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Extracellular DNA as Matrix Component in Microbial Biofilms

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Part of the book series: Nucleic Acids and Molecular Biology ((NUCLEIC,volume 25))

Abstract

Bacteria in nature primarily live in surface-associated communities commonly known as biofilms. Because bacteria in biofilms, in many cases, display tolerance to host immune systems, antibiotics, and biocides, they are often difficult or impossible to eradicate. Biofilm formation, therefore, leads to various persistent infections in humans and animals, and to a variety of complications in industry, where solid–water interfaces occur. Knowledge about the molecular mechanisms involved in biofilm formation is necessary for creating strategies to control biofilms. Recent studies have shown that extracellular DNA is an important component of the extracellular matrix of microbial biofilms. The present chapter is focussed on extracellular DNA as matrix component in biofilms formed by Pseudomonas aeruginosa as an example from the Gram-negative bacteria, and Streptococcus and Staphylococcus as examples from the Gram-positive bacteria. Besides the role of extracellular DNA in biofilm formation, the mechanisms involved in DNA release from P. aeruginosa, Streptococcus, and Staphylococcus are addressed.

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References

  • Aas FE, Wolfgang M, Frye S, Dunham S, Lovold C, Koomey M (2002) Competence for natural transformation in Neisseria gonorrhoeae: components of DNA binding and uptake linked to type IV pilus expression. Mol Microbiol 46:749–760

    Article  PubMed  CAS  Google Scholar 

  • Allesen-Holm M, Barken KB, Yang L, Klausen M, Webb JS, Kjelleberg S, Molin S, Givskov M, Tolker-Nielsen T (2006) A characterization of DNA-release in Pseudomonas aeruginosa cultures and biofilms. Mol Microbiol 59:1114–1128

    Article  PubMed  CAS  Google Scholar 

  • Baltimore RS, Christie CD, Smith GJ (1989) Immunohistopathologic localization of Pseudomonas aeruginosa in lungs from patients with cystic fibrosis. Am Rev Respir Dis 140:1650–1661

    Article  PubMed  CAS  Google Scholar 

  • Barken KB, Pamp SJ, Yang L, Gjermansen M, Bertrand JJ, Klausen M, Givskov M, Whitchurch CB, Engel JN, Tolker-Nielsen T (2008) Roles of type IV pili, flagellum-mediated motility and extracellular DNA in the formation of mature multicellular structures in Pseudomonas aeruginosa biofilms. Environ Microbiol 10:2331–2343

    Article  PubMed  CAS  Google Scholar 

  • Bartilson M, Marra A, Christine J, Asundi JS, Schneider WP, Hromockyj AE (2001) Differential fluorescence induction reveals Streptococcus pneumoniae loci regulated by competence stimulatory peptide. Mol Microbiol 39:126–135

    Article  PubMed  CAS  Google Scholar 

  • Bayles KW (2003) Are the molecular strategies that control apoptosis conserved in bacteria? Trends Microbiol 11:306–311

    Article  PubMed  CAS  Google Scholar 

  • Biswas R, Voggu L, Simon UK, Hentschel P, Thumm G, Gotz F (2006) Activity of the major staphylococcal autolysin Atl. FEMS Microbiol Lett 259:260–268

    Article  PubMed  CAS  Google Scholar 

  • Collier DN, Anderson L, McKnight SL, Noah TL, Knowles M, Boucher R, Schwab U, Gilligan P, Pesci EC (2002) A bacterial cell to cell signal in the lungs of cystic fibrosis patients. FEMS Microbiol Lett 215:41–46

    Article  PubMed  CAS  Google Scholar 

  • Costerton JW, Stewart PS, Greenberg EP (1999) Bacterial biofilms: a common cause of persistent infections. Science 284:1318–1322

