1887

Abstract

is a pleiomorphic fungus that forms mixed species biofilms with , an early colonizer of oral cavity surfaces. Activation of quorum sensing (QS; intercellular signalling) promotes monospecies biofilm development by these micro-organisms, but the role of QS in mixed species communities is not understood. The genes in encode a sensor–regulator system (ComDE), which is activated by the gene product (CSP, competence stimulating peptide) and modulates expression of QS-regulated genes. Dual species biofilms of Δ or Δ mutants with showed increased biomass compared to biofilms of DL1 wild-type with . The Δ mutant dual species biofilms in particular contained more extracellular DNA (eDNA), and could be dispersed with DNase I or protease treatment. Exogenous CSP complemented the Δ transformation deficiency, as well as the Δ- biofilm phenotype. Purified CSP did not affect hyphal filament formation but inhibited monospecies biofilm formation by . The results suggest that the QS-system modulates the production of eDNA and the incorporation of into dual species biofilms.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000010
2015-02-01
2019-12-15
Loading full text...

Full text loading...

/deliver/fulltext/micro/161/2/411.html?itemId=/content/journal/micro/10.1099/mic.0.000010&mimeType=html&fmt=ahah

References

  1. Aas J. A., Paster B. J., Stokes L. N., Olsen I., Dewhirst F. E.. ( 2005;). Defining the normal bacterial flora of the oral cavity. . J Clin Microbiol 43:, 5721–5732. [CrossRef][PubMed]
    [Google Scholar]
  2. Bamford C. V., d’Mello A., Nobbs A. H., Dutton L. C., Vickerman M. M., Jenkinson H. F.. ( 2009;). Streptococcus gordonii modulates Candida albicans biofilm formation through intergeneric communication. . Infect Immun 77:, 3696–3704. [CrossRef][PubMed]
    [Google Scholar]
  3. Brittan J. L., Buckeridge T. J., Finn A., Kadioglu A., Jenkinson H. F.. ( 2012;). Pneumococcal neuraminidase A: an essential upper airway colonization factor for Streptococcus pneumoniae.. Mol Oral Microbiol 27:, 270–283. [CrossRef][PubMed]
    [Google Scholar]
  4. Clayton Y. M., Noble W. C.. ( 1966;). Observations on the epidemiology of Candida albicans.. J Clin Pathol 19:, 76–78. [CrossRef][PubMed]
    [Google Scholar]
  5. Cruz M. R., Graham C. E., Gagliano B. C., Lorenz M. C., Garsin D. A.. ( 2013;). Enterococcus faecalis inhibits hyphal morphogenesis and virulence of Candida albicans.. Infect Immun 81:, 189–200. [CrossRef][PubMed]
    [Google Scholar]
  6. Dewhirst F. E., Chen T., Izard J., Paster B. J., Tanner A. C. R., Yu W.-H., Lakshmanan A., Wade W. G.. ( 2010;). The human oral microbiome. . J Bacteriol 192:, 5002–5017. [CrossRef][PubMed]
    [Google Scholar]
  7. Dutton L. C., Nobbs A. H., Jepson K., Jepson M. A., Vickerman M. M., Aqeel Alawfi S., Munro C. A., Lamont R. J., Jenkinson H. F.. ( 2014;). O-mannosylation in Candida albicans enables development of interkingdom biofilm communities. . MBio 5:, e00911. [CrossRef][PubMed]
    [Google Scholar]
  8. Falsetta M. L., Klein M. I., Colonne P. M., Scott-Anne K., Gregoire S., Pai C. H., Gonzalez-Begne M., Watson G., Krysan D. J.. & other authors ( 2014;). Symbiotic relationship between Streptococcus mutans and Candida albicans synergizes virulence of plaque biofilms in vivo.. Infect Immun 82:, 1968–1981. [CrossRef][PubMed]
    [Google Scholar]
  9. Flemming H. C., Wingender J.. ( 2010;). The biofilm matrix. . Nat Rev Microbiol 8:, 623–633.[PubMed]
    [Google Scholar]
  10. Foster J. S., Kolenbrander P. E.. ( 2004;). Development of a multispecies oral bacterial community in a saliva-conditioned flow cell. . Appl Environ Microbiol 70:, 4340–4348. [CrossRef][PubMed]
