The role of extracellular DNA in the establishment, maintenance and perpetuation of bacterial biofilms

References

• Allesen-Holm M, Barken KB, Yang L, et al. (2006). A characterization of DNA release in Pseudomonas aeruginosa cultures and biofilms. Mol Microbiol 59:1114–28
   PubMed Web of Science ®Google Scholar
• Andersson S, Dalhammar G, Land C, Kuttuva Rajarao G. (2009). Characterization of extracellular polymeric substances from denitrifying organism Comamonas denitrificans. Appl Microbiol Biotechnol 82:535--43
   Google Scholar
• Araújo E, de Andrade N, da Silva L, et al. (2010). Control of microbial adhesion as a strategy for food and bioprocess technology. Food Bioprocess Tech 3:321–32
   Google Scholar
• Arciola C, Montanaro L, Costerton J. (2011). New trends in diagnosis and control strategies for implant infections. Int J Artif Organs 34:727
   PubMed Web of Science ®Google Scholar
• Arciola CR. (2009). New concepts and new weapons in implant infections. Int J Artif Organs 32:533–6
   PubMed Web of Science ®Google Scholar
• Arenas J, Nijland R, Rodriguez FJ, et al. (2013). Involvement of three meningococcal surface-exposed proteins, the heparin-binding protein NhbA, the α-peptide of IgA protease and the autotransporter protease NalP, in initiation of biofilm formation. Mol Microb 87:254–68
   PubMed Web of Science ®Google Scholar
• Barken KB, Pamp SJ, Yang L, et al. (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 10:2331–43
   PubMed Web of Science ®Google Scholar
• Barnes AMT, Ballering KS, Leibman RS, et al. (2012). Enterococcus faecalis produces abundant extracellular structures containing DNA in the absence of cell lysis during early biofilm formation. mBio 3:e00193--00112
   Web of Science ®Google Scholar
• Bauer S, Kirschning CJ, Häcker H, et al. (2001). Human TLR9 confers responsiveness to bacterial DNA via species-specific CpG motif recognition. PNAS 98:9237–42
   PubMed Web of Science ®Google Scholar
• Bayles KW. (2003). Are the molecular strategies that control apoptosis conserved in bacteria? Trends Microbiol 11:306–11
   PubMedGoogle Scholar
• Berne C, Kysela DT, Brun YV. (2010). A bacterial extracellular DNA inhibits settling of motile progeny cells within a biofilm. Mol Microbiol 77:815–29
   PubMed Web of Science ®Google Scholar
• Biswas R, Voggu L, Simon UK, et al. (2006). Activity of the major staphylococcal autolysin Atl. FEMS Microbiol Lett 259:260–8
   PubMed Web of Science ®Google Scholar
• Björklöf K, Nurmiaho-Lassila EL, Klinger N, et al. (2001). Colonization strategies and conjugal gene transfer of inoculated Pseudomonas syringae on the leaf surface. J Appl Microbiol 89:423–32
   Google Scholar
• Böckelmann U, Janke A, Kuhn R, et al. (2006). Bacterial extracellular DNA forming a defined network-like structure. FEMS Microbiol Lett 262:31–8
   PubMed Web of Science ®Google Scholar
• Boks NP, Norde W, van der Mei HC, Busscher HJ. (2008). Forces involved in bacterial adhesion to hydrophilic and hydrophobic surfaces. Microbiology 154:3122–33
   PubMed Web of Science ®Google Scholar
• Bourgeois I, Camiade E, Biswas R, et al. (2009). Characterization of AtlL, a bifunctional autolysin of Staphylococcus lugdunensis with N-acetylglucosaminidase and N-acetylmuramoyl-L-alanine amidase activities. FEMS Microbiol Lett 290:105–13
   PubMed Web of Science ®Google Scholar
• Brinkmann V, Reichard U, Goosmann C, et al. (2004). Neutrophil extracellular traps kill bacteria. Science 303:1532–5
   PubMed Web of Science ®Google Scholar
• Brinkmann V, Zychlinsky A. (2012). Neutrophil extracellular traps: is immunity the second function of chromatin? J Cell Biol 198:773–83
   PubMed Web of Science ®Google Scholar
