Home LiteratureArticle Details
PMID: 12654815 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Mutation of luxS affects biofilm formation in Streptococcus mutans.

Infection and immunity ·Vol. 71 ·No. 4 ·2003-04-00 ·Pages 1972-9

Merritt J, Qi F, Goodman SD, Anderson MH, Shi W

Abstract

Quorum sensing is a bacterial mechanism for regulating gene expression in response to changes in population density. Many bacteria are capable of acyl-homoserine lactone-based or peptide-based intraspecies quorum sensing and luxS-dependent interspecies quorum sensing. While there is good evidence about the involvement of intraspecies quorum sensing in bacterial biofilm, little is known about the role of luxS in biofilm formation. In this study, we report for the first time that luxS-dependent quorum sensing is involved in biofilm formation of Streptococcus mutans. S. mutans is a major cariogenic bacterium in the multispecies bacterial biofilm commonly known as dental plaque. An ortholog of luxS for S. mutans was identified using the data available in the S. mutans genome project (http://www.genome.ou.edu/smutans.html). Using an assay developed for the detection of the LuxS-associated quorum sensing signal autoinducer 2 (AI-2), it was demonstrated that this ortholog was able to complement the luxS negative phenotype of Escherichia coli DH5alpha. It was also shown that AI-2 is indeed produced by S. mutans. AI-2 production is maximal during mid- to late-log growth in batch culture. Mutant strains devoid of the luxS gene were constructed and found to be defective in producing the AI-2 signal. There are also marked phenotypic differences between the wild type and the luxS mutants. Microscopic analysis of in vitro-grown biofilm structure revealed that the luxS mutant biofilms adopted a much more granular appearance, rather than the relatively smooth, confluent layer normally seen in the wild type. These results suggest that LuxS-dependent signal may play an important role in biofilm formation of S. mutans.

