Like all sessile organisms, surface-attached communities of bacteria known as biofilms must release and disperse cells into the environment to colonize new sites. For many pathogenic bacteria, biofilm dispersal plays an important role in the transmission of bacteria from environmental reservoirs to human hosts, in horizontal and vertical cross-host transmission, and in the exacerbation and spread of infection within a host. The molecular mechanisms of bacterial biofilm dispersal are only beginning to be elucidated. Biofilm dispersal is a promising area of research that may lead to the development of novel agents that inhibit biofilm formation or promote biofilm cell detachment. Such agents may be useful for the prevention and treatment of biofilms in a variety of industrial and clinical settings. This review describes the current status of research on biofilm dispersal, with an emphasis on studies aimed to characterize dispersal mechanisms, and to identify environmental cues and inter- and intracellular signals that regulate the dispersal process. The clinical implications of biofilm dispersal and the potential therapeutic applications of some of the most recent findings will also be discussed.
Get full access to this article
View all access options for this article.
References
1.
Adair CG, Gorman SP, Feron BM, Byers LM, Jones DS, Goldsmith CE, et al. (1999). Implications of endotracheal tube biofilm for ventilator-associated pneumonia. Intensive Care Med25:1072–1076.
2.
Alipour M, Suntres ZE, Omri A (2009). Importance of DNase and alginate lyase for enhancing free and liposome encapsulated aminoglycoside activity against Pseudomonas aeruginosa. J Antimicrob Chemother64:317–325.
3.
Alkawash MA, Soothill JS, Schiller NL (2006). Alginate lyase enhances antibiotic killing of mucoid Pseudomonas aeruginosa in biofilms. APMIS114:131–138.
4.
Allesen-Holm M, Barken KB, Yang L, Klausen M, Webb JS, Kjelleberg S, et al. (2006). A characterization of DNA release in Pseudomonas aeruginosa cultures and biofilms. Mol Microbiol59:1114–1128.
5.
Allison DG, Evans DJ, Brown MRW, Gilbert P (1990). Possible involvement of the division cycle in dispersal of Escherichia coli from biofilms. J Bacteriol172:1667–1669.
6.
Allison DG, Ruiz B, SanJose C, Jaspe A, Gilbert P (1998). Extracellular products as mediators of the formation and detachment of Pseudomonas fluorescens biofilms. FEMS Microbiol Lett167:179–184.
7.
Applegate DH, Bryers JD (1991). Effects of carbon and oxygen limitations and calcium concentrations on biofilm removal process. Biotechnol Bioeng37:17–25.
8.
Banas JA, Vickerman MM (2003). Glucan-binding proteins of the oral streptococci. Crit Rev Oral Biol Med14:89–99.
9.
Barraud N, Hassett DJ, Hwang SH, Rice SA, Kjelleberg S, Webb JS (2006). Involvement of nitric oxide in biofilm dispersal of Pseudomonas aeruginosa. J Bacteriol188:7344–7353.
10.
Baty AM 3rd, Eastburn CC, Techkarnjanaruk S, Goodman AE, Geesey GG (2000). Spatial and temporal variations in chitinolytic gene expression and bacterial biomass production during chitin degradation. Appl Environ Microbiol66:3574–3585.
11.
Bayer AS, Park S, Ramos MC, Nast CC, Eftikhar F, Schiller NL (1992). Effect of alginase on the natural history and antibiotic therapy of experimental endocarditis caused by mucoid Pseudomonas aeruginosa. Infect Immun60:3979–3985.
12.
Bayles KW (2007). The biological role of death and lysis in biofilm development. Nature Rev Microbiol5:721–726.
13.
Berkowitz RJ, Jones P (1985). Mouth-to-mouth transmission of the bacterium Streptococcus mutans between mother and child. Arch Oral Biol30:377–379.
14.
Bieber D, Ramer SW, Wu C-Y, Murray WJ, Tobe T, Fernandez R, et al. (1998). Type IV pili, transient bacterial aggregates, and virulence of enteropathogenic Escherichia coli. Science280:2114–2118.
15.
Boehm A, Steiner S, Zaehringer F, Casanova A, Hamburger F, Ritz D, et al. (2009). Second messenger signaling governs Escherichia coli biofilm induction upon ribosomal stress. Mol Microbiol72:1500–1516.
16.
Boles BR, Horswill AR (2008). Agr-mediated dispersal of Staphylococcus aureus biofilms. PLoS Pathog4:e1000052.
17.
Boles BR, Thoendel M, Singh PK (2005). Rhamnolipids mediate detachment of Pseudomonas aeruginosa from biofilms. Mol Microbiol57:1210–1223.
18.
Boyd A, Chakrabarty AM (1994). Role of alginate lyase in cell detachment of Pseudomonas aeruginosa. Appl Environ Microbiol60:2355–2359.
19.
Brennan PJ, Aspinall GO, Shin JE (1981). Structure of the specific oligosac-charides from the glycopeptidolipid antigens of serovars in the Mycobacterium avium-Mycobacterium intracellulare-Mycobacterium scrofulaceum complex. J Biol Chem256:6817–6822.
20.
Chiang P, Burrows LL (2003). Biofilm formation by hyperpiliated mutants of Pseudomonas aeruginosa. J Bacteriol185:2374–2378.
21.
Choi YC, Morgenroth E (2003). Monitoring biofilm detachment under dynamic changes in shear stress using laser-based particle size analysis and mass fractionation. Water Sci Technol47:69–76.
22.
Cleary J, Lai LC, Shaw RK, Straatman-Iwanowska A, Donnenberg MS, Frankel G, et al. (2004). Enteropathogenic Escherichia coli (EPEC) adhesion to intestinal epithelial cells: role of bundle-forming pili (BFP), EspA filaments and intimin. Microbiology150(Pt 3):527–538.
