1887

Abstract

The putative two-component system BfrAB is involved in biofilm development. Here, we provide evidence that BfrAB regulates the expression of and , which encode two ATP-binding cassette (ABC) transporters, and , which encodes a CAAX amino-terminal protease family protein. BfrC and BfrE are ATP-binding proteins, and BfrD, BfrF and BfrG are homologous membrane-spanning polypeptides. Similarly, BfrAB, the BfrAB homologous system in , controls the expression of two -homologous operons ( and ), a -homologous gene ( ) and another CAAX amino-terminal protease family protein gene (). Furthermore, we demonstrate that the purified BfrA DNA-binding domain from binds to the promoter regions of , , , , and . Finally, we show that the BfrA DNA-binding domain recognizes a conserved DNA motif with a consensus sequence of TTTCTTTAGAAATATTTTAGAATT. These data suggest, therefore, that BfrAB controls biofilm formation by regulating multiple ABC-transporter systems.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.023168-0
2009-01-01
2020-04-08
Loading full text...

Full text loading...

/deliver/fulltext/micro/155/1/165.html?itemId=/content/journal/micro/10.1099/mic.0.023168-0&mimeType=html&fmt=ahah

References

  1. Altschul S. F., Madden T. L., Schaffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J.. 1997; Gapped blast and psi-blast: a new generation of protein database search programs. Nucleic Acids Res25:3389–3402
    [Google Scholar]
  2. Bayliss R., Clarke C., Oakley C. M., Somerville W., Whitfield A. G., Young S. E.. 1983; The microbiology and pathogenesis of infective endocarditis. Br Heart J50:513–519
    [Google Scholar]
  3. Bhagwat S. P., Nary J., Burne R. A.. 2001; Effects of mutating putative two-component systems on biofilm formation by Streptococcus mutans UA159. FEMS Microbiol Lett205:225–230
    [Google Scholar]
  4. Brooks W., Demuth D. R., Gil S., Lamont R. J.. 1997; Identification of a Streptococcus gordonii SspB domain that mediates adhesion to Porphyromonas gingivalis. Infect Immun65:3753–3758
    [Google Scholar]
  5. Brown S. A., Whiteley M.. 2007; A novel exclusion mechanism for carbon resource partitioning in Aggregatibacter actinomycetemcomitans. J Bacteriol189:6407–6414
    [Google Scholar]
  6. Chung W. O., Demuth D. R., Lamont R. J.. 2000; Identification of a Porphyromonas gingivalis receptor for the Streptococcus gordonii SspB protein. Infect Immun68:6758–6762
    [Google Scholar]
  7. Decottignies A., Goffeau A.. 1997; Complete inventory of the yeast ABC proteins. Nat Genet15:137–145
    [Google Scholar]
  8. Dorel C., Vidal O., Prigent-Combaret C., Vallet I., Lejeune P.. 1999; Involvement of the Cpx signal transduction pathway of E. coli in biofilm formation. FEMS Microbiol Lett178:169–175
    [Google Scholar]
  9. Dunny G. M., Lee L. N., LeBlanc D. J.. 1991; Improved electroporation and cloning vector system for Gram-positive bacteria. Appl Environ Microbiol57:1194–1201
    [Google Scholar]
  10. Fournier B., Hooper D. C.. 2000; A new two-component regulatory system involved in adhesion, autolysis, and extracellular proteolytic activity of Staphylococcus aureus. J Bacteriol182:3955–3964
    [Google Scholar]
  11. Frandsen E. V., Pedrazzoli V., Kilian M.. 1991; Ecology of viridans streptococci in the oral cavity and pharynx. Oral Microbiol Immunol6:129–133
    [Google Scholar]
  12. Hancock L. E., Perego M.. 2004; The Enterococcus faecalis fsr two-component system controls biofilm development through production of gelatinase. J Bacteriol186:5629–5639
    [Google Scholar]
  13. Havarstein L. S., Gaustad P., Nes I. F., Morrison D. A.. 1996; Identification of the streptococcal competence-pheromone receptor. Mol Microbiol21:863–869
    [Google Scholar]
  14. Herzberg M. C.. 1996; Platelet–streptococcal interactions in endocarditis. Crit Rev Oral Biol Med7:222–236
