Home LiteratureArticle Details
PMID: 11976299 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

A quorum-sensing signaling system essential for genetic competence in Streptococcus mutans is involved in biofilm formation.

Journal of bacteriology ·Vol. 184 ·No. 10 ·2002-05-00 ·Pages 2699-708

Li YH, Tang N, Aspiras MB, Lau PC, Lee JH, Ellen RP, Cvitkovitch DG

Abstract

In a previous study, a quorum-sensing signaling system essential for genetic competence in Streptococcus mutans was identified, characterized, and found to function optimally in biofilms (Li et al., J. Bacteriol. 183:897-908, 2001). Here, we demonstrate that this system also plays a role in the ability of S. mutans to initiate biofilm formation. To test this hypothesis, S. mutans wild-type strain NG8 and its knockout mutants defective in comC, comD, comE, and comX, as well as a comCDE deletion mutant, were assayed for their ability to initiate biofilm formation. The spatial distribution and architecture of the biofilms were examined by scanning electron microscopy and confocal scanning laser microscopy. The results showed that inactivation of any of the individual genes under study resulted in the formation of an abnormal biofilm. The comC mutant, unable to produce or secrete a competence-stimulating peptide (CSP), formed biofilms with altered architecture, whereas the comD and comE mutants, which were defective in sensing and responding to the CSP, formed biofilms with reduced biomass. Exogenous addition of the CSP and complementation with a plasmid containing the wild-type comC gene into the cultures restored the wild-type biofilm architecture of comC mutants but showed no effect on the comD, comE, or comX mutant biofilms. The fact that biofilms formed by comC mutants differed from the comD, comE, and comX mutant biofilms suggested that multiple signal transduction pathways were affected by CSP. Addition of synthetic CSP into the culture medium or introduction of the wild-type comC gene on a shuttle vector into the comCDE deletion mutant partially restored the wild-type biofilm architecture and further supported this idea. We conclude that the quorum-sensing signaling system essential for genetic competence in S. mutans is important for the formation of biofilms by this gram-positive organism.

