1887

Abstract

Mature biofilm and planktonic cells of cultured in a neutral pH environment were subjected to comparative proteome analysis. Of the 242 protein spots identified, 48 were significantly altered in their level of expression (<0·050) or were unique to planktonic or biofilm-grown cells. Among these were four hypothetical proteins as well as proteins known to be associated with the maintenance of competence or found to possess a -box-like element upstream of their coding gene. Most notable among the non-responsive genes were those encoding the molecular chaperones DnaK, GroEL and GroES, which are considered to be up-regulated by sessile growth. Analysis of the rest of the proteome indicated that a number of cellular functions associated with carbon uptake and cell division were down-regulated. The data obtained were consistent with the hypothesis that a reduction in the general growth rate of mature biofilms of in a neutral pH environment is associated with the maintenance of transformation without the concomitant stress response observed during the transient state of competence in bacterial batch cultures.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.27830-0
2005-06-01
2021-07-30
Loading full text...

Full text loading...

/deliver/fulltext/micro/151/6/mic1511823.html?itemId=/content/journal/micro/10.1099/mic.0.27830-0&mimeType=html&fmt=ahah

References

  1. Abranches J., Chen Y. Y., Burne R. A. 2003; Characterization of S. mutans strains deficient in EIIABMan of the sugar phosphotransferase system. Appl Environ Microbiol 69:4760–4769 [CrossRef]
    [Google Scholar]
  2. Ajdic D., Sutcliffe I. C., Russell R. R., Ferretti J. J. 1996; Organization and nucleotide sequence of the Streptococcus mutans galactose operon. Gene 180:137–144 [CrossRef]
    [Google Scholar]
  3. Ajdic D., McShan W. M., McLaughlin R. E. & 16 other authors; 2002; Genome sequence of Streptococcus mutans UA159, a cariogenic dental pathogen. Proc Natl Acad Sci U S A 99:14434–14439 [CrossRef]
    [Google Scholar]
  4. Alban A., David S. O., Bjorkesten L., Andersson C., Sloge E., Lewis S., Currie I. 2003; A novel experimental design for comparative two-dimensional gel analysis: two-dimensional difference gel electrophoresis incorporating a pooled internal standard. Proteomics 3:36–44 [CrossRef]
    [Google Scholar]
  5. Aspiras M. B., Ellen R. P., Cvitkovitch D. G. 2004; ComX activity of Streptococcus mutans growing in biofilms. FEMS Microbiol Lett 238:167–174
    [Google Scholar]
  6. Beloin C., Ghigo J.-M. 2005; Finding gene expression patterns in bacterial biofilms. Trends Microbiol 13:16–19 [CrossRef]
    [Google Scholar]
  7. Berge M., Mortier-Barriere I., Martin B., Claverys J. P. 2003; Transformation of Streptococcus pneumoniae relies on DprA- and RecA-dependent protection of incoming DNA single strands. Mol Microbiol 50:527–536 [CrossRef]
    [Google Scholar]
  8. Berges D. A., DeWolf W. E. J., Dunn G. L., Newman D. J., Schmidt S. J., Taggart J. J., Gilvarg C. 1986; Studies on the active site of succinyl-CoA : tetrahydrodipicolinate N-succinyltransferase. Characterization using analogs of tetrahydrodipicolinate. J Biol Chem 261:6160–6167
    [Google Scholar]
  9. Bjedov I., Tenaillon O., Gerard B., Souza V., Denamur E., Radman M., Taddei F., Matic I. 2003; Stress-induced mutagenesis in bacteria. Science 300:1404–1409 [CrossRef]
    [Google Scholar]
  10. Boyer K. G., France J. T. 1976; Alkaline phosphatase, arylsulfatase and beta-glucuronidase in saliva of cyclic women. Int J Fertil 21:43–48
    [Google Scholar]
  11. Campbell E. A., Choi S. Y., Masure H. R. 1998; A competence regulon in Streptococcus pneumoniae revealed by genomic analysis. Mol Microbiol 27:929–939 [CrossRef]
    [Google Scholar]
  12. Choe J. K., Khan-Dawood F. S., Dawood M. Y. 1983; Progesterone and estradiol in the saliva and plasma during the menstrual cycle. Am J Obstet Gynecol 147:557–562
    [Google Scholar]
  13. Claverys J. P., Martin B. 2003; Bacterial ‘competence’ genes: signatures of active transformation, or only remnants?. Trends Microbiol 11:161–165 [CrossRef]
    [Google Scholar]
