 (2010). · DOI
  36. Chakraborty, A., Mukherjee, S., Chattopadhyay, R., Roy, S. & Chakrabarti, S. Conformational adaptation in the E. coli sigma 32 protein in response to heat shock. J Phys Chem B. 118, 4793–4802 (2014). · DOI
  37. Reder, A., Pother, D. C., Gerth, U. & Hecker, M. The modulator of the general stress response, MgsR, of Bacillus subtilis is subject to multiple and complex control mechanisms. Environ Microbiol. 14, 2838–2850 (2012). · DOI
  38. Kazmierczak, M. J., Wiedmann, M. & Boor, K. J. Alternative sigma factors and their roles in bacterial virulence. Microbiol Mol Biol Rev. 69, 527–543 (2005). · DOI
  39. Song, L. et al. A genome-wide study of two-component signal transduction systems in eight newly sequenced mutans streptococci strains. BMC genomics. 13, 128 (2012). · DOI
  40. van Die, I. M., Bergmans, H. E. & Hoekstra, W. P. Transformation in Escherichia coli: studies on the role of the heat shock in induction of competence. J Gen Microbiol. 129, 663–670 (1983).
  41. Murphy, M. E. The HSP70 family and cancer. Carcinogenesis. 34, 1181–1188, (2013). · DOI
  42. Vriezen, J. A., de Bruijn, F. J. & Nusslein, K. Responses of rhizobia to desiccation in relation to osmotic stress, oxygen and temperature. Appl Environ Microbiol. 73, 3451–3459 (2007). · DOI
  43. Tao, L., Chattoraj, P. & Biswas, I. CtsR regulation in mcsAB-deficient Gram-positive bacteria. J Bacteriol. 194, 1361–1368 (2012). · DOI
  44. Deng, D. M., ten Cate, J. M. & Crielaard, W. The adaptive response of Streptococcus mutans towards oral care products: involvement of the ClpP serine protease. Eur J Oral Sci. 115, 363–370, (2007). · DOI
  45. Fleury, B. et al. Transcriptomic and metabolic responses of Staphylococcus aureus exposed to supra-physiological temperatures. BMC Microbiol. 9, 76, (2009). · DOI
  46. Koo, H., Xiao, J. & Klein, M. I. Extracellular polysaccharides matrix--an often forgotten virulence factor in oral biofilm research. Int J Oral Sci. 1, 229–234 (2009). · DOI
  47. Koo, H., Falsetta, M. L. & Klein, M. I. The exopolysaccharide matrix: a virulence determinant of cariogenic biofilm. J Dent Res. 92, 1065–1073 (2013). · DOI · Paper page
  48. Liu, C. et al. Hyperosmotic response of streptococcus mutans: from microscopic physiology to transcriptomic profile. BMC Microbiol. 13, 275 (2013). · DOI
  49. Hong, F. et al. RankProd: a bioconductor package for detecting differentially expressed genes in meta-analysis. Bioinformatics. 22, 2825–2827, (2006). · DOI
  50. Subramanian, A., Kuehn, H., Gould, J., Tamayo, P. & Mesirov, J. P. GSEA-P: a desktop application for Gene Set Enrichment Analysis. Bioinformatics. 23, 3251–3253 (2007). · DOI
  51. Li, M. Y., Huang, R. J., Zhou, X. D. & Gregory, R. L. Role of sortase in Streptococcus mutans under the effect of nicotine. Int J Oral Sci. 5, 206–211 (2013). · DOI
  52. Taboada, B., Verde, C. & Merino, E. High accuracy operon prediction method based on STRING database scores. Nucleic Acids Res. 38, e130 (2010). · DOI
  53. Xu, X., Zhou, X. D. & Wu, C. D. The tea catechin epigallocatechin gallate suppresses cariogenic virulence factors of Streptococcus mutans. Antimicrob Agents Chemother. 55, 1229–1236 (2011). · DOI
  54. Cheng, L. et al. Antibacterial amorphous calcium phosphate nanocomposites with a quaternary ammonium dimethacrylate and silver nanoparticles. Dent Mater. 28, 561–572, (2012). · DOI · Paper page
  55. Liao, S. et al. Streptococcus mutans extracellular DNA is upregulated during growth in biofilms, actively released via membrane vesicles and influenced by components of the protein secretion machinery. J Bacteriol. 196, 2355–2366 (2014). · DOI · Paper page
  56. Xu, X., Zhou, X. D. & Wu, C. D. Tea catechin epigallocatechin gallate inhibits Streptococcus mutans biofilm formation by suppressing gtf genes. Arch Oral Biol. 57, 678–683 (2012). · DOI

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Metadata

Authors
Liu, C., Niu, Y., Zhou, X., Zheng, X., Wang, S., Guo, Q., Li, Y., Li, M., Li, J., Yang, Y., Ding, Y., Lamont, R. J., & Xu, X.
Venue
Scientific Reports
Published
2015-08-07
Volume
5
Issue
1
ISSN
2045-2322
Cited by
39
References
4
Language
en

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