• Busscher HJ, Norde W, van der Mei HC. (2008). Specific molecular recognition and nonspecific contributions to bacterial interaction forces. Appl Environ Microbiol 74:2559–64
   PubMed Web of Science ®Google Scholar
• Carrolo M, Frias MJ, Pinto FR, et al. (2010). Prophage spontaneous activation promotes DNA release enhancing biofilm formation in Streptococcus pneumoniae. PLoS ONE 5:e15678
   PubMed Web of Science ®Google Scholar
• Chandramohan L, Ahn J-S, Weaver KE, Bayles KW. (2009). An averlap between the control of programmed cell death in Bacillus anthracis and sporulation. J Bacteriol 191:4103–10
   PubMedGoogle Scholar
• Chiang WC, Nilsson M, Jensen PO, et al. (2013). Extracellular DNA shields against aminoglycosides in Pseudomonas aeruginosa biofilms. Antimicrob Agents Ch 57:2352–61
   PubMed Web of Science ®Google Scholar
• Conover MS, Mishra M, Deora R. (2011). Extracellular DNA is sssential for maintaining Bordetella biofilm integrity on abiotic surfaces and in the upper respiratory tract of mice. PLoS ONE 6:e16861
   Google Scholar
• Costerton JW, Stewart PS, Greenberg EP. (1999). Bacterial biofilms: a common cause of persistent infections. Science 284:1318–22
   PubMed Web of Science ®Google Scholar
• Dai L, Yang L, Parsons C, et al. (2012). Staphylococcus epidermidis recovered from indwelling catheters exhibit enhanced biofilm dispersal and “self-renewal” through downregulation of agr. BMC Microbiol 12:1–9
   PubMedGoogle Scholar
• Das T, Krom BP, van der Mei HC, et al. (2011a). DNA-mediated bacterial aggregation is dictated by acid-base interactions. Soft Matter 7:2927–35
   Google Scholar
• Das T, Kutty SK, Kumar N, Manefield M. (2013). Pyocyanin facilitates extracellular DNA binding to Pseudomonas aeruginosa influencing cell surface properties and aggregation. PLoS ONE 8:e58299
   PubMed Web of Science ®Google Scholar
• Das T, Sharma PK, Busscher HJ, et al. (2010). Role of extracellular DNA in initial bacterial adhesion and surface aggregation. Appl Environ Microbiol 76:3405–8
   PubMed Web of Science ®Google Scholar
• Das T, Sharma PK, Krom BP, et al. (2011b). Role of eDNA on the adhesion forces between Streptococcus mutans and substratum surfaces: influence of ionic strength and substratum hydrophobicity. Langmuir 27:10113–8
   PubMed Web of Science ®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 41:263–77
   PubMedGoogle Scholar
• Eckhart L, Fischer H, Barken KB, et al. (2007). DNase1L2 suppresses biofilm formation by Pseudomonas aeruginosa and Staphylococcus aureus. Brit J Dermatol 156:1342--45
   Google Scholar
• Flemming H-C, Wingender J. (2010). The biofilm matrix. Nat Rev Microbiol 8:623–33
   PubMed Web of Science ®Google Scholar
• Foster SJ. (1995). Molecular characterization and functional analysis of the major autolysin of Staphylococcus aureus 8325/4. J Bacteriol 177:5723–5
   PubMed Web of Science ®Google Scholar
• Fredheim EGA, Klingenberg C, Rohde H, et al. (2009). Biofilm formation by Staphylococcus haemolyticus. J Clin Microbiol 47:1172--80
   Google Scholar
• Fournier B, Hooper DC. (2000). A new two-component regulatory system Involved in adhesion, autolysis, and extracellular proteolytic activity of Staphylococcus aureus. J Bacteriol 182:3955–64
   PubMed Web of Science ®Google Scholar
• Frederiksen B, Pressler T, Hansen A, et al. (2006). Effect of aerosolized rhDNase (Pulmozyme®) on pulmonary colonization in patients with cystic fibrosis. Acta Pædiatrica 95:1070–4
   PubMed Web of Science ®Google Scholar
• Gloag ES, Turnbull L, Huang A, et al. (2013). Self-organization of bacterial biofilms is facilitated by extracellular DNA. PNAS 110:11541–6
   PubMed Web of Science ®Google Scholar
• Godeke J, Paul K, Lassak J, Thormann KM. (2011). Phage-induced lysis enhances biofilm formation in Shewanella oneidensis MR-1. ISME J 5:613--26