    Article  PubMed  CAS  Google Scholar 

  • D’Argenio DA, Calfee MW, Rainey PB, Pesci EC (2002) Autolysis and autoaggregation in Pseudomonas aeruginosa colony morphology mutants. J Bacteriol 184:6481–6489

    Article  PubMed  Google Scholar 

  • Davies DG, Parsek MR, Pearson JP, Iglewski BH, Costerton JW, Greenberg EP (1998) The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280:295–298

    Article  PubMed  CAS  Google Scholar 

  • Dillard JP, Seifert HS (2001) A variable genetic island specific for Neisseria gonorrhoeae is involved in providing DNA for natural transformation and is found more often in disseminated infection isolates. Mol Microbiol 41:263–277

    Article  PubMed  CAS  Google Scholar 

  • Dubnau D (1999) DNA uptake in bacteria. Annu Rev Microbiol 53:217–244

    Article  PubMed  CAS  Google Scholar 

  • Eckhart L, Fischer H, Barken KB, Tolker-Nielsen T, Tschachler E (2007) DNase1L2 suppresses biofilm formation by Pseudomonas aeruginosa and Staphylococcus aureus. Br J Dermatol 156:1342–1345

    Article  PubMed  CAS  Google Scholar 

  • Espinosa-Urgel M, Salido A, Ramos JL (2000) Genetic analysis of functions involved in adhesion of Pseudomonas putida to seeds. J Bacteriol 182:2363–2369

    Article  PubMed  CAS  Google Scholar 

  • Fournier B, Hooper DC (2000) A new two-component system involved in adhesion, autolysis, and extracellular proteolytic activity of Staphylococcus aureus. J Bacteriol 182:3955–3964

    Article  PubMed  CAS  Google Scholar 

  • Fredheim EGA, Klingenberg C, Rohde H, Frankenberger S, Gaustad P, Flægstad T, Sollid JE (2009) Biofilm formation by Staphylococcus haemolyticus. J Clin Microbiol 47:1172–1180

    Article  PubMed  CAS  Google Scholar 

  • Friedman L, Kolter R (2004) Two genetic loci produce distinct carbohydrate-rich structural components of the Pseudomonas aeruginosa biofilm matrix. J Bacteriol 186:4457–4465

    Article  PubMed  CAS  Google Scholar 

  • Froshauer S, Silvia AM, Chidambaram M, Sharma B, Weinstock GM (1996) Sensitization of bacteria to danofloxacin by temperate prophages. Antimicrob Agents Chemother 40:1561–1563

    PubMed  CAS  Google Scholar 

  • Guiral S, Mitchell TJ, Martin B, Claverys JP (2005) Competence-programmed predation of noncompetent cells in the human pathogen Streptococcus pneumoniae: genetic requirements. Proc Natl Acad Sci USA 102:8710–8715

    Article  PubMed  CAS  Google Scholar 

  • Hara T, Aumayr A, Ueda S (1981) Genetic transformation of Pseudomonas aeruginosa with extracellular DNA. J Gen Appl Microbiol 27:109–114

    Article  CAS  Google Scholar 

  • Hava DL, LeMieux J, Camilli A (2003) From nose to lung: the regulation behind Streptococcus pneumoniae virulence factors. Mol Microbiol 50:1103–1110

    Article  PubMed  CAS  Google Scholar 

  • Hendrickx L, Hausner M, Wuertz S (2003) Natural genetic transformation in monoculture Acinetobacter sp. BD413 biofilms. Appl Environ Microbiol 69:1721–1727

    Article  PubMed  CAS  Google Scholar 

  • Hentzer M, Givskov M, Eberl L (2004) Quorum sensing in biofilms: gossip in the slime world? In: Ghannoum M, O’Toole GA (eds) Microbial Biofilms. ASM, Washington, DC, pp 118–140

    Google Scholar 

  • Heurlier K, Denervaud V, Haenni M, Guy L, Krishnapillai V, Haas D (2005) Quorum-sensing-negative (lasR) mutants of Pseudomonas aeruginosa avoid cell lysis and death. J Bacteriol 187:4875–4883

