Home LiteratureArticle Details
PMID: 16369005 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Role of the luxS quorum-sensing system in biofilm formation and virulence of Staphylococcus epidermidis.

Infection and immunity ·Vol. 74 ·No. 1 ·2006-01-00 ·Pages 488-96

Xu L, Li H, Vuong C, Vadyvaloo V, Wang J, Yao Y, Otto M, Gao Q

Abstract

Nosocomial infections caused by Staphylococcus epidermidis are characterized by biofilm formation on implanted medical devices. Quorum-sensing regulation plays a major role in the biofilm development of many bacterial pathogens. Here, we describe luxS, a quorum-sensing system in staphylococci that has a significant impact on biofilm development and virulence. We constructed an isogenic DeltaluxS mutant strain of a biofilm-forming clinical isolate of S. epidermidis and demonstrated that luxS signaling is functional in S. epidermidis. The mutant strain showed increased biofilm formation in vitro and enhanced virulence in a rat model of biofilm-associated infection. Genetic complementation and addition of autoinducer 2-containing culture filtrate restored the wild-type phenotype, demonstrating that luxS repressed biofilm formation through a cell-cell signaling mechanism based on autoinducer 2 secretion. Enhanced production of the biofilm exopolysaccharide polysaccharide intercellular adhesin in the mutant strain is presumably the major cause of the observed phenotype. The agr quorum-sensing system has previously been shown to impact biofilm development and biofilm-associated infection in a way similar to that of luxS, although by regulation of different factors. Our study indicates a general scheme of quorum-sensing regulation of biofilm development in staphylococci, which contrasts with that observed in many other bacterial pathogens.