   Google Scholar
• Griffith F. (1928). The significance of pneumococcal types. J Hyg Camb 27:113–59
   PubMedGoogle Scholar
• Groicher KH, Firek BA, Fujimoto DF, Bayles KW. (2000). The Staphylococcus aureus lrgAB operon modulates murein hydrolase activity and penicillin tolerance. J Bacteriol 182:1794–801
   PubMed Web of Science ®Google Scholar
• Groisman EA. (2001). The pleiotropic two-component regulatory system PhoP-PhoQ. J Bacteriol 183:1835–42
   PubMed Web of Science ®Google Scholar
• Hall-Stoodley L, Nistico L, Sambanthamoorthy K, et al. (2008). Characterization of biofilm matrix, degradation by DNase treatment and evidence of capsule downregulation in Streptococcus pneumoniae clinical isolates. BMC Microbiol 8:173
   PubMed Web of Science ®Google Scholar
• Hamilton HL, Domínguez NM, Schwartz KJ, et al. (2005). Neisseria gonorrhoeae secretes chromosomal DNA via a novel type IV secretion system. Mol Microbiol 55:1704–21
   PubMedGoogle Scholar
• Hara T, Ueda S. (1981). A study on the mechanism of DNA excretion from P. aeruginosa KYU-1 – effect of mitomycin C on extracellular DNA production. Agr Biol Chem Tokyo 45:2457–61
   Web of Science ®Google Scholar
• Harmsen M, Lappann M, Knøchel S, Molin S. (2010). Role of extracellular DNA during biofilm formation by Listeria monocytogenes. Appl Environ Microbiol 76:2271–9
   PubMed Web of Science ®Google Scholar
• Heijstra B, Pichler F, Liang Q, et al. (2009). Extracellular DNA and Type IV pili mediate surface attachment by Acidovorax temperans. Anton Leeuw 95:343–9
   PubMedGoogle Scholar
• Heilmann C, Hussain M, Peters G, Götz F. (2003). Evidence for autolysin-mediated primary attachment of Staphylococcus epidermidis to a polystyrene surface. Mol Microbiol 24:1013–24
   Google Scholar
• Hemmi H, Akira S. (2002). Microbial DNA and host immunity. NJ: Humana Press, 39–47
   Google Scholar
• Hermansson M. (1999). The DLVO theory in microbial adhesion. Collid Surf B 14:105–19
   Web of Science ®Google Scholar
• Heurlier K, Dénervaud V, Haenni M, et al. (2005). Quorum-sensing-negative (lasR) mutants of Pseudomonas aeruginosa avoid cell lysis and death. J Bacteriol 187:4875–83
   PubMed Web of Science ®Google Scholar
• Hu W, Li L, Sharma S, et al. (2012). DNAbBuilds and strengthens the extracellular matrix in Myxococcus xanthus biofilms by interacting with exopolysaccharides. PLoS ONE 7:e51905
   Google Scholar
• Hunter KA, Liss PS. (1982). Organic matter and the surface charge of suspended particles in estuarine waters. Limnol Oceanogr 27:322–35
   Web of Science ®Google Scholar
• Huseby MJ, Kruse AC, Digre J, et al. (2010). Beta toxin catalyzes formation of nucleoprotein matrix in staphylococcal biofilms. PNAS 107:14407–12
   PubMed Web of Science ®Google Scholar
• Håvarstein LS, Martin B, Johnsborg O, et al. (2006). New insights into the pneumococcal fratricide: relationship to clumping and identification of a novel immunity factor. Mol Microbiol 59:1297–307
   PubMed Web of Science ®Google Scholar
• Inoue T, Shingaki R, Sogawa N, et al. (2003). Biofilm formation by a fimbriae/deficient mutant of Actinobacillus actinomycetemcomitans. Microbiol Immunol 47:877--81
   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 74:470–6
   PubMed Web of Science ®Google Scholar
• Izano EA, Shah SM, Kaplan JB. (2009). Intercellular adhesion and biocide resistance in nontypeable Haemophilus influenzae biofilms. Microb Pathog 46:207–13
   PubMed Web of Science ®Google Scholar
• Johnson L, Mulcahy H, Kanevets U, et al. (2012). Surface-localized spermidine protects the Pseudomonas aeruginosa outer membrane from antibiotic treatment and oxidative stress. J Bacteriol 194:813–26