    [Google Scholar]
  11. Haisman R. J., Jenkinson H. F.. ( 1991;). Mutants of Streptococcus gordonii Challis over-producing glucosyltransferase. . J Gen Microbiol 137:, 483–489. [CrossRef][PubMed]
    [Google Scholar]
  12. Håvarstein L. S., Gaustad P., Nes I. F., Morrison D. A.. ( 1996;). Identification of the streptococcal competence-pheromone receptor. . Mol Microbiol 21:, 863–869. [CrossRef][PubMed]
    [Google Scholar]
  13. Heng N. C., Tagg J. R., Tompkins G. R.. ( 2006;). Identification and characterization of the loci encoding the competence-associated alternative sigma factor of Streptococcus gordonii. . FEMS Microbiol Lett 259:, 27–34. [CrossRef][PubMed]
    [Google Scholar]
  14. Hogan D. A., Vik A., Kolter R.. ( 2004;). A Pseudomonas aeruginosa quorum-sensing molecule influences Candida albicans morphology. . Mol Microbiol 54:, 1212–1223. [CrossRef][PubMed]
    [Google Scholar]
  15. Jarosz L. M., Deng D. M., van der Mei H. C., Crielaard W., Krom B. P.. ( 2009;). Streptococcus mutans competence-stimulating peptide inhibits Candida albicans hypha formation. . Eukaryot Cell 8:, 1658–1664. [CrossRef][PubMed]
    [Google Scholar]
  16. Kanasi E., Dewhirst F. E., Chalmers N. I., Kent R. Jr, Moore A., Hughes C. V., Pradhan N., Loo C. Y., Tanner A. C. R.. ( 2010;). Clonal analysis of the microbiota of severe early childhood caries. . Caries Res 44:, 485–497. [CrossRef][PubMed]
    [Google Scholar]
  17. 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. . Microbiology 148:, 1627–1636.[PubMed]
    [Google Scholar]
  18. Lee M. S., Morrison D. A.. ( 1999;). Identification of a new regulator in Streptococcus pneumoniae linking quorum sensing to competence for genetic transformation. . J Bacteriol 181:, 5004–5016.[PubMed]
    [Google Scholar]
  19. Lembke C., Podbielski A., Hidalgo-Grass C., Jonas L., Hanski E., Kreikemeyer B.. ( 2006;). Characterization of biofilm formation by clinically relevant serotypes of group A streptococci. . Appl Environ Microbiol 72:, 2864–2875. [CrossRef][PubMed]
    [Google Scholar]
  20. 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][PubMed]
    [Google Scholar]
  21. Liao S., Klein M. I., Heim K. P., Fan Y., Bitoun J. P., Ahn S. J., Burne R. A., Koo H., Brady L. J., Wen Z. T.. ( 2014;). 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. [CrossRef][PubMed]
    [Google Scholar]
  22. Liu Y., Burne R. A.. ( 2011;). The major autolysin of Streptococcus gordonii is subject to complex regulation and modulates stress tolerance, biofilm formation, and extracellular-DNA release. . J Bacteriol 193:, 2826–2837. [CrossRef][PubMed]
    [Google Scholar]
  23. Liu X., Ramsey M. M., Chen X., Koley D., Whiteley M., Bard A. J.. ( 2011;). Real-time mapping of a hydrogen peroxide concentration profile across a polymicrobial bacterial biofilm using scanning electrochemical microscopy. . Proc Natl Acad Sci U S A 108:, 2668–2673. [CrossRef][PubMed]
    [Google Scholar]
  24. Lu Y., Su C., Unoje O., Liu H.. ( 2014;). Quorum sensing controls hyphal initiation in Candida albicans through Ubr1-mediated protein degradation. . Proc Natl Acad Sci U S A 111:, 1975–1980. [CrossRef][PubMed]
    [Google Scholar]
  25. Martins M., Uppuluri P., Thomas D. P., Cleary I. A., Henriques M., Lopez-Ribot J. L., Oliveira R.. ( 2010;). Presence of extracellular DNA in the Candida albicans biofilm matrix and its contribution to biofilms. . Mycopathologia 169:, 323–331. [CrossRef][PubMed]
    [Google Scholar]