    Article  PubMed  CAS  Google Scholar 

  • Høiby N (2002) Understanding bacterial biofilms in patients with cystic fibrosis: current and innovative approaches to potential therapies. J Cyst Fibros 1:249–254

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Jedrzejas MJ (2001) Pneumococcal virulence factors: structure and function. Microbiol Mol Biol Rev 65:187–207

    Article  PubMed  CAS  Google Scholar 

  • Kadurugamuwa JL, Beveridge TJ (1996) Bacteriolytic effect of membrane vesicles from Pseudomonas aeruginosa on other bacteria including pathogens: conceptually new antibiotics. J Bacteriol 178:2767–2774

    PubMed  CAS  Google Scholar 

  • Klausen M, Aaes-Jorgensen A, Molin S, Tolker-Nielsen T (2003a) Involvement of bacterial migration in the development of complex multicellular structures in Pseudomonas aeruginosa biofilms. Mol Microbiol 50:61–68

    Article  PubMed  CAS  Google Scholar 

  • Klausen M, Heydorn A, Ragas P, Lambertsen L, Aaes-Jorgensen A, Molin S, Tolker-Nielsen T (2003b) Biofilm formation by Pseudomonas aeruginosa wild type, flagella and type IV pili mutants. Mol Microbiol 48:1511–1524

    Article  PubMed  CAS  Google Scholar 

  • Kreth J, Merritt J, Shi W, Qi F (2005) Co-ordinated bacteriocin production and competence development: a possible mechanism for taking up DNA from neighbouring species. Mol Microbiol 57:392–404

    Article  PubMed  CAS  Google Scholar 

  • Kreth J, Zhang Y, Herzberg MC (2008) Streptococcal antagonism in oral biofilms: Streptococcus sanguinis and Streptococcus gordonii interference with Streptococcus mutans. J Bacteriol 190:4632–4640

    Article  PubMed  CAS  Google Scholar 

  • Lam J, Chan R, Lam K, Costerton JW (1980) Production of mucoid microcolonies by Pseudomonas aeruginosa within infected lungs in cystic fybrosis. Infect Immun 28:546–556

    PubMed  CAS  Google Scholar 

  • Lau GW, Haataja S, Lonetto M, Kensit SE, Marra A, Bryant AP, McDevitt D, Morrison DA, Holden DW (2001) A functional genomic analysis of type 3 Streptococcus pneumoniae virulence. Mol Microbiol 40:555–571

    Article  PubMed  CAS  Google Scholar 

  • Lethem MI, James SL, Marriott C, Burke JF (1990) The origin of DNA associated with mucus glycoproteins in cystic fibrosis sputum. Eur Respir J 3:19–23

    PubMed  CAS  Google Scholar 

  • Li YH, Lau PCY, Lee JH, Ellen RP, Cvitkovitch DG (2001) Natural genetic transformation of Streptococcus mutans growing in biofilms. J Bacteriol 183:897–908

    Article  PubMed  CAS  Google Scholar 

  • Li YH, Tang N, Aspiras MB, Lau PC, Lee JH, Ellen RP, Cvitkovitch DG (2002) A quorum-sensing signaling system essential for genetic competence in Streptococcus mutans is involved in biofilm formation. J Bacteriol 184:2699–2708

    Article  PubMed  CAS  Google Scholar 

  • Loo CY, Corliss DA, Ganeshkumar N (2000) Streptococcus gordonii biofilm formation: identification of genes that code for biofilm phenotypes. J Bacteriol 182:1374–1382

    Article  PubMed  CAS  Google Scholar 

  • Lorenz MG, Wackernagel W (1994) Bacterial gene transfer by natural genetic transformation in the environment. Microbiol Rev 58:563–602