   PubMed Web of Science ®Google Scholar
• Jones E, McGillivary G, Bakaletz L. (2012). Extracellular DNA within a nontypeable Haemophilus influenzae-induced biofilm binds human beta defensin-3 and reduces its antimicrobial activity. J Innate Immun 5:24--38
   PubMedGoogle Scholar
• Jucker BA, Harms H, Zehnder AJ. (1996). Adhesion of the positively charged bacterium Stenotrophomonas (Xanthomonas) maltophilia 70401 to glass and Teflon. J Bacteriol 178:5472–9
   PubMed Web of Science ®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 178:2767–74
   PubMed Web of Science ®Google Scholar
• Kaneko S, Itaya M. (2010). Extracellular nucleic acids, Vol. 25. Berlin Heidelberg: Springer, 39–53
   Google Scholar
• Kaplan J. (2009). Therapeutic potential of biofilm-dispersing enzymes. Int J Artif Organs 32:545–54
   PubMed Web of Science ®Google Scholar
• Kaplan JB. (2010). Biofilm dispersal: mechanisms, clinical Implications, and potential therapeutic uses. J Dent Res 89:205–18
   PubMed Web of Science ®Google Scholar
• Kausmally L, Johnsborg O, Lunde M, et al. (2005). Choline-binding protein D (CbpD) in Streptococcus pneumoniae is essential for competence-induced cell lysis. J Bacteriol 187:4338–45
   PubMedGoogle Scholar
• Klemm P, Vejborg R, Hancock V. (2010). Prevention of bacterial adhesion. Appl Microbiol Biotechnol 88:451–9
   PubMed Web of Science ®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 190:4632–40
   PubMed Web of Science ®Google Scholar
• Lappann M, Claus H, Van Alen T, et al. (2010). A dual role of extracellular DNA during biofilm formation of Neisseria meningitidis. Mol Microbiol 75:1355--71
   Google Scholar
• Lethem M, James S, Marriott C, Burke J. (1990). The origin of DNA associated with mucus glycoproteins in cystic fibrosis sputum. Eur Respir J 3:19–23
   PubMed Web of Science ®Google Scholar
• Li Y-H, Tang N, Aspiras MB, et al. (2002). A quorum-sensing signaling system essential for genetic competence in Streptococcus mutans is involved in biofilm formation. J Bacteriol 184:2699–708
   PubMed Web of Science ®Google Scholar
• Liu H, Wang L, Xie Z, Shen P. (2012). Involvement of DNA in biofilm formation II: from bacterial adhesion to biofilm formation. J Nat Sci Wuhan 17:162–8
   Google Scholar
• Liu H-H, Yang Y-R, Shen X-C, et al. (2008). Role of DNA in bacterial aggregation. Curr Microbiol 57:139–44
   PubMedGoogle Scholar
• Loo CY, Corliss DA, Ganeshkumar N. (2000). Streptococcus gordonii biofilm formation: identification of genes that code for biofilm phenotypes. J Bacteriol 182:1374–82
   PubMed Web of Science ®Google Scholar
• Lorenz M, Wackernagel W. (1994). Bacterial gene transfer by natural genetic transformation in the environment. Microbiol Rev 58:563–602
   PubMedGoogle Scholar
• Lorenz MG, Gerjets D, Wackernagel W. (1991). Release of transforming plasmid and chromosomal DNA from two cultured soil bacteria. Arch Microbiol 156:319–26
   PubMed Web of Science ®Google Scholar
• Mann EE, Rice KC, Boles BR, et al. (2009). Modulation of eDNA release and degradation affects Staphylococcus aureus biofilm maturation. PLoS ONE 4:e5822
   PubMed Web of Science ®Google Scholar
• Marshall KC, Stout R, Mitchell R. (1971). Mechanism of the initial events in the sorption of marine bacteria to surfaces. J Gen Microbiol 68:337–48
   Google Scholar
• Matsukawa M, Greenberg EP. (2004). Putative exopolysaccharide synthesis genes Influence Pseudomonas aeruginosa biofilm development. J Bacteriol 186:4449–56
   PubMed Web of Science ®Google Scholar
• Mitik-Dineva N, Wang J, Stoddart PR, et al. (2008). International Conference on Nanoscience and Nanotechnology, Australia, 2008, 113–16
   Google Scholar