  14. Claverys J. P., Prudhomme M., Mortier-Barriere I., Martin B. 2000; Adaptation to the environment: Streptococcus pneumoniae, a paradigm for recombination-mediated genetic plasticity?. Mol Microbiol 35:251–259 [CrossRef]
    [Google Scholar]
  15. Cordwell S. J., Larsen M. R., Cole R. T., Walsh B. J. 2002; Comparative proteomics of Staphylococcus aureus and the response of methicillin-resistant and methicillin-sensitive strains to Triton X-100. Microbiology 148:2765–2781
    [Google Scholar]
  16. Courcelle J., Hanawalt P. C. 2003; RecA-dependent recovery of arrested DNA replication forks. Annu Rev Genet 37:611–646 [CrossRef]
    [Google Scholar]
  17. Courcelle J., Ganesan A. K., Hanawalt P. C. 2001; Therefore, what are recombination proteins there for?. Bioessays 23:463–470 [CrossRef]
    [Google Scholar]
  18. Cvitkovitch D. G. 2001; Genetic competence and transformation in oral streptococci. Crit Rev Oral Biol Med 12:217–243 [CrossRef]
    [Google Scholar]
  19. Cvitkovitch D. G., Boyd D. A., Thevenot T., Hamilton I. R. 1995; Glucose transport by a mutant of Streptococcus mutans unable to accumulate sugars via the phosphoenolpyruvate phosphotransferase system. J Bacteriol 177:2251–2258
    [Google Scholar]
  20. Cvitkovitch D. G., Li Y. H., Ellen R. P. 2003; Quorum sensing and biofilm formation in streptococcal infections. J Clin Invest 112:1626–1632 [CrossRef]
    [Google Scholar]
  21. Dagkessamanskaia A., Moscoso M., Henard V., Guiral S., Overweg K., Reuter M., Martin B., Wells J., Claverys J. P. 2004; Interconnection of competence, stress and CiaR regulons in Streptococcus pneumoniae: competence triggers stationary phase autolysis of ciaR mutant cells. Mol Microbiol 51:1071–1086 [CrossRef]
    [Google Scholar]
  22. Dawes C., Watanabe S., Biglow-Lecomte P., Dibdin G. H. 1989; Estimation of the velocity of the salivary film at some different locations in the mouth. J Dent Res 68:1479–1482 [CrossRef]
    [Google Scholar]
  23. Dubnau D. 1991; The regulation of genetic competence in Bacillus subtilis. Mol Microbiol 1:11–18
    [Google Scholar]
  24. Greenberg M. M., Weledji Y. N., Kim J., Bales B. C. 2004; Repair of oxidized abasic sites by exonuclease III, endonuclease IV, and endonuclease III. Biochemistry 43:8178–8183 [CrossRef]
    [Google Scholar]
  25. Hahn K., Faustoferri R. C., Quivey R. G. Jr 1999; Induction of an AP endonuclease activity in Streptococcus mutans during growth at low pH. Mol Microbiol 31:1489–1498 [CrossRef]
    [Google Scholar]
  26. Herp A., Wu A. M., Moschera J. 1979; Current concepts of the structure and nature of mammalian salivary mucous glycoproteins. Mol Cell Biochem 23:27–44
    [Google Scholar]
  27. Iwami Y., Abbe K., Takahashi-Abbe S., Yamada T. 1992; Acid production by streptococci growing at low pH in a chemostat under anaerobic conditions. Oral Microbiol Immunol 7:304–308 [CrossRef]
    [Google Scholar]
  28. Jacques N. A., Hardy L., Knox K. W., Wicken A. J. 1979; Effect of growth conditions on the formation of extracellular lipoteichoic acid by Streptococcus mutans BHT. Infect Immun 25:75–84
    [Google Scholar]
  29. Jakubovics N. S., Jenkinson H. F. 2001; Out of the iron age: new insights into the critical role of manganese homeostasis in bacteria. Microbiology 147:1709–1718
    [Google Scholar]
  30. Jayaraman G. C., Penders J. E., Burne R. A. 1997; 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 [CrossRef]
    [Google Scholar]
  31. Jefferson K. K. 2004; What drives bacteria to produce a biofilm?. FEMS Microbiol Lett 236:163–173 [CrossRef]
    [Google Scholar]
  32. Jonquières R., Bierne H., Fiedler F., Gounon P., Cossart P. 1999; Interaction between the protein InlB of Listeria monocytogenes and lipoteichoic acid: a novel mechanism of protein association at the surface of Gram-positive bacteria. Mol Microbiol 34:902–914 [CrossRef]
    [Google Scholar]
  33. Kitten T., Munro C. L., Michalek S. M., Macrina F. L. 2000; Genetic characterization of a Streptococcus mutans LraI family operon and role in virulence. Infect Immun 68:4441–4451 [CrossRef]
    [Google Scholar]
