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PMID: 17452642 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

The cidA murein hydrolase regulator contributes to DNA release and biofilm development in Staphylococcus aureus.

Proceedings of the National Academy of Sciences of the United States of America ·Vol. 104 ·No. 19 ·2007-05-08 ·Pages 8113-8

Rice KC, Mann EE, Endres JL, Weiss EC, Cassat JE, Smeltzer MS, Bayles KW

Abstract

The Staphylococcus aureus cidA and lrgA genes have been shown to affect cell lysis under a variety of conditions during planktonic growth. It is hypothesized that these genes encode holins and antiholins, respectively, and may serve as molecular control elements of bacterial cell lysis. To examine the biological role of cell death and lysis, we studied the impact of the cidA mutation on biofilm development. Interestingly, this mutation had a dramatic impact on biofilm morphology and adherence. The cidA mutant (KB1050) biofilm exhibited a rougher appearance compared with the parental strain (UAMS-1) and was less adherent. Propidium iodide staining revealed that KB1050 accumulated more dead cells within the biofilm population relative to UAMS-1, indicative of reduced cell lysis. In agreement with this finding, quantitative real-time PCR experiments demonstrated the presence of 5-fold less genomic DNA in the KB1050 biofilm relative to UAMS-1. Furthermore, treatment of the UAMS-1 biofilm with DNase I caused extensive cell detachment, whereas similar treatment of the KB1050 biofilm had only a modest effect. These results demonstrate that cidA-controlled cell lysis plays a significant role during biofilm development and that released genomic DNA is an important structural component of S. aureus biofilm.

MeSH Terms
Bacterial Adhesion Biofilms DNA, Bacterial/metabolism N-Acetylmuramoyl-L-alanine Amidase/metabolism Operon/physiology Staphylococcus aureus/genetics,physiology
Chemicals
DNA, Bacterial N-Acetylmuramoyl-L-alanine Amidase
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Rice Kelly C
Department of Pathology and Microbiology, University of Nebraska Medical Center, Omaha, NE 68198, USA.
Mann Ethan E
Endres Jennifer L
Weiss Elizabeth C
Cassat James E
Smeltzer Mark S
Bayles Kenneth W
References (71)
71 references, click to expand
  1. The teicoplanin-associated locus regulator (TcaR) and the intercellular adhesin locus regulator (IcaR) are transcriptional inhibitors of the ica locus in Staphylococcus aureus.
    J Bacteriol. 2004 Apr;186(8):2449-56 PMID: 15060048
  2. Gene expression in Bacillus subtilis surface biofilms with and without sporulation and the importance of yveR for biofilm maintenance.
    Biotechnol Bioeng. 2004 May 5;86(3):344-64 PMID: 15083514
  3. Transcription of the Staphylococcus aureus cid and lrg murein hydrolase regulators is affected by sigma factor B.
    J Bacteriol. 2004 May;186(10):3029-37 PMID: 15126464
  4. Biofilm development and cell death in the marine bacterium Pseudoalteromonas tunicata.
    Appl Environ Microbiol. 2004 Jun;70(6):3232-8 PMID: 15184116
  5. Global gene expression in Staphylococcus aureus biofilms.
    J Bacteriol. 2004 Jul;186(14):4665-84 PMID: 15231800
  6. DNA-containing membrane vesicles of Pseudomonas aeruginosa PAO1 and their genetic transformation potential.
    Microbiology. 2004 Jul;150(Pt 7):2161-9 PMID: 15256559
  7. Biofilm mode of growth of Streptococcus intermedius favored by a competence-stimulating signaling peptide.
    J Bacteriol. 2004 Sep;186(18):6327-31 PMID: 15342606
  8. Identification and molecular characterization of a putative regulatory locus that affects autolysis in Staphylococcus aureus.