    PubMed  CAS  Google Scholar 

  • Lorenz MG, Gerjets D, Wackernagel W (1991) Release of transforming plasmid and Chromosomal DNA from two cultured soil bacteria. Arch Microbiol 156:319–326

    Article  PubMed  CAS  Google Scholar 

  • Lowy F (1998) Staphylococcus aureus infections. N Engl J Med 339:520–532

    Article  PubMed  CAS  Google Scholar 

  • Mack D, Rohde H, Harris LG, Davies AP, Horstkotte MA, Knobloch JK (2006) Biofilm formation in medical device-related infection. Int J Artif Organs 29:343–359

    PubMed  CAS  Google Scholar 

  • Mashburn LM, Whiteley M (2005) Membrane vesicles traffic signals and facilitate group activities in a prokaryote. Nature 437:422–425

    Article  PubMed  CAS  Google Scholar 

  • Matsukawa M, Greenberg EP (2004) Putative exopolysaccharide synthesis genes influence Pseudomonas aeruginosa biofilm development. J Bacteriol 186:4449–4456

    Article  PubMed  CAS  Google Scholar 

  • Matz C, Kjelleberg S (2005) Off the hook – how bacteria survive protozoan grazing. Trends Microbiol 13:302–307

    Article  PubMed  CAS  Google Scholar 

  • Moreau-Marquis S, Stanton BA, O'Toole GA (2008) Pseudomonas aeruginosa biofilm formation in the cystic fibrosis airway. Pulm Pharmacol Ther 21:595–599

    Article  PubMed  CAS  Google Scholar 

  • Moscoso M, Claverys JP (2004) Release of DNA into the medium by competent Streptococcus pneumoniae: kinetics, mechanism and stability of the liberated DNA. Mol Microbiol 54:783–794

    Article  PubMed  CAS  Google Scholar 

  • Mulcahy H, Charron-Mazenod L, Lewenza S (2008) Extracellular DNA chelates cations and induces antibiotic resistance in Pseudomonas aeruginosa biofilms. PLoS Pathog 4:1–12

    Article  Google Scholar 

  • Murakawa T (1973a) Slime production by Pseudomonas aeruginosa. III. Purification of slime and its physicochemical properties. Jpn J Microbiol 17:273–281

    PubMed  CAS  Google Scholar 

  • Murakawa T (1973b) Slime production by Pseudomonas aeruginosa. IV. Chemical analysis of two varieties of slime produced by Pseudomonas aeruginosa. Jpn J Microbiol 17:513–520

    PubMed  CAS  Google Scholar 

  • Muto Y, Goto S (1986) Transformation by extracellular DNA produced by Pseudomonas aeruginosa. Microbiol Immunol 30:621–628

    PubMed  CAS  Google Scholar 

  • Nakamura S, Higashiyama Y, Izumikawa K, Seki M, Kakeya H, Yamamoto Y, Yanagihara K, Miyazaki Y, Mizuta Y, Kohno S (2008) The roles of the quorum-sensing system in the release of extracellular DNA, lipopolysaccharide, and membrane vesicles from Pseudomonas aeruginosa. Jpn J Infect Dis 61:375–378

    PubMed  CAS  Google Scholar 

  • Nemoto K, Hirota K, Murakami K, Taniguti K, Murata H, Viducic D, Miyake Y (2003) Effect of Varidase (streptodornase) on biofilm formed by Pseudomonas aeruginosa. Chemotherapy 49:121–125

    Article  PubMed  CAS  Google Scholar 

  • Palmen R, Hellingwerf KJ (1995) Acinetobacter calcoaceticus liberates chromosomal DNA during induction of competence by cell lysis. Curr Microbiol 30:7–10

    Article  PubMed  CAS  Google Scholar 

  • Palmer KL, Mashburn LM, Singh PK, Whiteley M (2005) Cystic fibrosis sputum supports growth and cues key aspects of Pseudomonas aeruginosa physiology. J Bacteriol 187:5267–5277

