Home LiteratureArticle Details
PMID: 15978073 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Co-ordinated bacteriocin production and competence development: a possible mechanism for taking up DNA from neighbouring species.

Molecular microbiology ·Vol. 57 ·No. 2 ·2005-07-00 ·Pages 392-404

Kreth J, Merritt J, Shi W, Qi F

Abstract

It is important to ensure DNA availability when bacterial cells develop competence. Previous studies in Streptococcus pneumoniae demonstrated that the competence-stimulating peptide (CSP) induced autolysin production and cell lysis of its own non-competent cells, suggesting a possible active mechanism to secure a homologous DNA pool for uptake and recombination. In this study, we found that in Streptococcus mutans CSP induced co-ordinated expression of competence and mutacin production genes. This mutacin (mutacin IV) is a non-lantibiotic bacteriocin which kills closely related Streptococcal species such as S. gordonii. In mixed cultures of S. mutans and S. gordonii harbouring a shuttle plasmid, plasmid DNA transfer from S. gordonii to S. mutans was observed in a CSP and mutacin IV-dependent manner. Further analysis demonstrated an increased DNA release from S. gordonii upon addition of the partially purified mutacin IV extract. On the basis of these findings, we propose that Streptococcus mutans, which resides in a multispecies oral biofilm, may utilize the competence-induced bacteriocin production to acquire transforming DNA from other species living in the same ecological niche. This hypothesis is also consistent with a well-known phenomenon that a large genomic diversity exists among different S. mutans strains. This diversity may have resulted from extensive horizontal gene transfer.