    [Google Scholar]
  15. Higgins C. F.. 1992; ABC transporters: from microorganisms to man. Annu Rev Cell Biol8:67–113
    [Google Scholar]
  16. Holland I. B., Blight M. A.. 1999; ABC-ATPases, adaptable energy generators fuelling transmembrane movement of a variety of molecules in organisms from bacteria to humans. J Mol Biol293:381–399
    [Google Scholar]
  17. Jones P. M., George A. M.. 2004; The ABC transporter structure and mechanism: perspectives on recent research. Cell Mol Life Sci61:682–699
    [Google Scholar]
  18. Kilian M., Holmgren K.. 1981; Ecology and nature of immunoglobulin A1 protease-producing streptococci in the human oral cavity and pharynx. Infect Immun31:868–873
    [Google Scholar]
  19. Kuboniwa M., Tribble G. D., James C. E., Kilic A. O., Tao L., Herzberg M. C., Shizukuishi S., Lamont R. J.. 2006; Streptococcus gordonii utilizes several distinct gene functions to recruit Porphyromonas gingivalis into a mixed community. Mol Microbiol60:121–139
    [Google Scholar]
  20. Lamont R. J., El-Sabaeny A., Park Y., Cook G. S., Costerton J. W., Demuth D. R.. 2002; Role of the Streptococcus gordonii SspB protein in the development of Porphyromonas gingivalis biofilms on streptococcal substrates. Microbiology148:1627–1636
    [Google Scholar]
  21. Li Y. H., Lau P. C., Tang N., Svensater G., Ellen R. P., Cvitkovitch D. G.. 2002; Novel two-component regulatory system involved in biofilm formation and acid resistance in Streptococcus mutans. J Bacteriol184:6333–6342
    [Google Scholar]
  22. Loo C. Y., Corliss D. A., Ganeshkumar N.. 2000; Streptococcus gordonii biofilm formation: identification of genes that code for biofilm phenotypes. J Bacteriol182:1374–1382
    [Google Scholar]
  23. Lunsford R. D.. 1998; Streptococcal transformation: essential features and applications of a natural gene exchange system. Plasmid39:10–20
    [Google Scholar]
  24. Macrina F. L., Evans R. P., Tobian J. A., Hartley D. L., Clewell D. B., Jones K. R.. 1983; Novel shuttle plasmid vehicles for Escherichia–Streptococcus transgeneric cloning. Gene25:145–150
    [Google Scholar]
  25. Manford M., Matharu J., Farrington K.. 1992; Infective endocarditis in a district general hospital. J R Soc Med85:262–266
    [Google Scholar]
  26. McNab R., Ford S. K., El-Sabaeny A., Barbieri B., Cook G. S., Lamont R. J.. 2003; LuxS-based signaling in Streptococcus gordonii: autoinducer 2 controls carbohydrate metabolism and biofilm formation with Porphyromonas gingivalis. J Bacteriol185:274–284
    [Google Scholar]
  27. Nambu Y., Sugai M., Gonda H., Lee C. G., Katakai T., Agata Y., Yokota Y., Shimizu A.. 2003; Transcription-coupled events associating with immunoglobulin switch region chromatin. Science302:2137–2140
    [Google Scholar]
  28. Nobbs A. H., Vajna R. M., Johnson J. R., Zhang Y., Erlandsen S. L., Oli M. W., Kreth J., Brady L. J., Herzberg M. C.. 2007; Consequences of a sortase A mutation in Streptococcus gordonii. Microbiology153:4088–4097
    [Google Scholar]
  29. Nyvad B., Kilian M.. 1987; Microbiology of the early colonization of human enamel and root surfaces in vivo. Scand J Dent Res95:369–380
    [Google Scholar]
  30. Nyvad B., Kilian M.. 1990; Comparison of the initial streptococcal microflora on dental enamel in caries-active and in caries-inactive individuals. Caries Res24:267–272
    [Google Scholar]
  31. Otto K., Silhavy T. J.. 2002; Surface sensing and adhesion of Escherichia coli controlled by the Cpx-signaling pathway. Proc Natl Acad Sci U S A99:2287–2292
    [Google Scholar]
  32. Palmer K. L., Mashburn L. M., Singh P. K., Whiteley M.. 2005; Cystic fibrosis sputum supports growth and cues key aspects of Pseudomonas aeruginosa physiology. J Bacteriol187:5267–5277
    [Google Scholar]