  34. Kleerebezem M., Quadri L. E., Kuipers O. P., de Vos W. M. 1997; Quorum sensing by peptide pheromones and two-component signal-transduction systems in Gram-positive bacteria. Mol Microbiol 24:895–904 [CrossRef]
    [Google Scholar]
  35. Lemos J. A., Chen Y. Y., Burne R. A. 2001; Genetic and physiologic analysis of the groE operon and role of the HrcA repressor in stress gene regulation and acid tolerance inStreptococcus mutans . J Bacteriol 183:6074–6084 [CrossRef]
    [Google Scholar]
  36. Lemos J. A. C., Abranches J., Burne R. A. 2005; Responses of cariogenic streptococci to environmental stresses. Curr Issues Mol Biol 7:95–107
    [Google Scholar]
  37. Len A. C., Cordwell S. J., Harty D. W. S., Jacques N. A. 2003; Cellular and extracellular proteome analysis of Streptococcus mutans grown in a chemostat. Proteomics 3:627–646 [CrossRef]
    [Google Scholar]
  38. Len A. C., Harty D. W. S., Jacques N. A. 2004a; Stress-responsive proteins are upregulated in Streptococcus mutans during acid tolerance. Microbiology 150:1339–1351 [CrossRef]
    [Google Scholar]
  39. Len A. C., Harty D. W. S., Jacques N. A. 2004b; Proteome analysis of Streptococcus mutans metabolic phenotype during acid tolerance. Microbiology 150:1353–1366 [CrossRef]
    [Google Scholar]
  40. Li Y. H., Lau P. C., Lee J. H., Ellen R. P., Cvitkovitch D. G. 2001a; Natural genetic transformation of Streptococcus mutans growing in biofilms. J Bacteriol 183:897–908 [CrossRef]
    [Google Scholar]
  41. Li Y. H., Hanna M. N., Ellen R. P., Cvitkovitch D. G, Svensäter G. 2001b; Cell density modulates acid adaptation in Streptococcus mutans: implications for survival in biofilms. J Bacteriol 183:6875–6884 [CrossRef]
    [Google Scholar]
  42. Li Y. H., Tang N., Aspiras M. B., Lau P. C., Lee J. H., Ellen R. P., Cvitkovitch D. G. 2002; A quorum-sensing signaling system essential for genetic competence in Streptococcus mutans is involved in biofilm formation. J Bacteriol 184:2699–2708 [CrossRef]
    [Google Scholar]
  43. Lindner C., Nijland R., van Hartskamp M., Bron S., Hamoen L. W., Kuipers O. P. 2004; Differential expression of two paralogous genes of Bacillus subtilis encoding single-stranded DNA binding protein. J Bacteriol 186:1097–1105 [CrossRef]
    [Google Scholar]
  44. Lindquist B., Emilson C. G. 2004; Colonization of Streptococcus mutans and Streptococcus sobrinus genotypes and caries development in children to mothers harboring both species. Caries Res 38:95–103 [CrossRef]
    [Google Scholar]
  45. Macgregor I. D. 1989; Effects of smoking on oral ecology. A review of the literature. Clin Prev Dent 11:3–7
    [Google Scholar]
  46. Martin B., Garcia P., Castanie M. P., Claverys J. P. 1995; The recA gene of Streptococcus pneumoniae is part of a competence-induced operon and controls lysogenic induction. Mol Microbiol 15:367–379 [CrossRef]
    [Google Scholar]
  47. Masure H. R., Pearce B. J., Shio H., Spellerberg B. 1998; Membrane targeting of RecA during genetic transformation. Mol Microbiol 27:845–852 [CrossRef]
    [Google Scholar]
  48. Mortier-Barriere I., de Saizieu A., Claverys J. P., Martin B. 1998; Competence-specific induction of recA is required for full recombination proficiency during transformation in Streptococcus pneumoniae. Mol Microbiol 27:159–170 [CrossRef]
    [Google Scholar]
  49. Nouwens A. S., Cordwell S. J., Larsen M. R., Molloy M. P., Gillings M., Willcox M. D., Walsh B. J. 2000; Complementing genomics with proteomics: the membrane subproteome of Pseudomonas aeruginosa PAO1. Electrophoresis 21:3797–3809 [CrossRef]
    [Google Scholar]
  50. Paik S., Brown A., Munro C. L., Cornelissen C. N., Kitten T. 2003; The sloABCR operon of Streptococcus mutans encodes an Mn and Fe transport system required for endocarditis virulence and its Mn-dependent repressor. J Bacteriol 185:5967–5975 [CrossRef]
    [Google Scholar]
  51. Palmer R. J., Caldwell D. E. Jr 1995; A flow cell for the study of plaque-biofilm development. J Microb Methods 24:171–182 [CrossRef]
    [Google Scholar]
  52. Patel S. S., Picha K. M. 2000; Structure and function of hexameric helicases. Annu Rev Biochem 69:651–697 [CrossRef]
    [Google Scholar]