• Molin S, Tolker-Nielsen T. (2003). Gene transfer occurs with enhanced efficiency in biofilms and induces enhanced stabilisation of the biofilm structure. Curr Opin Biotechnol 14:255–61
   PubMed Web of Science ®Google Scholar
• Moscoso M, Claverys J-P. (2004). Release of DNA into the medium by competent Streptococcus pneumoniae: kinetics, mechanism and stability of the liberated DNA. Mol Microbiol 54:783–94
   PubMedGoogle Scholar
• Moscoso M, García E, López R. (2006). Biofilm formation by Streptococcus pneumoniae: role of choline, extracellular DNA, and capsular polysaccharide in microbial accretion. J Bacteriol 188:7785–95
   PubMed Web of Science ®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:e1000213
   PubMedGoogle Scholar
• Muto Y, Goto S. (1986). Transformation by extracellular DNA produced by Pseudomonas aeruginosa. Microbiol Immunol 30:621–8
   PubMedGoogle Scholar
• Nakamura Y, Itoh T, Matsuda H, Gojobori T. (2004). Biased biological functions of horizontally transferred genes in prokaryotic genomes. Nat Genet 36:760–6
   PubMed Web of Science ®Google Scholar
• Nijland R, Hall MJ, Burgess JG. (2010). Dispersal of biofilms by secreted, matrix degrading, bacterial DNase. PLoS ONE 5:e15668
   PubMed Web of Science ®Google Scholar
• Oshida T, Sugai M, Komatsuzawa H, et al. (1995). A Staphylococcus aureus autolysin that has an N-acetylmuramoyl-L-alanine amidase domain and an endo-beta-N-acetylglucosaminidase domain: cloning, sequence analysis, and characterization. PNAS 92:285–9
   PubMed Web of Science ®Google Scholar
• Palmen R, Hellingwerf KJ. (1995). Acinetobacter calcoaceticus liberates chromosomal DNA during induction of competence by cell lysis. Curr Microbiol 30:7–10
   PubMedGoogle Scholar
• Petersen FC, Pecharki D, Scheie AA. (2004). Biofilm mode of growth of Streptococcus intermedius favored by a competence-stimulating signaling peptide. J Bacteriol 186:6327–31
   PubMed Web of Science ®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 187:4392–400
   PubMedGoogle Scholar
• Pietrocola G, Arciola CR, Rindi S, et al. (2011). Toll-like receptors (TLRs) in innate immune defense against Staphylococcus aureus. Int J Artif Organ 34:799–810
   PubMedGoogle Scholar
• Qin Z, Ou Y, Yang L, et al. (2007). Role of autolysin-mediated DNA release in biofilm formation of Staphylococcus epidermidis. Microbiology 153:2083–92
   PubMed Web of Science ®Google Scholar
• Ranjit DK, Endres JL, Bayles KW. (2011). Staphylococcus aureus CidA and LrgA proteins exhibit holin-like properties. J Bacteriol 193:2468–76
   PubMed Web of Science ®Google Scholar
• Regev-Yochay G, TrzciÅski K, Thompson CM, et al. (2006). Interference between Streptococcus pneumoniae and Staphylococcus aureus: in vitro hydrogen peroxide-mediated killing by Streptococcus pneumoniae. J Bacteriol 188:4996–5001
   PubMed Web of Science ®Google Scholar
• Rice KC, Bayles KW. (2003). Death’s toolbox: examining the molecular components of bacterial programmed cell death. Mol Microbiol 50:729–38
   PubMed Web of Science ®Google Scholar
• Rice KC, Bayles KW. (2008). Molecular control of bacterial death and lysis. Microbiol Mol Biol R 72:85–109
   PubMed Web of Science ®Google Scholar
• Rice KC, Mann EE, Endres JL, et al. (2007). The cidA murein hydrolase regulator contributes to DNA release and biofilm development in Staphylococcus aureus. PNAS 104:8113–8
   PubMed Web of Science ®Google Scholar
• Rijnaarts HHM, Norde W, Bouwer EJ, et al. (1995). Reversibility and mechanism of bacterial adhesion. Collid Surface B 4:5–22
   Google Scholar
• Roberts AP, Pratten J, Wilson M, Mullany P. (2006). Transfer of a conjugative transposon, Tn5397 in a model oral biofilm. FEMS Microbiol Lett 177:63–6
   Google Scholar