    J Bacteriol. 1996 Feb;178(3):611-8 PMID: 8550490
  9. A characterization of DNA release in Pseudomonas aeruginosa cultures and biofilms.
    Mol Microbiol. 2006 Feb;59(4):1114-28 PMID: 16430688
  10. Inhibition of competence development in Streptococcus pneumoniae by increased basal-level expression of the ComDE two-component regulatory system.
    Microbiology. 2006 Feb;152(Pt 2):323-31 PMID: 16436420
  11. The role of proton motive force in expression of the Staphylococcus aureus cid and lrg operons.
    Mol Microbiol. 2006 Mar;59(5):1395-404 PMID: 16468984
  12. Characterization of the Staphylococcus aureus CidR regulon: elucidation of a novel role for acetoin metabolism in cell death and lysis.
    Mol Microbiol. 2006 Apr;60(2):458-68 PMID: 16573694
  13. Quorum sensing and DNA release in bacterial biofilms.
    Curr Opin Microbiol. 2006 Apr;9(2):133-7 PMID: 16529982
  14. Activity of the major staphylococcal autolysin Atl.
    FEMS Microbiol Lett. 2006 Jun;259(2):260-8 PMID: 16734789
  15. Ecological advantages of autolysis during the development and dispersal of Pseudoalteromonas tunicata biofilms.
    Appl Environ Microbiol. 2006 Aug;72(8):5414-20 PMID: 16885293
  16. Switch from planktonic to sessile life: a major event in pneumococcal pathogenesis.
    Mol Microbiol. 2006 Sep;61(5):1196-210 PMID: 16925554
  17. The atlA operon of Streptococcus mutans: role in autolysin maturation and cell surface biogenesis.
    J Bacteriol. 2006 Oct;188(19):6877-88 PMID: 16980491
  18. Transcriptional profiling of a Staphylococcus aureus clinical isolate and its isogenic agr and sarA mutants reveals global differences in comparison to the laboratory strain RN6390.
    Microbiology. 2006 Oct;152(Pt 10):3075-90 PMID: 17005987
  19. Biofilm formation by Streptococcus pneumoniae: role of choline, extracellular DNA, and capsular polysaccharide in microbial accretion.
    J Bacteriol. 2006 Nov;188(22):7785-95 PMID: 16936041
  20. Cell density- and ComE-dependent expression of a group of mutacin and mutacin-like genes in Streptococcus mutans.
    FEMS Microbiol Lett. 2006 Dec;265(1):11-7 PMID: 16981904
  21. The Staphylococcus aureus lrgAB operon modulates murein hydrolase activity and penicillin tolerance.
    J Bacteriol. 2000 Apr;182(7):1794-801 PMID: 10714982
  22. The bactericidal action of penicillin: new clues to an unsolved mystery.
    Trends Microbiol. 2000 Jun;8(6):274-8 PMID: 10838585
  23. A new two-component regulatory system involved in adhesion, autolysis, and extracellular proteolytic activity of Staphylococcus aureus.
    J Bacteriol. 2000 Jul;182(14):3955-64 PMID: 10869073
  24. Quantification of biofilm structures by the novel computer program COMSTAT.
    Microbiology. 2000 Oct;146 ( Pt 10):2395-407 PMID: 11021916
  25. 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
  26. Natural genetic transformation of Streptococcus mutans growing in biofilms.
    J Bacteriol. 2001 Feb;183(3):897-908 PMID: 11208787
  27. Staphylococcus aureus accessory regulators: expression within biofilms and effect on adhesion.
    Microbes Infect. 2001 Jul;3(8):633-7 PMID: 11445449
  28. Gene expression in Pseudomonas aeruginosa biofilms.
    Nature. 2001 Oct 25;413(6858):860-4 PMID: 11677611
  29. Evaluation of a tetracycline-inducible promoter in Staphylococcus aureus in vitro and in vivo and its application in demonstrating the role of sigB in microcolony formation.