  53. Peterson S. N., Sung C. K., Cline R. & 13 other authors; 2004; Identification of competence pheromone responsive genes in Streptococcus pneumoniae by use of DNA microarrays. Mol Microbiol 51:1051–1070 [CrossRef]
    [Google Scholar]
  54. Sabounchi-Schutt F., Astrom J., Olsson I., Eklund A., Grunewald J., Bjellqvist B. 2000; An immobiline DryStrip application method enabling high-capacity two-dimensional gel electrophoresis. Electrophoresis 21:3649–3656 [CrossRef]
    [Google Scholar]
  55. Saier M. H., Chauvaux S., Cook G. M., Deutscher J., Paulsen I. T., Reizer J., Ye J. J. Jr 1996; Catabolite repression and inducer control in Gram-positive bacteria. Microbiology 142:217–230 [CrossRef]
    [Google Scholar]
  56. Schleifer K. H., Kilpper-Bälz R. 1987; Molecular and chemotaxonomic approaches to the classification of streptococci, enterococci and lactococci: a review. Syst Appl Microbiol 10:1–19 [CrossRef]
    [Google Scholar]
  57. Simpson C. L., Russell R. R. B. 1998; Identification of a homolog of CcpA catabolite repressor protein in Streptococcus mutans. Infect Immun 66:2085–2092
    [Google Scholar]
  58. Sissons C. H., Cutress T. W., Hoffman M. P., Wakefield J. S. 1991; A multi-station dental plaque microcosm (artificial mouth) for the study of plaque growth, metabolism, pH, and mineralization. J Dent Res 70:1409–1416 [CrossRef]
    [Google Scholar]
  59. Stanley N. R., Britton R. A., Grossman A. D., Lazazzera B. A. 2003; Identification of catabolite repression as a physiological regulator of biofilm formation by Bacillus subtilis by use of DNA microarrays. J Bacteriol 185:1951–1957 [CrossRef]
    [Google Scholar]
  60. Steffen S. E., Katz F. S., Bryant F. R. 2002; Complete inhibition of Streptococcus pneumoniae RecA protein-catalyzed ATP hydrolysis by single-stranded DNA-binding protein (SSB protein): implications for the mechanism of SSB protein-stimulated DNA strand exchange. J Biol Chem 277:14493–14500 [CrossRef]
    [Google Scholar]
  61. Stoodley P., Sauer K., Davies D. G., Costerton J. W. 2002; Biofilms as complex differentiated communities. Annu Rev Microbiol 56:187–209 [CrossRef]
    [Google Scholar]
  62. Suntharalingam P., Cvitkovitch D. G. 2005; Quorum sensing in streptococcal biofilm formation. Trends Microbiol 13:3–6 [CrossRef]
    [Google Scholar]
  63. Tao L., MacAlister T. J., Tanzer J. M. 1993; Transformation efficiency of EMS-induced mutants of Streptococcus mutans of altered cell shape. J Dent Res 72:1032–1039 [CrossRef]
    [Google Scholar]
  64. Vadeboncoeur C., Pelletier M. 1997; The phosphoenolpyruvate : sugar phospho-transferase system of oral streptococci and its role in the control of sugar metabolism. FEMS Microbiol Rev 19:187–207 [CrossRef]
    [Google Scholar]
  65. Vadeboncoeur C., St Martin S., Brochu D., Hamilton I. R. 1991; Effect of growth rate and pH on intracellular levels and activities of the components of the phosphoenolpyruvate : sugar phosphotransferase system in Streptococcus mutans Ingbritt. Infect Immun 59:900–906
    [Google Scholar]
  66. Velten M., McGovern S., Marsin S., Ehrlich S. D., Noirot P., Polard P. 2003; A two-protein strategy for the functional loading of a cellular replicative DNA helicase. Mol Cell 11:1009–1020 [CrossRef]
    [Google Scholar]
  67. Volkert M. R., Landini P. 2001; Transcriptional responses to DNA damage. Curr Opin Microbiol 4:178–185 [CrossRef]
    [Google Scholar]
  68. Welin J., Wilkins J. C., Beighton D., Wrzesinski K., Fey S. J., Mose-Larsen P., Hamilton I. R, Svensäter G. 2003; Effect of acid shock on protein expression by biofilm cells of Streptococcus mutans. FEMS Microbiol Lett 227:287–293 [CrossRef]
    [Google Scholar]
  69. Wen Z. T., Burne R. A. 2002; Functional genomics approach to identifying genes required for biofilm development by Streptococcus mutans. Appl Environ Microbiol 68:1196–1203 [CrossRef]
    [Google Scholar]
  70. Zalewska A., Zwierz K., Zolkowski K., Gindzienski A. 2000; Structure and biosynthesis of human salivary mucins. Acta Biochim Pol 47:1067–1079
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.27830-0
Loading
/content/journal/micro/10.1099/mic.0.27830-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error