    Article  PubMed  CAS  Google Scholar 

  • Petersen FC, Pecharki D, Scheie AA (2004) Biofilm mode of growth of Streptococcus intermedius favored by a competence-stimulating signaling peptide. J Bacteriol 186:6327–6331

    Article  PubMed  CAS  Google Scholar 

  • Petersen FC, Tao L, Scheie AA (2005) DNA binding-uptake system: a link between cell-to-cell communication and biofilm formation. J Bacteriol 187:4392–4400

    Article  PubMed  CAS  Google Scholar 

  • Phillips I, Culebras E, Moreno F, Baquero F (1987) Induction of the SOS response by new 4-quinolones. J Antimicrob Chemother 20:631–638

    Article  PubMed  CAS  Google Scholar 

  • Qin Z, Ou Y, Yang L, Zhu Y, Tolker-Nielsen T, Molin S, Qu D (2007) Role of autolysin-mediated DNA release in biofilm formation of Staphylococcus epidermidis. Microbiology 153:2083–2092

    Article  PubMed  CAS  Google Scholar 

  • Renelli M, Matias V, Lo RY, Beveridge TJ (2004) DNA-containing membrane vesicles of Pseudomonas aeruginosa PAO1 and their genetic transformation potential. Microbiology 150:2161–2169

    Article  PubMed  CAS  Google Scholar 

  • Rice KC, Mann EE, Endres JL, WeissEC CJE, Smeltzer MS, Bayles KW (2007) The cidA murein hydrolase regulator contributes to DNA release and biofilm development in Staphylococcus aureus. Proc Natl Acad Sci USA 104:8113–8118

    Article  PubMed  CAS  Google Scholar 

  • Rupp ME, Archer GL (1994) Coagulase-negative staphylococci: pathogens associated with medical progress. Clin Infect Dis 19:231–243

    Article  PubMed  CAS  Google Scholar 

  • Schlegel R, Slade HD (1973) Properties of a Streptococcus sanguis (group H) bacteriocin and its separation from the competence factor of transformation. J Bacteriol 115:655–661

    PubMed  CAS  Google Scholar 

  • Seidl K, Goerke C, Woiz C, Mack D, Berger-Baechi B, Bischoff M (2008) Staphylococcus aureus CcpA affects biofilm formation. Infect Immun 76:2044–2050

    Article  PubMed  CAS  Google Scholar 

  • Shibata Y, Kawada M, Nakano Y, Toyoshima K, Yamashita Y (2005) Identification and characterization of an autolysin-encoding gene of Streptococcus mutans. Infect Immun 73:3512–3520

    Article  PubMed  CAS  Google Scholar 

  • Sriramulu DD, Lunsdorf H, Lam JS, Römling U (2005) Microcolony formation: a novel biofilm model of Pseudomonas aeruginosa for the cystic fibrosis lung. J Med Microbiol 54:667–676

    Article  PubMed  Google Scholar 

  • Steinberger RE, Holden PA (2005) Extracellular DNA in single- and multiple-species unsaturated biofilms. Appl Environ Microbiol 71:5404–5410

    Article  PubMed  CAS  Google Scholar 

  • Steinmoen H, Knutsen E, Håvarstein LS (2002) Induction of natural competence in Streptococcus pneumoniae triggers lysis and DNA release from a subfraction of the cell population. Proc Natl Acad Sci USA 99:7681–7686

    Article  PubMed  CAS  Google Scholar 

  • Steinmoen H, Teigen A, Håvarstein LS (2003) Competence-induced cells of Streptococcus pneumoniae lyse competence-deficient cells of the same strain during cocultivation. J Bacteriol 185:7176–7183

    Article  PubMed  CAS  Google Scholar 

  • Stewart GJ, Carlson CA, Ingraham JL (1983) Evidence for an active role of donor cells in natural transformation of Pseudomonas stutzeri. J Bacteriol 156:30–35