  26. Mashburn-Warren L., Morrison D. A., Federle M. J.. ( 2010;). A novel double-tryptophan peptide pheromone controls competence in Streptococcus spp. via an Rgg regulator. . Mol Microbiol 78:, 589–606. [CrossRef][PubMed]
    [Google Scholar]
  27. 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 Bacteriol 185:, 274–284. [CrossRef][PubMed]
    [Google Scholar]
  28. Merritt J., Qi F.. ( 2012;). The mutacins of Streptococcus mutans: regulation and ecology. . Mol Oral Microbiol 27:, 57–69. [CrossRef][PubMed]
    [Google Scholar]
  29. Milne S. W., Cheetham J., Lloyd D., Aves S., Bates S.. ( 2011;). Cassettes for PCR-mediated gene tagging in Candida albicans utilizing nourseothricin resistance. . Yeast 28:, 833–841. [CrossRef][PubMed]
    [Google Scholar]
  30. Naseem S., Gunasekera A., Araya E., Konopka J. B.. ( 2011;). N-acetylglucosamine (GlcNAc) induction of hyphal morphogenesis and transcriptional responses in Candida albicans are not dependent on its metabolism. . J Biol Chem 286:, 28671–28680. [CrossRef][PubMed]
    [Google Scholar]
  31. Nobbs A. H., Vickerman M. M., Jenkinson H. F.. ( 2010;). Heterologous expression of Candida albicans cell wall-associated adhesins in Saccharomyces cerevisiae reveals differential specificities in adherence and biofilm formation and in binding oral Streptococcus gordonii.. Eukaryot Cell 9:, 1622–1634. [CrossRef][PubMed]
    [Google Scholar]
  32. Nyvad B., Kilian M.. ( 1990;). Comparison of the initial streptococcal microflora on dental enamel in caries-active and in caries-inactive individuals. . Caries Res 24:, 267–272. [CrossRef][PubMed]
    [Google Scholar]
  33. Okshevsky M., Meyer R. L.. ( 2013;). The role of extracellular DNA in the establishment, maintenance and perpetuation of bacterial biofilms. . Crit Rev Microbiol 1–11. [CrossRef][PubMed]
    [Google Scholar]
  34. Palmer R. J. Jr, Gordon S. M., Cisar J. O., Kolenbrander P. E.. ( 2003;). Coaggregation-mediated interactions of streptococci and actinomyces detected in initial human dental plaque. . J Bacteriol 185:, 3400–3409. [CrossRef][PubMed]
    [Google Scholar]
  35. Pammi M., Liang R., Hicks J., Mistretta T. A., Versalovic J.. ( 2013;). Biofilm extracellular DNA enhances mixed species biofilms of Staphylococcus epidermidis and Candida albicans.. BMC Microbiol 13:, 257. [CrossRef][PubMed]
    [Google Scholar]
  36. PHE ( 2013;). Voluntary surveillance of candidaemia in England, Wales and Northern Ireland: 2012. . Health Protection Report 7. HCAI.
    [Google Scholar]
  37. Piotrowski A., Luo P., Morrison D. A.. ( 2009;). Competence for genetic transformation in Streptococcus pneumoniae: termination of activity of the alternative sigma factor ComX is independent of proteolysis of ComX and ComW. . J Bacteriol 191:, 3359–3366. [CrossRef][PubMed]
    [Google Scholar]
  38. Podbielski A., Spellerberg B., Woischnik M., Pohl B., Lütticken R.. ( 1996;). Novel series of plasmid vectors for gene inactivation and expression analysis in group A streptococci (GAS). . Gene 177:, 137–147. [CrossRef][PubMed]
    [Google Scholar]
  39. Ricker A., Vickerman M., Dongari-Bagtzoglou A.. ( 2014;). Streptococcus gordonii glucosyltransferase promotes biofilm interactions with Candida albicans.. J Oral Microbiol 6:, 23419. [CrossRef][PubMed]
    [Google Scholar]
  40. Sapaar B., Nur A., Hirota K., Yumoto H., Murakami K., Amoh T., Matsuo T., Ichikawa T., Miyake Y.. ( 2014;). Effects of extracellular DNA from Candida albicans and pneumonia-related pathogens on Candida biofilm formation and hyphal transformation. . J Appl Microbiol 116:, 1531–1542. [CrossRef][PubMed]
    [Google Scholar]
  41. Shak J. R., Vidal J. E., Klugman K. P.. ( 2013;). Influence of bacterial interactions on pneumococcal colonization of the nasopharynx. . Trends Microbiol 21:, 129–135. [CrossRef][PubMed]