    Infect Immun. 2001 Dec;69(12):7851-7 PMID: 11705967
  30. Extracellular DNA required for bacterial biofilm formation.
    Science. 2002 Feb 22;295(5559):1487 PMID: 11859186
  31. 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
  32. Multiple Streptococcus mutans Genes Are Involved in Biofilm Formation.
    Appl Environ Microbiol. 2002 Dec;68(12):6283-91 PMID: 12450853
  33. Identification of catabolite repression as a physiological regulator of biofilm formation by Bacillus subtilis by use of DNA microarrays.
    J Bacteriol. 2003 Mar;185(6):1951-7 PMID: 12618459
  34. A major autolysin of Pseudomonas aeruginosa: subcellular distribution, potential role in cell growth and division and secretion in surface membrane vesicles.
    J Bacteriol. 1996 May;178(9):2479-88 PMID: 8626312
  35. Bacteriolytic effect of membrane vesicles from Pseudomonas aeruginosa on other bacteria including pathogens: conceptually new antibiotics.
    J Bacteriol. 1996 May;178(10):2767-74 PMID: 8631663
  36. Identification of LytSR-regulated genes from Staphylococcus aureus.
    J Bacteriol. 1996 Oct;178(19):5810-2 PMID: 8824633
  37. Evidence for autolysin-mediated primary attachment of Staphylococcus epidermidis to a polystyrene surface.
    Mol Microbiol. 1997 Jun;24(5):1013-24 PMID: 9220008
  38. 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
  39. Bacteriophage and phenotypic variation in Pseudomonas aeruginosa biofilm development.
    J Bacteriol. 2004 Dec;186(23):8066-73 PMID: 15547279
  40. Comparison of assays for detection of agents causing membrane damage in Staphylococcus aureus.
    J Antimicrob Chemother. 2004 Dec;54(6):1127-9 PMID: 15531595
  41. Acetic acid induces expression of the Staphylococcus aureus cidABC and lrgAB murein hydrolase regulator operons.
    J Bacteriol. 2005 Feb;187(3):813-21 PMID: 15659658
  42. Differential gene expression profiling of Staphylococcus aureus cultivated under biofilm and planktonic conditions.
    Appl Environ Microbiol. 2005 May;71(5):2663-76 PMID: 15870358
  43. Identification and characterization of an autolysin-encoding gene of Streptococcus mutans.
    Infect Immun. 2005 Jun;73(6):3512-20 PMID: 15908380
  44. Release of DNA into the medium by competent Streptococcus pneumoniae: kinetics, mechanism and stability of the liberated DNA.
    Mol Microbiol. 2004 Nov;54(3):783-94 PMID: 15491367
  45. 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
  46. Inhibition of wall autolysis of staphylococci by sodium polyanethole sulfonate "liquoid".
    Arch Microbiol. 1986 Mar;144(2):110-5 PMID: 3013113
  47. Bacterial biofilms in nature and disease.
    Annu Rev Microbiol. 1987;41:435-64 PMID: 3318676
  48. Salt-induced cell lysis of Staphylococcus aureus.
    Curr Microbiol. 1995 May;30(5):299-303 PMID: 7766158
  49. Role of the accessory gene regulator (agr) in pathogenesis of staphylococcal osteomyelitis.
    Infect Immun. 1995 Sep;63(9):3373-80 PMID: 7642265
  50. Microbial biofilms.
    Annu Rev Microbiol. 1995;49:711-45 PMID: 8561477
  51. The Staphylococcus aureus cidC gene encodes a pyruvate oxidase that affects acetate metabolism and cell death in stationary phase.
    Mol Microbiol. 2005 Jun;56(6):1664-74 PMID: 15916614
  52. Regulation of bacteriocin production in Streptococcus mutans by the quorum-sensing system required for development of genetic competence.
    J Bacteriol. 2005 Jun;187(12):3980-9 PMID: 15937160
  53. Competence-programmed predation of noncompetent cells in the human pathogen Streptococcus pneumoniae: genetic requirements.