MeSH Terms
Bacterial Proteins/physiology Bacteriocins/biosynthesis,genetics DNA, Bacterial/genetics,metabolism Gene Expression Regulation, Bacterial Gene Transfer, Horizontal Genes, Reporter Green Fluorescent Proteins Plasmids Streptococcus mutans/genetics,metabolism Transformation, Bacterial/physiology
Chemicals
Bacterial Proteins Bacteriocins DNA, Bacterial competence factor, Streptococcus Green Fluorescent Proteins
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Kreth Jens
Department of Oral Biology and Medicine, UCLA School of Dentistry, P.O. Box 951668, Los Angeles, CA 90095-1668, USA.
Merritt Justin
Shi Wenyuan
Qi Fengxia
References (49)
49 references, click to expand
  1. Enhanced transformation of Streptococcus mutans by modifications in culture conditions.
    Anal Biochem. 1993 Oct;214(1):343-6 PMID: 8250246
  2. Identification of comS, a gene of the srfA operon that regulates the establishment of genetic competence in Bacillus subtilis.
    Proc Natl Acad Sci U S A. 1994 Sep 27;91(20):9397-401 PMID: 7937777
  3. Nucleotide sequence of the 18-kb conjugative transposon Tn916 from Enterococcus faecalis.
    Plasmid. 1994 Nov;32(3):350-4 PMID: 7899523
  4. A small gene, designated comS, located within the coding region of the fourth amino acid-activation domain of srfA, is required for competence development in Bacillus subtilis.
    Mol Microbiol. 1995 Jan;15(1):55-63 PMID: 7752896
  5. FACS-optimized mutants of the green fluorescent protein (GFP).
    Gene. 1996;173(1 Spec No):33-8 PMID: 8707053
  6. Regulation of competence for genetic transformation in Streptococcus pneumoniae by an auto-induced peptide pheromone and a two-component regulatory system.
    Mol Microbiol. 1996 Aug;21(4):853-62 PMID: 8878046
  7. Novel series of plasmid vectors for gene inactivation and expression analysis in group A streptococci (GAS).
    Gene. 1996 Oct 24;177(1-2):137-47 PMID: 8921859
  8. Streptococcal competence for genetic transformation: regulation by peptide pheromones.
    Microb Drug Resist. 1997 Spring;3(1):27-37 PMID: 9109094
  9. Instruments of microbial warfare: bacteriocin synthesis, toxicity and immunity.
    Trends Microbiol. 1998 Feb;6(2):66-71 PMID: 9507641
  10. The bacteria of periodontal diseases.
    Periodontol 2000. 1994 Jun;5:66-77 PMID: 9673163
  11. Generation of bioluminescent Streptococcus mutans and its usage in rapid analysis of the efficacy of antimicrobial compounds.
    Antimicrob Agents Chemother. 1998 Aug;42(8):1906-10 PMID: 9687382
  12. Rapid and quantitative detection of Streptococcus mutans with species-specific monoclonal antibodies.
    Hybridoma. 1998 Aug;17(4):365-71 PMID: 9790071
  13. 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
  14. A unique nine-gene comY operon in Streptococcus mutans.
    Microbiology. 2005 Jan;151(Pt 1):157-66 PMID: 15632435
  15. Genetic analysis of a unique bacteriocin, Smb, produced by Streptococcus mutans GS5.
    Antimicrob Agents Chemother. 2005 Feb;49(2):541-8 PMID: 15673730
  16. Bacterial diversity within the human subgingival crevice.
    Proc Natl Acad Sci U S A. 1999 Dec 7;96(25):14547-52 PMID: 10588742
  17. Purification and biochemical characterization of mutacin I from the group I strain of Streptococcus mutans, CH43, and genetic analysis of mutacin I biosynthesis genes.
    Appl Environ Microbiol. 2000 Aug;66(8):3221-9 PMID: 10919773
  18. Microarray-based identification of a novel Streptococcus pneumoniae regulon controlled by an autoinduced peptide.
    J Bacteriol. 2000 Sep;182(17):4696-703 PMID: 10940007
  19. Global analysis of transcription kinetics during competence development in Streptococcus pneumoniae using high density DNA arrays.
    Mol Microbiol. 2000 Jun;36(6):1279-92 PMID: 10931279
  20. Regulation of competence for genetic transformation in Streptococcus pneumoniae: a link between quorum sensing and DNA processing genes.
    Res Microbiol. 2000 Jul-Aug;151(6):445-51 PMID: 10961457
  21. Allelic variation in a peptide-inducible two-component system of Streptococcus pneumoniae.
    FEMS Microbiol Lett. 2000 Sep 15;190(2):231-6 PMID: 11034284
  22. The group I strain of Streptococcus mutans, UA140, produces both the lantibiotic mutacin I and a nonlantibiotic bacteriocin, mutacin IV.
    Appl Environ Microbiol. 2001 Jan;67(1):15-21 PMID: 11133423
  23. Natural genetic transformation of Streptococcus mutans growing in biofilms.
    J Bacteriol. 2001 Feb;183(3):897-908 PMID: 11208787
  24. Assessment of GFP fluorescence in cells of Streptococcus gordonii under conditions of low pH and low oxygen concentration.
    Microbiology. 2001 May;147(Pt 5):1383-91 PMID: 11320140
  25. Bacterial diversity in human subgingival plaque.