MeSH Terms
Animals Bacterial Proteins/genetics,physiology Biofilms/growth & development Carbon-Sulfur Lyases Cross Infection/metabolism Disease Models, Animal Homoserine/analogs & derivatives,metabolism Humans Lactones/metabolism Male Microscopy, Electron, Scanning Mutation Rats Rats, Sprague-Dawley Staphylococcal Infections/metabolism,microbiology Staphylococcus epidermidis/genetics,pathogenicity,physiology,ultrastructure Virulence
Chemicals
Bacterial Proteins Lactones N-octanoylhomoserine lactone Homoserine Carbon-Sulfur Lyases LuxS protein, Bacteria
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Xu Lin
Key Laboratory of Medical Molecular Virology, Shanghai Medical College, Fudan University, Shanghai 200032, People's Republic of China.
Li Hualin
Vuong Cuong
Vadyvaloo Viveka
Wang Jianping
Yao Yufeng
Otto Michael
Gao Qian
References (58)
58 references, click to expand
  1. Identification of three essential regulatory gene loci governing expression of Staphylococcus epidermidis polysaccharide intercellular adhesin and biofilm formation.
    Infect Immun. 2000 Jul;68(7):3799-807 PMID: 10858187
  2. Association of biofilm production of coagulase-negative staphylococci with expression of a specific polysaccharide intercellular adhesin.
    J Infect Dis. 1996 Oct;174(4):881-4 PMID: 8843236
  3. Functional study of antibodies against a fibrogenin-binding protein in Staphylococcus epidermidis adherence to polyethylene catheters.
    J Infect Dis. 2001 Jul 1;184(1):52-5 PMID: 11398109
  4. Quorum sensing is a global regulatory mechanism in enterohemorrhagic Escherichia coli O157:H7.
    J Bacteriol. 2001 Sep;183(17):5187-97 PMID: 11489873
  5. Evidence for autolysin-mediated primary attachment of Staphylococcus epidermidis to a polystyrene surface.
    Mol Microbiol. 1997 Jun;24(5):1013-24 PMID: 9220008
  6. Structure of the pheromone peptide of the Staphylococcus epidermidis agr system.
    FEBS Lett. 1998 Mar 6;424(1-2):89-94 PMID: 9537521
  7. Quorum sensing in Escherichia coli and Salmonella typhimurium.
    Proc Natl Acad Sci U S A. 1998 Jun 9;95(12):7046-50 PMID: 9618536
  8. Characterization of the N-acetylglucosaminyltransferase activity involved in the biosynthesis of the Staphylococcus epidermidis polysaccharide intercellular adhesin.
    J Biol Chem. 1998 Jul 17;273(29):18586-93 PMID: 9660830
  9. 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
  10. Characterization of Staphylococcus epidermidis polysaccharide intercellular adhesin/hemagglutinin in the pathogenesis of intravascular catheter-associated infection in a rat model.
    Infect Immun. 1999 May;67(5):2656-9 PMID: 10225938
  11. Genomewide analysis of gene expression in Staphylococcus epidermidis biofilms: insights into the pathophysiology of S. epidermidis biofilms and the role of phenol-soluble modulins in formation of biofilms.
    J Infect Dis. 2005 Jan 15;191(2):289-98 PMID: 15609240
  12. Transformation of Staphylococcus epidermidis and other staphylococcal species with plasmid DNA by electroporation.
    FEMS Microbiol Lett. 1990 Jan 1;54(1-3):203-7 PMID: 2182373
  13. Quorum sensing in bacteria.
    Annu Rev Microbiol. 2001;55:165-99 PMID: 11544353
  14. Mutation of luxS affects growth and virulence factor expression in Streptococcus pyogenes.
    Mol Microbiol. 2001 Oct;42(1):145-57 PMID: 11679074
  15. Intra- and interspecies regulation of gene expression by Actinobacillus actinomycetemcomitans LuxS.
    Infect Immun. 2001 Dec;69(12):7625-34 PMID: 11705942
  16. Characterization of comQ and comX, two genes required for production of ComX pheromone in Bacillus subtilis.
    J Bacteriol. 2002 Jan;184(2):410-9 PMID: 11751817
  17. Mob psychology.
    J Bacteriol. 2002 Feb;184(4):873-83 PMID: 11807045
  18. Structural identification of a bacterial quorum-sensing signal containing boron.
    Nature. 2002 Jan 31;415(6871):545-9 PMID: 11823863
  19. Role of Neisseria meningitidis luxS in cell-to-cell signaling and bacteremic infection.
    Infect Immun. 2002 Apr;70(4):2245-8 PMID: 11895997
  20. Staphylococcus epidermidis infections.
    Microbes Infect. 2002 Apr;4(4):481-9 PMID: 11932199
  21. LuxS: its role in central metabolism and the in vitro synthesis of 4-hydroxy-5-methyl-3(2H)-furanone.
    Microbiology. 2002 Apr;148(Pt 4):909-22 PMID: 11932438
  22. Biofilm formation and interaction with the surfaces of gallstones by Salmonella spp.
    Infect Immun. 2002 May;70(5):2640-9 PMID: 11953406
  23. Staphylococcus and biofilms.
    Mol Microbiol. 2002 Mar;43(6):1367-78 PMID: 11952892
  24. The luxS gene is involved in cell-cell signalling for toxin production in Clostridium perfringens.
    Mol Microbiol. 2002 Apr;44(1):171-9 PMID: 11967077
  25. LuxS-based signaling in Streptococcus gordonii: autoinducer 2 controls carbohydrate metabolism and biofilm formation with Porphyromonas gingivalis.
    J Bacteriol. 2003 Jan;185(1):274-84 PMID: 12486064
  26. luxS and arcB control aerobic growth of Actinobacillus actinomycetemcomitans under iron limitation.
    Infect Immun. 2003 Jan;71(1):298-308 PMID: 12496179
  27. Mutation of luxS affects biofilm formation in Streptococcus mutans.
    Infect Immun. 2003 Apr;71(4):1972-9 PMID: 12654815
  28. Glucose-related dissociation between icaADBC transcription and biofilm expression by Staphylococcus epidermidis: evidence for an additional factor required for polysaccharide intercellular adhesin synthesis.