• Sahu PK, Iyer PS, Oak AM, et al. (2012). Characterization of eDNA from the clinical strain Acinetobacter baumannii AIIMS 7 and its role in biofilm formation. Sci World J 2012:10
   Google Scholar
• Salgado-Pabón W, Du Y, Hackett KT, et al. (2010). Increased expression of the type IV secretion system in piliated Neisseria gonorrhoeae variants. J Bacteriol 192:1912–20
   PubMed Web of Science ®Google Scholar
• Sanchez-Torres V, Maeda T, Wood TK. (2010). Global regulator H-NS and lipoprotein NlpI influence production of extracellular DNA in Escherichia coli. Biochem Biophys Res Commun 401:197–202
   PubMed Web of Science ®Google Scholar
• Schooling SR, Hubley A, Beveridge TJ. (2009). Interactions of DNA with biofilm-derived membrane vesicles. J Bacteriol 191:4097–102
   PubMedGoogle Scholar
• Seper A, Fengler VHI, Roier S, et al. (2011). Extracellular nucleases and extracellular DNA play important roles in Vibrio cholerae biofilm formation. Mol Microbiol 82:1015–37
   PubMed Web of Science ®Google Scholar
• Shak S, Capon DJ, Hellmiss R, et al. (1990). Recombinant human DNase I reduces the viscosity of cystic fibrosis sputum. PNAS 87:9188–92
   PubMed Web of Science ®Google Scholar
• Spoering A, Gilmore M. (2006). Quorum sensing and DNA release in bacterial biofilms. Curr Opin Microbiol 9:133–7
   PubMed Web of Science ®Google Scholar
• Springael D, Peys K, Ryngaert A, et al. (2002). Community shifts in a seeded 3-chlorobenzoate degrading membrane biofilm reactor: indications for involvement of in situ horizontal transfer of the clc-element from inoculum to contaminant bacteria. Environ Microbiol 4:70–80
   PubMed Web of Science ®Google Scholar
• Steinberger RE, Holden PA. (2005). Extracellular DNA in single- and multiple-species unsaturated biofilms. Appl Environ Microbiol 71:5404–10
   PubMed Web of Science ®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. PNAS 99:7681–6
   PubMed Web of Science ®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 185:7176–83
   PubMedGoogle Scholar
• Stewart GJ, Carlson CA, Ingraham JL. (1983). Evidence for an active role of donor cells in natural transformation of Pseudomonas stutzeri. J Bacteriol 156:30–5
   PubMedGoogle Scholar
• Streips UN, Young FE. (1974). Transformation in Bacillus subtilis using excreted DNA. Mol Gen Genet 133:47–55
   PubMedGoogle Scholar
• Sykes R. (2010). The 2009 Garrod Lecture: the evolution of antimicrobial resistance: a Darwinian perspective. J Antimicrob Chemother 65:1842–52
   PubMed Web of Science ®Google Scholar
• Tang L, Schramm A, Neu TR, et al. (in press). Extracellular DNA in adhesion and biofilm formation of four environmental isolates: a quantitative study. FEMS Microbiol Ecol. DOI: 10.1111/1574-6941.12168
   Google Scholar
• Tetz GV, Artemenko NK, Tetz VV. (2009). Effect of DNase and antibiotics onbiofilm characteristics. Antimicrob Agents Chemother 53:1204–9
   PubMed Web of Science ®Google Scholar
• Thomas CM, Nielsen KM. (2005). Mechanisms of, and barriers to, horizontal gene transfer between bacteria. Nat Rev Microbiol 3:711–21
   PubMed Web of Science ®Google Scholar
• Thomas V, Hancock L. (2009). Suicide and fratricide in bacterial biofilms. Int J Artif Organ 32:537–44
   PubMedGoogle Scholar
• Thomas VC, Hiromasa Y, Harms N, et al. (2009). A fratricidal mechanism is responsible for eDNA release and contributes to biofilm development of Enterococcus faecalis. Mol Microbiol 72:1022–36
   PubMed Web of Science ®Google Scholar
• Thomas VC, Thurlow LR, Boyle D, Hancock LE. (2008). Regulation of autolysis-dependent extracellular DNA release by Enterococcus faecalis extracellular proteases influences biofilm development. J Bacteriol 190:5690–8
   PubMed Web of Science ®Google Scholar