    [Google Scholar]
  42. Silverman R. J., Nobbs A. H., Vickerman M. M., Barbour M. E., Jenkinson H. F.. ( 2010;). Interaction of Candida albicans cell wall Als3 protein with Streptococcus gordonii SspB adhesin promotes development of mixed-species communities. . Infect Immun 78:, 4644–4652. [CrossRef][PubMed]
    [Google Scholar]
  43. Son M., Ahn S.-J., Guo Q., Burne R. A., Hagen S. J.. ( 2012;). Microfluidic study of competence regulation in Streptococcus mutans: environmental inputs modulate bimodal and unimodal expression of comX. . Mol Microbiol 86:, 258–272. [CrossRef][PubMed]
    [Google Scholar]
  44. Sztajer H., Szafranski S. P., Tomasch J., Reck M., Nimtz M., Rohde M., Wagner-Döbler I.. ( 2014;). Cross-feeding and interkingdom communication in dual-species biofilms of Streptococcus mutans and Candida albicans.. ISME J 8:, 2256–2271. [CrossRef][PubMed]
    [Google Scholar]
  45. Taff H. T., Mitchell K. F., Edward J. A., Andes D. R.. ( 2013;). Mechanisms of Candida biofilm drug resistance. . Future Microbiol 8:, 1325–1337. [CrossRef][PubMed]
    [Google Scholar]
  46. 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 Bacteriol 189:, 7799–7807. [CrossRef][PubMed]
    [Google Scholar]
  47. Wei H., Håvarstein L. S.. ( 2012;). Fratricide is essential for efficient gene transfer between pneumococci in biofilms. . Appl Environ Microbiol 78:, 5897–5905. [CrossRef][PubMed]
    [Google Scholar]
  48. Whitmore S. E., Lamont R. J.. ( 2011;). The pathogenic persona of community-associated oral streptococci. . Mol Microbiol 81:, 305–314. [CrossRef][PubMed]
    [Google Scholar]
  49. Wisplinghoff H., Bischoff T., Tallent S. M., Seifert H., Wenzel R. P., Edmond M. B.. ( 2004;). Nosocomial bloodstream infections in US hospitals: analysis of 24,179 cases from a prospective nationwide surveillance study. . Clin Infect Dis 39:, 309–317. [CrossRef][PubMed]
    [Google Scholar]
  50. Wright C. J., Burns L. H., Jack A. A., Back C. R., Dutton L. C., Nobbs A. H., Lamont R. J., Jenkinson H. F.. ( 2013;). Microbial interactions in building of communities. . Mol Oral Microbiol 28:, 83–101. [CrossRef][PubMed]
    [Google Scholar]
  51. Xie Z., Thompson A., Sobue T., Kashleva H., Xu H., Vasilakos J., Dongari-Bagtzoglou A.. ( 2012;). Candida albicans biofilms do not trigger reactive oxygen species and evade neutrophil killing. . J Infect Dis 206:, 1936–1945. [CrossRef][PubMed]
    [Google Scholar]
  52. Xu Y., Kreth J.. ( 2013;). Role of LytF and AtlS in eDNA release by Streptococcus gordonii.. PLoS ONE 8:, e62339. [CrossRef][PubMed]
    [Google Scholar]
  53. Xu H., Jenkinson H. F., Dongari-Bagtzoglou A.. ( 2014a;). Innocent until proven guilty: mechanisms and roles of Streptococcus-Candida interactions in oral health and disease. . Mol Oral Microbiol 29:, 99–116. [CrossRef][PubMed]
    [Google Scholar]
  54. Xu H., Sobue T., Thompson A., Xie Z., Poon K., Ricker A., Cervantes J., Diaz P. I., Dongari-Bagtzoglou A.. ( 2014b;). Streptococcal co-infection augments Candida pathogenicity by amplifying the mucosal inflammatory response. . Cell Microbiol 16:, 214–231. [CrossRef][PubMed]
    [Google Scholar]
  55. Zarnowski R., Westler W. M., Lacmbouh G. A., Marita J. M., Bothe J. R., Bernhardt J., Lounes-Hadj Sahraoui A., Fontaine J., Sanchez H.. & other authors ( 2014;). Novel entries in a fungal biofilm matrix encyclopedia. . MBio 5:, e01333–e14. [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000010
Loading
/content/journal/micro/10.1099/mic.0.000010
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