    Proc Natl Acad Sci U S A. 2005 Jun 14;102(24):8710-5 PMID: 15928084
  54. DNA binding-uptake system: a link between cell-to-cell communication and biofilm formation.
    J Bacteriol. 2005 Jul;187(13):4392-400 PMID: 15968048
  55. Co-ordinated bacteriocin production and competence development: a possible mechanism for taking up DNA from neighbouring species.
    Mol Microbiol. 2005 Jul;57(2):392-404 PMID: 15978073
  56. Staphylococcus aureus develops an alternative, ica-independent biofilm in the absence of the arlRS two-component system.
    J Bacteriol. 2005 Aug;187(15):5318-29 PMID: 16030226
  57. A LysR-type regulator, CidR, is required for induction of the Staphylococcus aureus cidABC operon.
    J Bacteriol. 2005 Sep;187(17):5893-900 PMID: 16109930
  58. Extracellular DNA in single- and multiple-species unsaturated biofilms.
    Appl Environ Microbiol. 2005 Sep;71(9):5404-10 PMID: 16151131
  59. Transcriptome analysis of Pseudomonas aeruginosa growth: comparison of gene expression in planktonic cultures and developing and mature biofilms.
    J Bacteriol. 2005 Sep;187(18):6571-6 PMID: 16159792
  60. Global gene expression in Escherichia coli biofilms.
    Mol Microbiol. 2003 Apr;48(1):253-67 PMID: 12657059
  61. The Staphylococcus aureus cidAB operon: evaluation of its role in regulation of murein hydrolase activity and penicillin tolerance.
    J Bacteriol. 2003 Apr;185(8):2635-43 PMID: 12670989
  62. SarA and not sigmaB is essential for biofilm development by Staphylococcus aureus.
    Mol Microbiol. 2003 May;48(4):1075-87 PMID: 12753197
  63. Effect of Varidase (streptodornase) on biofilm formed by Pseudomonas aeruginosa.
    Chemotherapy. 2003 Jun;49(3):121-5 PMID: 12815204
  64. Mutation of sarA in Staphylococcus aureus limits biofilm formation.
    Infect Immun. 2003 Jul;71(7):4206-11 PMID: 12819120
  65. Cell death in Pseudomonas aeruginosa biofilm development.
    J Bacteriol. 2003 Aug;185(15):4585-92 PMID: 12867469
  66. Are the molecular strategies that control apoptosis conserved in bacteria?
    Trends Microbiol. 2003 Jul;11(7):306-11 PMID: 12875813
  67. Pathophysiology and management of pulmonary infections in cystic fibrosis.
    Am J Respir Crit Care Med. 2003 Oct 15;168(8):918-51 PMID: 14555458
  68. Death's toolbox: examining the molecular components of bacterial programmed cell death.
    Mol Microbiol. 2003 Nov;50(3):729-38 PMID: 14617136
  69. 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
  70. Control of glucose- and NaCl-induced biofilm formation by rbf in Staphylococcus aureus.
    J Bacteriol. 2004 Feb;186(3):722-9 PMID: 14729698
  71. Quorum sensing in Staphylococcus aureus biofilms.
    J Bacteriol. 2004 Mar;186(6):1838-50 PMID: 14996815
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
DOI
10.1073/pnas.0610226104
Published
2007-05-08
Epub
2007-00-23
Pages
8113-8
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC1876580
Subset
IM
Grants
NCRR NIH HHS · RR17417-01 · United States
NIAID NIH HHS · R01AI038901 · United States
NIAID NIH HHS · R01 AI038901 · United States
NIAID NIH HHS · R01AI43356 · United States
NCRR NIH HHS · C06 RR017417 · United States
NIAID NIH HHS · R01 AI043356 · United States
External Links
PubMed source DOI: 10.1073/pnas.0610226104 PMC Full Text View journal details
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