    J Bacteriol. 2001 Jun;183(12):3770-83 PMID: 11371542
  26. A quorum-sensing signaling system essential for genetic competence in Streptococcus mutans is involved in biofilm formation.
    J Bacteriol. 2002 May;184(10):2699-708 PMID: 11976299
  27. Induction of natural competence in Streptococcus pneumoniae triggers lysis and DNA release from a subfraction of the cell population.
    Proc Natl Acad Sci U S A. 2002 May 28;99(11):7681-6 PMID: 12032343
  28. Involvement of Lsp, a member of the LraI-lipoprotein family in Streptococcus pyogenes, in eukaryotic cell adhesion and internalization.
    Infect Immun. 2002 Sep;70(9):4859-69 PMID: 12183530
  29. Multiple Streptococcus mutans Genes Are Involved in Biofilm Formation.
    Appl Environ Microbiol. 2002 Dec;68(12):6283-91 PMID: 12450853
  30. Transient association of an alternative sigma factor, ComX, with RNA polymerase during the period of competence for genetic transformation in Streptococcus pneumoniae.
    J Bacteriol. 2003 Jan;185(1):349-58 PMID: 12486073
  31. Controlling competence in Bacillus subtilis: shared use of regulators.
    Microbiology. 2003 Jan;149(Pt 1):9-17 PMID: 12576575
  32. Mutation of luxS affects biofilm formation in Streptococcus mutans.
    Infect Immun. 2003 Apr;71(4):1972-9 PMID: 12654815
  33. Competence-induced cells of Streptococcus pneumoniae lyse competence-deficient cells of the same strain during cocultivation.
    J Bacteriol. 2003 Dec;185(24):7176-83 PMID: 14645278
  34. Identification of competence pheromone responsive genes in Streptococcus pneumoniae by use of DNA microarrays.
    Mol Microbiol. 2004 Feb;51(4):1051-70 PMID: 14763980
  35. Interconnection of competence, stress and CiaR regulons in Streptococcus pneumoniae: competence triggers stationary phase autolysis of ciaR mutant cells.
    Mol Microbiol. 2004 Feb;51(4):1071-86 PMID: 14763981
  36. LuxS-mediated signaling in Streptococcus mutans is involved in regulation of acid and oxidative stress tolerance and biofilm formation.
    J Bacteriol. 2004 May;186(9):2682-91 PMID: 15090509
  37. Two separate quorum-sensing systems upregulate transcription of the same ABC transporter in Streptococcus pneumoniae.
    J Bacteriol. 2004 May;186(10):3078-85 PMID: 15126469
  38. Transcriptional analysis of mutacin I (mutA) gene expression in planktonic and biofilm cells of Streptococcus mutans using fluorescent protein and glucuronidase reporters.
    Oral Microbiol Immunol. 2004 Aug;19(4):252-6 PMID: 15209996
  39. Inactivation of the ciaH Gene in Streptococcus mutans diminishes mutacin production and competence development, alters sucrose-dependent biofilm formation, and reduces stress tolerance.
    Infect Immun. 2004 Aug;72(8):4895-9 PMID: 15271957
  40. ComX activity of Streptococcus mutans growing in biofilms.
    FEMS Microbiol Lett. 2004 Sep 1;238(1):167-74 PMID: 15336418
  41. Production and properties of bacteriocins (mutacins) from Streptococcus mutans.
    Arch Oral Biol. 1975 Oct;20(10):641-8 PMID: 1059386
  42. A cloning vector able to replicate in Escherichia coli and Streptococcus sanguis.
    Gene. 1982 Oct;19(3):345-53 PMID: 6295886
  43. Nucleotide sequence of the Streptococcus faecalis plasmid gene encoding the 3'5"-aminoglycoside phosphotransferase type III.
    Gene. 1983 Sep;23(3):331-41 PMID: 6313476
  44. Distinct bacteriocin groups correlate with different groups of Streptococcus mutans plasmids.
    Infect Immun. 1985 Apr;48(1):51-6 PMID: 2984124
  45. Epidemiological application of a new bacteriocin typing scheme for Streptococcus mutans.
    Community Dent Oral Epidemiol. 1990 Aug;18(4):194-6 PMID: 2387134
  46. Insertional inactivation of the gene encoding a 76-kilodalton cell surface polypeptide in Streptococcus gordonii Challis has a pleiotropic effect on cell surface composition and properties.
    Infect Immun. 1990 Nov;58(11):3689-97 PMID: 2228239
  47. The regulation of genetic competence in Bacillus subtilis.
    Mol Microbiol. 1991 Jan;5(1):11-8 PMID: 1901615
  48. Streptococcus mutans: classification in bacteriocin-types.
    Microbiologica. 1991 Jul;14(3):223-8 PMID: 1921743
  49. Genetic competence in Bacillus subtilis.
    Microbiol Rev. 1991 Sep;55(3):395-424 PMID: 1943994
Article Info
Journal
Molecular microbiology
Abbr.
Mol Microbiol
ISSN
0950-382X
Published
2005-07-00
Pages
392-404
Language
English
Region
England
NLM ID
8712028
PMCID
PMC1262684
Subset
IM
Grants
NIDCR NIH HHS · U01 DE015018 · United States
NIDCR NIH HHS · R01 DE014757 · United States
NIDCR NIH HHS · U01-DE15018 · United States
NIDCR NIH HHS · T32 DE007296 · United States
NIDCR NIH HHS · R01-DE014757 · 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