MeSH Terms
Amino Acid Sequence Bacterial Proteins/genetics,metabolism Biofilms/growth & development Carbon-Sulfur Lyases Culture Media Escherichia coli/genetics,metabolism Gene Expression Regulation, Bacterial Genetic Complementation Test Homoserine/analogs & derivatives,metabolism Humans Lactones/metabolism Molecular Sequence Data Mutation Sequence Alignment Signal Transduction Streptococcus mutans/genetics,growth & development
Chemicals
Bacterial Proteins Culture Media Lactones N-octanoylhomoserine lactone Homoserine Carbon-Sulfur Lyases LuxS protein, Bacteria
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Merritt Justin
UCLA Molecular Biology Institute and School of Dentistry, 10833 Le Conte Avenue, Los Angeles, CA 90095-1668, USA.
Qi Fengxia
Goodman Steven D
Anderson Maxwell H
Shi Wenyuan
References (41)
41 references, click to expand
  1. Mutation of luxS affects growth and virulence factor expression in Streptococcus pyogenes.
    Mol Microbiol. 2001 Oct;42(1):145-57 PMID: 11679074
  2. Genetics of acid adaptation in oral streptococci.
    Crit Rev Oral Biol Med. 2001;12(4):301-14 PMID: 11603503
  3. Intra- and interspecies regulation of gene expression by Actinobacillus actinomycetemcomitans LuxS.
    Infect Immun. 2001 Dec;69(12):7625-34 PMID: 11705942
  4. Structural identification of a bacterial quorum-sensing signal containing boron.
    Nature. 2002 Jan 31;415(6871):545-9 PMID: 11823863
  5. Functional genomics approach to identifying genes required for biofilm development by Streptococcus mutans.
    Appl Environ Microbiol. 2002 Mar;68(3):1196-203 PMID: 11872468
  6. Biology, immunology, and cariogenicity of Streptococcus mutans.
    Microbiol Rev. 1980 Jun;44(2):331-84 PMID: 6446023
  7. Studies on transformation of Escherichia coli with plasmids.
    J Mol Biol. 1983 Jun 5;166(4):557-80 PMID: 6345791
  8. Coaggregations among oral bacteria.
    Methods Enzymol. 1995;253:385-97 PMID: 7476402
  9. Intergeneric coaggregation of oral Treponema spp. with Fusobacterium spp. and intrageneric coaggregation among Fusobacterium spp.
    Infect Immun. 1995 Dec;63(12):4584-8 PMID: 7591109
  10. Microbial biofilms.
    Annu Rev Microbiol. 1995;49:711-45 PMID: 8561477
  11. Cell-cell communication in gram-positive bacteria.
    Annu Rev Microbiol. 1997;51:527-64 PMID: 9343359
  12. The involvement of cell-to-cell signals in the development of a bacterial biofilm.
    Science. 1998 Apr 10;280(5361):295-8 PMID: 9535661
  13. Quorum sensing in Escherichia coli and Salmonella typhimurium.
    Proc Natl Acad Sci U S A. 1998 Jun 9;95(12):7046-50 PMID: 9618536
  14. Rapid and quantitative detection of Streptococcus mutans with species-specific monoclonal antibodies.
    Hybridoma. 1998 Aug;17(4):365-71 PMID: 9790071
  15. 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
  16. Biofilms, infectious agents, and dental unit waterlines: a review.
    Can J Microbiol. 1998 Nov;44(11):1019-28 PMID: 10029997
  17. The specific genes for lantibiotic mutacin II biosynthesis in Streptococcus mutans T8 are clustered and can be transferred en bloc.
    Appl Environ Microbiol. 1999 Mar;65(3):1356-60 PMID: 10049909
  18. Self perception in bacteria: quorum sensing with acylated homoserine lactones.
    Curr Opin Microbiol. 1998 Apr;1(2):183-9 PMID: 10066485
  19. Biofilms.
    Curr Opin Microbiol. 1999 Jun;2(3):270-5 PMID: 10383861
  20. Inactivation of the gbpA gene of Streptococcus mutans alters structural and functional aspects of plaque biofilm which are compensated by recombination of the gtfB and gtfC genes.
    Infect Immun. 1999 Aug;67(8):3909-14 PMID: 10417155
  21. Purification of mutacin III from group III Streptococcus mutans UA787 and genetic analyses of mutacin III biosynthesis genes.
    Appl Environ Microbiol. 1999 Sep;65(9):3880-7 PMID: 10473390
  22. How bacteria talk to each other: regulation of gene expression by quorum sensing.
    Curr Opin Microbiol. 1999 Dec;2(6):582-7 PMID: 10607620
  23. Genetic analyses of bacterial biofilm formation.
    Curr Opin Microbiol. 1999 Dec;2(6):598-603 PMID: 10607630
  24. Quorum sensing controls expression of the type III secretion gene transcription and protein secretion in enterohemorrhagic and enteropathogenic Escherichia coli.
    Proc Natl Acad Sci U S A. 1999 Dec 21;96(26):15196-201 PMID: 10611361
  25. Streptococcus gordonii biofilm formation: identification of genes that code for biofilm phenotypes.
    J Bacteriol. 2000 Mar;182(5):1374-82 PMID: 10671461
  26. Intercellular communication in Helicobacter pylori: luxS is essential for the production of an extracellular signaling molecule.
    Infect Immun. 2000 Jun;68(6):3193-9 PMID: 10816463
  27. Evidence for a signaling system in Helicobacter pylori: detection of a luxS-encoded autoinducer.
    J Bacteriol. 2000 Jul;182(13):3638-43 PMID: 10850976
  28. 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
  29. Oral microbial communities: biofilms, interactions, and genetic systems.
    Annu Rev Microbiol. 2000;54:413-37 PMID: 11018133
  30. Impact of the agr quorum-sensing system on adherence to polystyrene in Staphylococcus aureus.
    J Infect Dis. 2000 Dec;182(6):1688-93 PMID: 11069241
  31. Microbial biofilms: from ecology to molecular genetics.
    Microbiol Mol Biol Rev. 2000 Dec;64(4):847-67 PMID: 11104821
  32. Shigella flexneri LuxS quorum-sensing system modulates virB expression but is not essential for virulence.
    Infect Immun. 2001 Jan;69(1):15-23 PMID: 11119484
  33. 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
  34. Periodontal pathogens produce quorum sensing signal molecules.
    Infect Immun. 2001 May;69(5):3431-4 PMID: 11292769
  35. Signaling system in Porphyromonas gingivalis based on a LuxS protein.
    J Bacteriol. 2001 Jul;183(13):3903-9 PMID: 11395453
  36. The LuxS family of bacterial autoinducers: biosynthesis of a novel quorum-sensing signal molecule.
    Mol Microbiol. 2001 Jul;41(2):463-76 PMID: 11489131
  37. The cep quorum-sensing system of Burkholderia cepacia H111 controls biofilm formation and swarming motility.
    Microbiology. 2001 Sep;147(Pt 9):2517-28 PMID: 11535791
  38. Crystal structure of the quorum-sensing protein LuxS reveals a catalytic metal site.
    Proc Natl Acad Sci U S A. 2001 Sep 25;98(20):11169-74 PMID: 11553770
  39. Cloning of the Streptococcus mutans gene encoding glucan binding protein B and analysis of genetic diversity and protein production in clinical isolates.
    Infect Immun. 2001 Nov;69(11):6931-41 PMID: 11598068
  40. The 1.2 A structure of a novel quorum-sensing protein, Bacillus subtilis LuxS.
    J Mol Biol. 2001 Oct 12;313(1):111-22 PMID: 11601850
  41. The microbiology of primary dental caries in humans.
    J Dent Educ. 2001 Oct;65(10):1028-37 PMID: 11699974
Article Info
Journal
Infection and immunity
Abbr.
Infect Immun
ISSN
0019-9567
Published
2003-04-00
Pages
1972-9
Language
English
Region
United States
NLM ID
0246127
PMCID
PMC152054
Subset
IM
Grants
NIDCR NIH HHS · R01 DE013965 · United States
NIAID NIH HHS · T32 AI007323 · United States
NIDCR NIH HHS · DE 013965 · United States
NIAID NIH HHS · T32 AI 07323 · 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