  33. Park Y., Simionato M. R., Sekiya K.. other authors 2005; Short fimbriae of Porphyromonas gingivalis and their role in coadhesion with Streptococcus gordonii. Infect Immun73:3983–3989
    [Google Scholar]
  34. Parkins M. D., Ceri H., Storey D. G.. 2001; Pseudomonas aeruginosa GacA, a factor in multihost virulence, is also essential for biofilm formation. Mol Microbiol40:1215–1226
    [Google Scholar]
  35. Pei J., Grishin N. V.. 2001; Type II CAAX prenyl endopeptidases belong to a novel superfamily of putative membrane-bound metalloproteases. Trends Biochem Sci26:275–277
    [Google Scholar]
  36. Podlesek Z., Comino A., Herzog-Velikonja B., Zgur-Bertok D., Komel R., Grabnar M.. 1995; Bacillus licheniformis bacitracin-resistance ABC transporter: relationship to mammalian multidrug resistance. Mol Microbiol16:969–976
    [Google Scholar]
  37. Prigent-Combaret C., Vidal O., Dorel C., Lejeune P.. 1999; Abiotic surface sensing and biofilm-dependent regulation of gene expression in Escherichia coli. J Bacteriol181:5993–6002
    [Google Scholar]
  38. Rosan B., Lamont R. J.. 2000; Dental plaque formation. Microbes Infect2:1599–1607
    [Google Scholar]
  39. Sambrook J., Fritsch E. F., Maniatis T.. 1989; Molecular Cloning: a Laboratory Manual , 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  40. Schaffer A. A., Aravind L., Madden T. L., Shavirin S., Spouge J. L., Wolf Y. I., Koonin E. V., Altschul S. F.. 2001; Improving the accuracy of psi-blast protein database searches with composition-based statistics and other refinements. Nucleic Acids Res29:2994–3005
    [Google Scholar]
  41. Shemesh M., Tam A., Steinberg D.. 2007; Differential gene expression profiling of Streptococcus mutans cultured under biofilm and planktonic conditions. Microbiology153:1307–1317
    [Google Scholar]
  42. Simionato M. R., Tucker C. M., Kuboniwa M., Lamont G., Demuth D. R., Tribble G. D., Lamont R. J.. 2006; Porphyromonas gingivalis genes involved in community development with Streptococcus gordonii. Infect Immun74:6419–6428
    [Google Scholar]
  43. Socransky S. S., Haffajee A. D., Cugini M. A., Smith C., Kent R. L. Jr. 1998; Microbial complexes in subgingival plaque. J Clin Periodontol25:134–144
    [Google Scholar]
  44. Stock A. M., Robinson V. L., Goudreau P. N.. 2000; Two-component signal transduction. Annu Rev Biochem69:183–215
    [Google Scholar]
  45. Tao L., Herzberg M. C.. 1999; Identifying in vivo expressed streptococcal genes in endocarditis. Methods Enzymol310:109–116
    [Google Scholar]
  46. Terleckyj B., Shockman G. D.. 1975; Amino acid requirements of Streptococcus mutans and other oral streptococci. Infect Immun11:656–664
    [Google Scholar]
  47. 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
    [Google Scholar]
  48. Toledo-Arana A., Merino N., Vergara-Irigaray M., Debarbouille M., Penades J. R., Lasa I.. 2005; Staphylococcus aureus develops an alternative, ica-independent biofilm in the absence of the arlRS two-component system. J Bacteriol187:5318–5329
    [Google Scholar]
  49. Vickerman M. M., Iobst S., Jesionowski A. M., Gill S. R.. 2007; Genome-wide transcriptional changes in Streptococcus gordonii in response to competence signaling peptide. J Bacteriol189:7799–7807
    [Google Scholar]
  50. Zhang Y., Lei Y., Khammanivong A., Herzberg M. C.. 2004; Identification of a novel two-component system in Streptococcus gordonii V288 involved in biofilm formation. Infect Immun72:3489–3494
    [Google Scholar]
  51. Zhang Y., Lei Y., Nobbs A., Khammanivong A., Herzberg M. C.. 2005; Inactivation of Streptococcus gordonii SspAB alters expression of multiple adhesin genes. Infect Immun73:3351–3357
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.023168-0
Loading
/content/journal/micro/10.1099/mic.0.023168-0
Loading

Data & Media loading...

Most cited this month

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