全部 标题 作者
关键词 摘要

OALib Journal期刊
ISSN: 2333-9721
费用:99美元

查看量下载量

相关文章

更多...
PLOS ONE  2009 

Modulation of eDNA Release and Degradation Affects Staphylococcus aureus Biofilm Maturation

DOI: 10.1371/journal.pone.0005822

Full-Text   Cite this paper   Add to My Lib

Abstract:

Recent studies have demonstrated a role for Staphylococcus aureus cidA-mediated cell lysis and genomic DNA release in biofilm adherence. The current study extends these findings by examining both temporal and additional genetic factors involved in the control of genomic DNA release and degradation during biofilm maturation. Cell lysis and DNA release were found to be critical for biofilm attachment during the initial stages of development and the released DNA (eDNA) remained an important matrix component during biofilm maturation. This study also revealed that an lrgAB mutant exhibits increased biofilm adherence and matrix-associated eDNA consistent with its proposed role as an inhibitor of cidA-mediated lysis. In flow-cell assays, both cid and lrg mutations had dramatic effects on biofilm maturation and tower formation. Finally, staphylococcal thermonuclease was shown to be involved in biofilm development as a nuc mutant formed a thicker biofilm containing increased levels of matrix-associated eDNA. Together, these findings suggest a model in which the opposing activities of the cid and lrg gene products control cell lysis and genomic DNA release during biofilm development, while staphylococcal thermonuclease functions to degrade the eDNA, possibly as a means to promote biofilm dispersal.