• Thurlow LR, Hanke ML, Fritz T, et al. (2011). Staphylococcus aureus biofilms prevent macrophage phagocytosis and attenuate inflammation in vivo. J Immunol 186:6585–96
   PubMed Web of Science ®Google Scholar
• van Loosdrecht MCM, Lyklema J, Norde W, Zehnder AJB. (1989). Bacterial adhesion: a physicochemical approach. Microb Ecol 17:1–15
   PubMed Web of Science ®Google Scholar
• van Oss CJ. (1995). Hydrophobicity of biosurfaces – origin, quantitative determination and interaction energies. Collid Surf B 5:91–110
   Web of Science ®Google Scholar
• Van Schaik EJ, Giltner CL, Audette GF, et al. (2005). DNA binding: a novel function of Pseudomonas aeruginosa type IV pili. J Bacteriol 187:1455–64
   PubMedGoogle Scholar
• Véscovi EG, Ayala YM, Di Cera E, Groisman EA. (1997). Characterization of the bacterial sensor protein PhoQ: evidence for distinct bindingsites for Mg2+ and Ca2+. J Biol Chem 272:1440–3
   PubMed Web of Science ®Google Scholar
• Vijayalakshmi S, Hancock L. (2012). Deletion of σ54 (rpoN) alters the rate of autolysis and biofilm formation in Enterococcus faecalis. J Bacteriol 194:368–75
   PubMedGoogle Scholar
• Vilain S, Pretorius JM, Theron J, Brözel VS. (2009). DNA as an adhesin: Bacillus cereus requires extracellular DNA to form biofilms. Appl Environ Microbiol 75:2861–8
   PubMed Web of Science ®Google Scholar
• Walker TS, Tomlin KL, Worthen GS, et al. (2005). Enhanced Pseudomonas aeruginosa biofilm development mediated by human neutrophils. Infect Immun 73:3693–701
   PubMed Web of Science ®Google Scholar
• Watanabe M, Sasaki K, Nakashimada Y, et al. (1998). Growth and flocculation of a marine photosynthetic bacterium Rhodovulum sp. Appl Microbiol Biotechnol 50:682–91
   Web of Science ®Google Scholar
• Watson Robert O, Manzanillo Paolo S, Cox Jeffery S. (2012). Extracellular M. tuberculosis DNA targets bacteria for autophagy by activating the host DNA-sensing pathway. Cell 150:803–15
   PubMedGoogle Scholar
• Webb JS, Thompson LS, James S, et al. (2003). Cell death in Pseudomonas aeruginosa biofilm development. J Bacteriol 185:4585–92
   PubMed Web of Science ®Google Scholar
• Weiss L, Harlos JP. (1972). Short-term interactions between cell surfaces. Prog Surf Sci 1:355–405
   Google Scholar
• Whitchurch CB, Tolker-Nielsen T, Ragas PC, Mattick JS. (2002). Extracellular DNA required for bacterial biofilm formation. Science 295:1487
   PubMed Web of Science ®Google Scholar
• Xiong Y, Liu Y. (2010). Biological control of microbial attachment: a promising alternative for mitigating membrane biofouling. Appl Microbiol Biotechnol 86:825–37
   PubMed Web of Science ®Google Scholar
• Yokoi K, Sugahara K, Iguchi A, et al. (2008). Molecular properties of the putative autolysin Atl encoded by Staphylococcus warneri: mutational and biochemical analyses of the amidase and glucosaminidase domains. Gene 416:66–76
   PubMedGoogle Scholar
• Yoshida A, Kuramitsu HK. (2002). Multiple Streptococcus mutans genes are involved in biofilm formation. Appl Environ Microbiol 68:6283–91
   PubMed Web of Science ®Google Scholar
• Zafra O, Lamprecht-Grandío M, de Figueras CG, González-Pastor JE. (2012). Extracellular DNA release by undomesticated Bacillus subtilis is regulated by early competence. PLoS ONE 7:e48716
   PubMed Web of Science ®Google Scholar
• Zhao J, Wang Q, Li M, et al. (2013). Escherichia coli toxin gene hipA affects biofilm formation and DNA release. Microbiology 159:633–40
   PubMedGoogle Scholar
• Zheng L, Chen Z, Itzek A, et al. (2011). Catabolite control protein a controls hydrogen peroxide production and cell death in Streptococcus sanguinis. J Bacteriol 193:516–26
   Web of Science ®Google Scholar
• Zobell C. (1943). The effect of solid surfaces upon bacterial activity. J Bacteriol 46:39–56
   PubMedGoogle Scholar