MeSH Terms
Bacterial Proteins/physiology Biofilms DNA-Binding Proteins/physiology Gene Expression Regulation, Bacterial Streptococcus mutans/genetics,physiology
Chemicals
Bacterial Proteins ComA protein, Bacteria DNA-Binding Proteins
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Li Yung-Hua
Dental Research Institute, University of Toronto, 124 Edward Street, Toronto, Ontario, Canada M5G 1G6.
Tang Nan
Aspiras Marcelo B
Lau Peter C Y
Lee Janet H
Ellen Richard P
Cvitkovitch Dennis G
References (41)
41 references, click to expand
  1. The com locus controls genetic transformation in Streptococcus pneumoniae.
    Mol Microbiol. 1997 Feb;23(4):683-92 PMID: 9157240
  2. The intercellular adhesion (ica) locus is present in Staphylococcus aureus and is required for biofilm formation.
    Infect Immun. 1999 Oct;67(10):5427-33 PMID: 10496925
  3. Quorum sensing by peptide pheromones and two-component signal-transduction systems in Gram-positive bacteria.
    Mol Microbiol. 1997 Jun;24(5):895-904 PMID: 9219998
  4. Cell-cell communication in gram-positive bacteria.
    Annu Rev Microbiol. 1997;51:527-64 PMID: 9343359
  5. Growth dynamics in a natural biofilm and its impact on oral disease management.
    Adv Dent Res. 1997 Apr;11(1):14-23 PMID: 9524438
  6. Analysis of gene expression in Streptococcus mutans in biofilms in vitro.
    Adv Dent Res. 1997 Apr;11(1):100-9 PMID: 9524447
  7. The involvement of cell-to-cell signals in the development of a bacterial biofilm.
    Science. 1998 Apr 10;280(5361):295-8 PMID: 9535661
  8. Streptococcus gordonii biofilm formation: identification of genes that code for biofilm phenotypes.
    J Bacteriol. 2000 Mar;182(5):1374-82 PMID: 10671461
  9. Acyl-homoserine lactone quorum sensing in gram-negative bacteria: a signaling mechanism involved in associations with higher organisms.
    Proc Natl Acad Sci U S A. 2000 Aug 1;97(16):8789-93 PMID: 10922036
  10. Microarray-based identification of a novel Streptococcus pneumoniae regulon controlled by an autoinduced peptide.
    J Bacteriol. 2000 Sep;182(17):4696-703 PMID: 10940007
  11. Bacterial quorum sensing in pathogenic relationships.
    Infect Immun. 2000 Sep;68(9):4839-49 PMID: 10948095
  12. Biofilm formation as microbial development.
    Annu Rev Microbiol. 2000;54:49-79 PMID: 11018124
  13. Gene expression analysis of the Streptococcus pneumoniae competence regulons by use of DNA microarrays.
    J Bacteriol. 2000 Nov;182(21):6192-202 PMID: 11029442
  14. Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms.
    Nature. 2000 Oct 12;407(6805):762-4 PMID: 11048725
  15. Genetic transformation in Streptococcus mutans requires a peptide secretion-like apparatus.
    Oral Microbiol Immunol. 2000 Oct;15(5):329-34 PMID: 11154426
  16. Natural genetic transformation of Streptococcus mutans growing in biofilms.
    J Bacteriol. 2001 Feb;183(3):897-908 PMID: 11208787
  17. Cell density modulates acid adaptation in Streptococcus mutans: implications for survival in biofilms.
    J Bacteriol. 2001 Dec;183(23):6875-84 PMID: 11698377
  18. Effects of mutating putative two-component systems on biofilm formation by Streptococcus mutans UA159.
    FEMS Microbiol Lett. 2001 Dec 18;205(2):225-30 PMID: 11750807
  19. Prevalence of Streptococcus sanguis and Streptococcus mutans in the mouth of persons wearing full-dentures.
    Arch Oral Biol. 1969 Mar;14(3):243-9 PMID: 5255438
  20. Biology, immunology, and cariogenicity of Streptococcus mutans.
    Microbiol Rev. 1980 Jun;44(2):331-84 PMID: 6446023
  21. Biological role of the pneumococcal amidase. Cloning of the lytA gene in Streptococcus pneumoniae.
    Eur J Biochem. 1987 May 4;164(3):621-4 PMID: 3569279
  22. Construction and characterization of isogenic mutants of Streptococcus mutans deficient in major surface protein antigen P1 (I/II).
    Infect Immun. 1989 Nov;57(11):3306-13 PMID: 2807526
  23. Optical sectioning of microbial biofilms.
    J Bacteriol. 1991 Oct;173(20):6558-67 PMID: 1917879
  24. Molecular, genetic, and functional analysis of the basic replicon of pVA380-1, a plasmid of oral streptococcal origin.
    Plasmid. 1992 Sep;28(2):130-45 PMID: 1409970
  25. Growth phase-dependent regulation and membrane localization of SpaB, a protein involved in biosynthesis of the lantibiotic subtilin.
    Appl Environ Microbiol. 1994 Jan;60(1):1-11 PMID: 8117069
  26. Glucose transport by a mutant of Streptococcus mutans unable to accumulate sugars via the phosphoenolpyruvate phosphotransferase system.
    J Bacteriol. 1995 May;177(9):2251-8 PMID: 7730250
  27. Use of a novel mobilizable vector to inactivate the scrA gene of Streptococcus sobrinus by allelic replacement.
    J Bacteriol. 1995 Sep;177(17):5028-34 PMID: 7665480
  28. Construction and evaluation of new drug-resistance cassettes for gene disruption mutagenesis in Streptococcus pneumoniae, using an ami test platform.
    Gene. 1995 Oct 16;164(1):123-8 PMID: 7590300
  29. Characteristics of accumulation of oral gram-positive bacteria on mucin-conditioned glass surfaces in a model system.
    Oral Microbiol Immunol. 1994 Feb;9(1):1-11 PMID: 7478748
  30. An unmodified heptadecapeptide pheromone induces competence for genetic transformation in Streptococcus pneumoniae.
    Proc Natl Acad Sci U S A. 1995 Nov 21;92(24):11140-4 PMID: 7479953
  31. Cell density control of staphylococcal virulence mediated by an octapeptide pheromone.
    Proc Natl Acad Sci U S A. 1995 Dec 19;92(26):12055-9 PMID: 8618843
  32. Microbial biofilms.
    Annu Rev Microbiol. 1995;49:711-45 PMID: 8561477
  33. Adherence, accumulation, and cell division of a natural adherent bacterial population.
    J Bacteriol. 1996 Feb;178(4):1172-7 PMID: 8576054
  34. Detachment of Streptococcus mutans biofilm cells by an endogenous enzymatic activity.
    Infect Immun. 1996 Mar;64(3):1035-8 PMID: 8641755
  35. Genetic networks controlling the initiation of sporulation and the development of genetic competence in Bacillus subtilis.
    Annu Rev Genet. 1995;29:477-508 PMID: 8825484
  36. Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis.
    Mol Microbiol. 1998 May;28(3):449-61 PMID: 9632250
  37. Thinking about bacterial populations as multicellular organisms.
    Annu Rev Microbiol. 1998;52:81-104 PMID: 9891794
  38. Quorum sensing in Escherichia coli, Salmonella typhimurium, and Vibrio harveyi: a new family of genes responsible for autoinducer production.
    Proc Natl Acad Sci U S A. 1999 Feb 16;96(4):1639-44 PMID: 9990077
  39. Identification of a new regulator in Streptococcus pneumoniae linking quorum sensing to competence for genetic transformation.
    J Bacteriol. 1999 Aug;181(16):5004-16 PMID: 10438773
  40. Identification of DNA binding sites for ComE, a key regulator of natural competence in Streptococcus pneumoniae.
    Mol Microbiol. 1999 Aug;33(4):817-27 PMID: 10447890
  41. Two alternative mechanisms of cell separation in staphylococci: one lytic and one mechanical.
    Arch Microbiol. 1997 Apr;167(4):239-50 PMID: 9075623
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
Published
2002-05-00
Pages
2699-708
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC135014
Subset
IM
Grants
NIDCR NIH HHS · R01 DE013230 · United States
NIDCR NIH HHS · DE 013230-02 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com