References

[1]  Costerton JW, Cheng KJ, Geesey GG, Ladd TI, Nickel JC, et al. (1987) Bacterial biofilms in nature and disease. Annu Rev Microbiol 41: 435–464.
[2]  Costerton JW, Lewandowski Z, DeBeer D, Caldwell D, Korber D, et al. (1994) Biofilms, the customized microniche. J Bacteriol 176: 2137–2142.
[3]  Boles BR, Horswill AR (2008) Agr-mediated dispersal of Staphylococcus aureus biofilms. PLoS Pathog 4: e1000052.
[4]  Vuong C, Otto M (2008) The biofilm exopolysaccharide polysaccharide intercellular adhesion–a molecular and biochemical approach. Methods Mol Biol 431: 97–106.
[5]  Otto M (2008) Staphylococcal biofilms. Curr Top Microbiol Immunol 322: 207–228.
[6]  Izano EA, Amarante MA, Kher WB, Kaplan JB (2008) Differential roles of poly-N-acetylglucosamine surface polysaccharide and extracellular DNA in Staphylococcus aureus and Staphylococcus epidermidis biofilms. Appl Environ Microbiol 74: 470–476.
[7]  Rice KC, Mann EE, Endres JL, Weiss EC, Cassat JE, et al. (2007) The cidA murein hydrolase regulator contributes to DNA release and biofilm development in Staphylococcus aureus. Proc Natl Acad Sci U S A 104: 8113–8118.
[8]  Lasa I, Penades JR (2006) Bap: a family of surface proteins involved in biofilm formation. Res Microbiol 157: 99–107.
[9]  Costerton JW (2004) Microbioal Biofilms. In: Ghannoum MaOT, George A, editors. Microbial Biofilms. 1 ed. Washington, D.C.: American Society for Microbiology. pp. 5–19.
[10]  Whitchurch CB, Tolker-Nielsen T, Ragas PC, Mattick JS (2002) Extracellular DNA required for bacterial biofilm formation. Science 295: 1487.
[11]  Allesen-Holm M, Barken KB, Yang L, Klausen M, Webb JS, et al. (2006) A characterization of DNA release in Pseudomonas aeruginosa cultures and biofilms. Mol Microbiol 59: 1114–1128.
[12]  Thomas VC, Thurlow LR, Boyle D, Hancock LE (2008) Regulation of autolysis-dependent eDNA release by Enterococcus faecalis extracellular proteases influences biofilm development. J Bacteriol.
[13]  Steinberger RE, Holden PA (2005) Extracellular DNA in single- and multiple-species unsaturated biofilms. Appl Environ Microbiol 71: 5404–5410.
[14]  Qin Z, Ou Y, Yang L, Zhu Y, Tolker-Nielsen T, et al. (2007) Role of autolysin-mediated DNA release in biofilm formation of Staphylococcus epidermidis. Microbiology 153: 2083–2092.
[15]  Bockelmann U, Janke A, Kuhn R, Neu TR, Wecke J, et al. (2006) Bacterial extracellular DNA forming a defined network-like structure. FEMS Microbiol Lett 262: 31–38.
[16]  Mulcahy H, Charron-Mazenod L, Lewenza S (2008) Extracellular DNA chelates cations and induces antibiotic resistance in Pseudomonas aeruginosa biofilms. PLoS Pathog 4: e1000213.
[17]  Webb JS, Thompson LS, James S, Charlton T, Tolker-Nielsen T, et al. (2003) Cell death in Pseudomonas aeruginosa biofilm development. J Bacteriol 185: 4585–4592.
[18]  Rice KC, Firek BA, Nelson JB, Yang SJ, Patton TG, et al. (2003) The Staphylococcus aureus cidAB operon: evaluation of its role in regulation of murein hydrolase activity and penicillin tolerance. J Bacteriol 185: 2635–2643.
[19]  Groicher KH, Firek BA, Fujimoto DF, Bayles KW (2000) The Staphylococcus aureus lrgAB operon modulates murein hydrolase activity and penicillin tolerance. J Bacteriol 182: 1794–1801.
[20]  Rice KC, Bayles KW (2008) Molecular control of bacterial death and lysis. Microbiol Mol Biol Rev 72: 85–109. table of contents.
[21]  Rice KC, Bayles KW (2003) Death's toolbox: examining the molecular components of bacterial programmed cell death. Mol Microbiol 50: 729–738.
[22]  Brunskill EW, Bayles KW (1996) Identification and molecular characterization of a putative regulatory locus that affects autolysis in Staphylococcus aureus. J Bacteriol 178: 611–618.
[23]  Yang SJ, Rice KC, Brown RJ, Patton TG, Liou LE, et al. (2005) A LysR-type regulator, CidR, is required for induction of the Staphylococcus aureus cidABC operon. J Bacteriol 187: 5893–5900.
[24]  Patton TG, Yang SJ, Bayles KW (2006) The role of proton motive force in expression of the Staphylococcus aureus cid and lrg operons. Mol Microbiol 59: 1395–1404.
[25]  Rice KC, Nelson JB, Patton TG, Yang SJ, Bayles KW (2005) Acetic acid induces expression of the Staphylococcus aureus cidABC and lrgAB murein hydrolase regulator operons. J Bacteriol 187: 813–821.
[26]  Gillaspy AF, Hickmon SG, Skinner RA, Thomas JR, Nelson CL, et al. (1995) Role of the accessory gene regulator (agr) in pathogenesis of staphylococcal osteomyelitis. Infect Immun 63: 3373–3380.
[27]  Shafer WM, Iandolo JJ (1979) Genetics of staphylococcal enterotoxin B in methicillin-resistant isolates of Staphylococcus aureus. Infect Immun 25: 902–911.