    J Bacteriol. 2003 May;185(9):2879-86 PMID: 12700267
  29. LuxS quorum sensing: more than just a numbers game.
    Curr Opin Microbiol. 2003 Apr;6(2):191-7 PMID: 12732311
  30. Mutation of luxS of Streptococcus pneumoniae affects virulence in a mouse model.
    Infect Immun. 2003 Jun;71(6):3206-12 PMID: 12761100
  31. Autoinduction and signal transduction in the regulation of staphylococcal virulence.
    Mol Microbiol. 2003 Jun;48(6):1429-49 PMID: 12791129
  32. Regulation of Vibrio vulnificus virulence by the LuxS quorum-sensing system.
    Mol Microbiol. 2003 Jun;48(6):1647-64 PMID: 12791145
  33. Detection of a luxS-signaling molecule in Bacillus anthracis.
    Infect Immun. 2003 Jul;71(7):3914-9 PMID: 12819077
  34. Quorum-sensing control of biofilm factors in Staphylococcus epidermidis.
    J Infect Dis. 2003 Sep 1;188(5):706-18 PMID: 12934187
  35. Genome-based analysis of virulence genes in a non-biofilm-forming Staphylococcus epidermidis strain (ATCC 12228).
    Mol Microbiol. 2003 Sep;49(6):1577-93 PMID: 12950922
  36. Modulation of Pseudomonas aeruginosa gene expression by host microflora through interspecies communication.
    Mol Microbiol. 2003 Dec;50(5):1477-91 PMID: 14651632
  37. The bacterial insertion sequence element IS256 occurs preferentially in nosocomial Staphylococcus epidermidis isolates: association with biofilm formation and resistance to aminoglycosides.
    Infect Immun. 2004 Feb;72(2):1210-5 PMID: 14742578
  38. LuxS is required for persistent pneumococcal carriage and expression of virulence and biosynthesis genes.
    Infect Immun. 2004 May;72(5):2964-75 PMID: 15102809
  39. Characterization of monospecies biofilm formation by Helicobacter pylori.
    J Bacteriol. 2004 May;186(10):3124-32 PMID: 15126474
  40. Vibrio fischeri LuxS and AinS: comparative study of two signal synthases.
    J Bacteriol. 2004 Jun;186(12):3873-81 PMID: 15175301
  41. luxS mutants of Serratia defective in autoinducer-2-dependent 'quorum sensing' show strain-dependent impacts on virulence and production of carbapenem and prodigiosin.
    Microbiology. 2004 Jun;150(Pt 6):1901-10 PMID: 15184576
  42. The luxS gene is not required for Borrelia burgdorferi tick colonization, transmission to a mammalian host, or induction of disease.
    Infect Immun. 2004 Aug;72(8):4864-7 PMID: 15271949
  43. Growth phase regulation of flaA expression in Helicobacter pylori is luxS dependent.
    Infect Immun. 2004 Sep;72(9):5506-10 PMID: 15322055
  44. Synthesis of LuxS inhibitors targeting bacterial cell-cell communication.
    Org Lett. 2004 Sep 2;6(18):3043-6 PMID: 15330583
  45. Salmonella typhimurium recognizes a chemically distinct form of the bacterial quorum-sensing signal AI-2.
    Mol Cell. 2004 Sep 10;15(5):677-87 PMID: 15350213
  46. Increased colonization of indwelling medical devices by quorum-sensing mutants of Staphylococcus epidermidis in vivo.
    J Infect Dis. 2004 Oct 15;190(8):1498-505 PMID: 15378444
  47. Three parallel quorum-sensing systems regulate gene expression in Vibrio harveyi.
    J Bacteriol. 2004 Oct;186(20):6902-14 PMID: 15466044
  48. Studies on transformation of Escherichia coli with plasmids.
    J Mol Biol. 1983 Jun 5;166(4):557-80 PMID: 6345791
  49. Introduction of pAM beta 1 into Listeria monocytogenes by conjugation and homology between native L. monocytogenes plasmids.
    Infect Immun. 1984 Apr;44(1):157-61 PMID: 6323313
  50. Adherence of coagulase-negative staphylococci to plastic tissue culture plates: a quantitative model for the adherence of staphylococci to medical devices.
    J Clin Microbiol. 1985 Dec;22(6):996-1006 PMID: 3905855
  51. Parallel induction by glucose of adherence and a polysaccharide antigen specific for plastic-adherent Staphylococcus epidermidis: evidence for functional relation to intercellular adhesion.
    Infect Immun. 1992 May;60(5):2048-57 PMID: 1314224
  52. Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators.
    J Bacteriol. 1994 Jan;176(2):269-75 PMID: 8288518
  53. Cross-species induction of luminescence in the quorum-sensing bacterium Vibrio harveyi.
    J Bacteriol. 1997 Jun;179(12):4043-5 PMID: 9190823
  54. Gene replacement in Staphylococcus carnosus and Staphylococcus xylosus.
    FEMS Microbiol Lett. 1997 Jun 1;151(1):1-8 PMID: 9198277
  55. Multiple signalling systems controlling expression of luminescence in Vibrio harveyi: sequence and function of genes encoding a second sensory pathway.
    Mol Microbiol. 1994 Jul;13(2):273-86 PMID: 7984107
  56. The intercellular adhesin involved in biofilm accumulation of Staphylococcus epidermidis is a linear beta-1,6-linked glucosaminoglycan: purification and structural analysis.
    J Bacteriol. 1996 Jan;178(1):175-83 PMID: 8550413
  57. Molecular basis of intercellular adhesion in the biofilm-forming Staphylococcus epidermidis.
    Mol Microbiol. 1996 Jun;20(5):1083-91 PMID: 8809760
  58. 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
Article Info
Journal
Infection and immunity
Abbr.
Infect Immun
ISSN
0019-9567
DOI
10.1128/IAI.74.1.488-496.2006
Published
2006-01-00
Pages
488-96
Language
English
Region
United States
NLM ID
0246127
PMCID
PMC1346618
Subset
IM
External Links
PubMed source DOI: 10.1128/IAI.74.1.488-496.2006 PMC Full Text View journal details
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

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2