    PubMed  CAS  Google Scholar 

  • Sutherland IW (2001) The biofilm matrix – an immobilized but dynamic microbial environment. Arch Microbiol 9:222–227

    CAS  Google Scholar 

  • Thomas SR, Ray A, Hodson ME, Pitt TL (2000) Increased sputum amino acid concentrations and auxotrophy of Pseudomonas aeruginosa in severe cystic fibrosis lung disease. Thorax 55:795–797

    Article  PubMed  CAS  Google Scholar 

  • Trotonda MP, Tamber S, Memmi G, Cheung AL (2008) MgrA represses biofilm formation in Staphylococcus aureus. Infect Immun 76:5645–5654

    Article  PubMed  CAS  Google Scholar 

  • van der Ploeg JR (2005) Regulation of bacteriocin production in Streptococcus mutans by the quorum-sensing system required for development of genetic competence. J Bacteriol 187:3980–3989

    Article  PubMed  Google Scholar 

  • van Schaik EJ, Giltner CL, Audette GF, Keizer DW, Bautista DL, Slupsky CM, Sykes BD, Irvin RT (2005) DNA binding: a novel function of Pseudomonas aeruginosa type IV pili. J Bacteriol 187:1455–1464

    Article  PubMed  Google Scholar 

  • Vuong C, Gotz F, Otto M (2000) Construction and characterization of an agr deletion mutant of Staphylococcus epidermidis. Infect Immun 68:1048–1053

    Article  PubMed  CAS  Google Scholar 

  • Walker TS, Tomlin KL, Worthen GS, Poch KR, Lieber JG, Saavedra MT, Fessler MB, Malcolm KC, Vasil ML, Nick JA (2005) Enhanced Pseudomonas aeruginosa biofilm development mediated by human neutrophils. Infect Immun 73:3693–3701

    Article  PubMed  CAS  Google Scholar 

  • Wang BY, Chi B, Kuramitsu HK (2002) Genetic exchange between Treponema denticola and Streptococcus gordonii in biofilms. Oral Microbiol Immunol 2:108–112

    Article  Google Scholar 

  • Webb JS, Thompson LS, James S, Charlton T, Tolker-Nielsen T, Koch B, Givskov M, Kjelleberg S (2003) Cell death in Pseudomonas aeruginosa biofilm Development. J Bacteriol 185:4585–4592

    Article  PubMed  CAS  Google Scholar 

  • Whitchurch CB, Tolker-Nielsen T, Ragas PC, Mattick JS (2002) Extracellular DNA is required for bacterial biofilm formation. Science 295:1487

    Article  PubMed  CAS  Google Scholar 

  • Worlitzsch D, Tarran R, Ulrich M, Schwab U, Cekici A, Meyer KC, Birrer P, Bellon G, Berger J, Weiss T, Botzenhart K, Yankaskas JR, Randell S, Boucher RC, Döring G (2002) Effects of reduced mucus oxygen concentration in airway Pseudomonas infections of cystic fibrosis patients. J Clin Invest 109:317–325

    PubMed  CAS  Google Scholar 

  • Yang L, Barken KB, Skindersoe ME, Christensen AB, Givskov M, Tolker-Nielsen T (2007) Effects of iron on DNA release and biofilm development by Pseudomonas aeruginosa. Microbiology 153:1318–1328

    Article  PubMed  CAS  Google Scholar 

  • Yoshida A, Kuramitsu HK (2002) Multiple Streptococcus mutans genes are involved in biofilm formation. Appl Environ Microbiol 68:6283–6291

    Article  PubMed  CAS  Google Scholar 

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Chiang, WC., Tolker-Nielsen, T. (2010). Extracellular DNA as Matrix Component in Microbial Biofilms. In: Kikuchi, Y., Rykova, E. (eds) Extracellular Nucleic Acids. Nucleic Acids and Molecular Biology, vol 25. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-12617-8_1

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