[28]  Cassat JE, Dunman PM, McAleese F, Murphy E, Projan SJ, et al. (2005) Comparative genomics of Staphylococcus aureus musculoskeletal isolates. J Bacteriol 187: 576–592.
[29]  Heydorn A, Nielsen AT, Hentzer M, Sternberg C, Givskov M, et al. (2000) Quantification of biofilm structures by the novel computer program COMSTAT. Microbiology 146(Pt 10): 2395–2407.
[30]  Yang L, Barken KB, Skindersoe ME, Christensen AB, Givskov M, et al. (2007) Effects of iron on DNA release and biofilm development by Pseudomonas aeruginosa. Microbiology 153: 1318–1328.
[31]  Yabu K, Kaneda S (1995) Salt-induced cell lysis of Staphylococcus aureus. Curr Microbiol 30: 299–303.
[32]  Wecke J, Lahav M, Ginsburg I, Kwa E, Giesbrecht P (1986) Inhibition of wall autolysis of staphylococci by sodium polyanethole sulfonate “liquoid”. Arch Microbiol 144: 110–115.
[33]  Rice KC, Patton T, Yang SJ, Dumoulin A, Bischoff M, et al. (2004) Transcription of the Staphylococcus aureus cid and lrg murein hydrolase regulators is affected by sigma factor B. J Bacteriol 186: 3029–3037.
[34]  Brunskill E (1995) Investigation and analysis of the LytS and LytR two-component regulatory system from Staphylococcus aureus: the molecular control of autolysis: University of Maryland Graduate School.
[35]  Webb JS, Lau M, Kjelleberg S (2004) Bacteriophage and phenotypic variation in Pseudomonas aeruginosa biofilm development. J Bacteriol 186: 8066–8073.
[36]  Patton TG, Rice KC, Foster MK, Bayles KW (2005) The Staphylococcus aureus cidC gene encodes a pyruvate oxidase that affects acetate metabolism and cell death in stationary phase. Mol Microbiol 56: 1664–1674.
[37]  Ogris M, Wagner E, Steinlein P (2000) A versatile assay to study cellular uptake of gene transfer complexes by flow cytometry. Biochim Biophys Acta 1474: 237–243.
[38]  Bayles KW (2007) The biological role of death and lysis in biofilm development. Nat Rev Microbiol 5: 721–726.
[39]  Cassat J, Dunman PM, Murphy E, Projan SJ, Beenken KE, et al. (2006) 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 152: 3075–3090.
[40]  Beenken KE, Dunman PM, McAleese F, Macapagal D, Murphy E, et al. (2004) Global gene expression in Staphylococcus aureus biofilms. J Bacteriol 186: 4665–4684.
[41]  Tsang LH, Cassat JE, Shaw LN, Beenken KE, Smeltzer MS (2008) Factors contributing to the biofilm-deficient phenotype of Staphylococcus aureus sarA mutants. PLoS ONE 3: e3361.
[42]  Bayles KW (2003) Are the molecular strategies that control apoptosis conserved in bacteria? Trends Microbiol 11: 306–311.
[43]  Stewart PS, Rani SA, Gjersing E, Codd SL, Zheng Z, et al. (2007) Observations of cell cluster hollowing in Staphylococcus epidermidis biofilms. Lett Appl Microbiol 44: 454–457.
[44]  Ma L, Conover M, Lu H, Parsek MR, Bayles K, et al. (2009) Assembly and development of the Pseudomonas aeruginosa biofilm matrix. PLoS Pathog 5: e1000354.
[45]  Yang SJ, Dunman PM, Projan SJ, Bayles KW (2006) Characterization of the Staphylococcus aureus CidR regulon: elucidation of a novel role for acetoin metabolism in cell death and lysis. Mol Microbiol 60: 458–468.
[46]  Rani SA, Pitts B, Beyenal H, Veluchamy RA, Lewandowski Z, et al. (2007) Spatial patterns of DNA replication, protein synthesis, and oxygen concentration within bacterial biofilms reveal diverse physiological states. J Bacteriol 189: 4223–4233.
[47]  Brunskill EW, Bayles KW (1996) Identification of LytSR-regulated genes from Staphylococcus aureus. J Bacteriol 178: 5810–5812.
[48]  Yarwood JM, Bartels DJ, Volper EM, Greenberg EP (2004) Quorum sensing in Staphylococcus aureus biofilms. J Bacteriol 186: 1838–1850.
[49]  Hanahan D (1983) Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166: 557–580.
[50]  Kreiswirth BN, Lofdahl S, Betley MJ, O'Reilly M, Schlievert PM, et al. (1983) The toxic shock syndrome exotoxin structural gene is not detectably transmitted by a prophage. Nature 305: 709–712.
[51]  Miller LG, Perdreau-Remington F, Rieg G, Mehdi S, Perlroth J, et al. (2005) Necrotizing fasciitis caused by community-associated methicillin-resistant Staphylococcus aureus in Los Angeles. N Engl J Med 352: 1445–1453.
[52]  Kazakova SV, Hageman JC, Matava M, Srinivasan A, Phelan L, et al. (2005) A clone of methicillin-resistant Staphylococcus aureus among professional football players. N Engl J Med 352: 468–475.
[53]  Charpentier E, Anton AI, Barry P, Alfonso B, Fang Y, et al. (2004) Novel cassette-based shuttle vector system for gram-positive bacteria. Appl Environ Microbiol 70: 6076–6085.

Full-Text

Contact Us

service@oalib.com

QQ:3279437679

WhatsApp +8615387084133