23.
Costerton JW, Stewart PS, Greenberg EP (1999). Bacterial biofilms: a common cause of persistent infections. Science284:1318–1322.
24.
Darouiche RO, Mansouri MD, Gawande PV, Madhyastha S. (2009). Antimicrobial and antibiofilm efficacy of triclosan and DispersinB® combination. J Antimicrob Chemother64:88–93.
25.
Davey ME, Caiazza NC, O’Toole GA (2003). Rhamnolipid surfactant production affects biofilm architecture in Pseudomonas aeruginosa PAO1. J Bacteriol185:1027–1036.
26.
Davies DG, Marques CN (2009). A fatty acid messenger is responsible for inducing dispersion in microbial biofilms. J Bacteriol191:1393–1403.
27.
Delaquis PJ, Caldwell DE, Lawrence JR, McCurdy AR (1989). Detachment of Pseudomonas fluorescens from biofilms on glass surfaces in response to nutrient stress. Microb Ecol18:199–210.
28.
Dong YH, Zhang XF, An SW, Xu JL, Zhang LH (2008). A novel two-component system BqsS-BqsR modulates quorum sensing-dependent biofilm decay in Pseudomonas aeruginosa. Commun Integr Biol1:88–96.
29.
Dow JM, Crossman L, Findlay K, He YQ, Feng JX, Tang JL (2003). Biofilm dispersal in Xanthomonas campestris is controlled by cell-cell signalling and is required for full virulence in plants. Proc Natl Acad Sci USA100:10995–11000.
30.
Erard JC, Miyasaki KT, Wolinsky LE (1989). Detachment of oral bacteria from saliva-coated hydroxyapatite by polymorphonuclear leukocytes. J Periodontol60:211–216.
31.
Finkelstein RA, Boesman-Finkelstein M, Chang Y, Häse CC (1992). Vibrio cholerae hemagglutinin/protease, colonial variation, virulence, and detachment. Infect Immun60:472–478.
32.
Foca M, Jakob K, Whittier S, Latta PD, Factor S, Rubenstein D, et al. (2000). Endemic Pseudomonas aeruginosa infection in a neonatal intensive care unit. New Engl J Med343:695–700.
33.
Frank KL, Patel R (2007). Poly-N-acetylglucosamine is not a major component of the extracellular matrix in biofilms formed by icaADBC-positive Staphylococcus lugdunensis isolates. Infect Immun75:4728–4742.
34.
Freeman R, Geier H, Weigel KM, Do J, Ford TE, Cangelosi GA (2006). Roles for cell wall glycopeptidolipids in surface adherence and planktonic dispersal of Mycobacterium avium. Appl Environ Microbiol72:7554–7558.
35.
Fuqua C, Greenberg EP (2002). Listening in on bacteria: acyl-homoserine lactone signalling. Nat Rev Mol Cell Biol3:685–695.
36.
Fux CA, Wilson S, Stoodley P (2004). Detachment characteristics and oxacillin resistance of Staphylococcus aureus biofilm emboli in an in vitro catheter infection model. J Bacteriol186:4486–4491.
37.
Gilbert P, Allison DG, Evans DJ, Handley PS, Brown MR (1989). Growth rate control of adherent bacterial populations. Appl Environ Microbiol55:1308–1311.
38.
Gilbert P, Evans DJ, Brown MR (1993). Formation and dispersal of biofilms in vivo and in situ. J Appl Bacteriol74(Suppl):67S–78S.
39.
Gjermansen M, Ragas P, Sternberg C, Molin S, Tolker-Nielsen T (2005). Characterization of starvation-induced dispersion in Pseudomonas putida biofilms. Environ Microbiol7:894–906.
40.
Gjermansen M, Ragas P, Tolker-Nielsen T (2006). Proteins with GGDEF and EAL domains regulate Pseudomonas putida biofilm formation and dispersal. FEMS Microbiol Lett265:215–224.
41.
Gjermansen M, Nilsson M, Yang L, Tolker-Nielsen T (2009). Characterization of starvation-induced dispersion in Pseudomonas putida biofilms: genetic elements and molecular mechanisms. Mol Microbiol (in press). doi:10.1111/j.1365-2958.2009.06793.x
42.
Hall-Stoodley L, Stoodley P (2005). Biofilm formation and dispersal and the transmission of human pathogens. Trends Microbiol13:7–10; erratum in Trends Microbiol 13:300–301, 2005.
43.
Hall-Stoodley L, Costerton JW, Stoodley P (2004). Bacterial biofilms: from the natural environment to infectious diseases. Nature Rev Microbiol2:95–108.
44.
Hammer BK, Bassler BL (2003). Quorum sensing controls biofilm formation in Vibrio cholerae. Mol Microbiol50:101–114.
45.
Helmstetter CE, Cummings DJ (1964). An improved method for the selection of bacterial cells at division. Biochim Biophys Acta82:608–610.
46.
Hentzer M, Riedel K, Rasmussen TB, Heydorn A, Andersen JB, Parsek MR, et al. (2002). Inhibition of quorum sensing in Pseudomonas aeruginosa biofilm bacteria by a halogenated furanone compound. Microbiology148(Pt 1):87–102.
47.
Hunt SM, Werner EM, Huang B, Hamilton MA, Stewart PS (2004). Hypothesis for the role of nutrient starvation in biofilm detachment. Appl Environ Microbiol70:7418–7425.
48.
Inoue T, Shingaki R, Sogawa N, Sogawa CA, Asaumi J, Kokeguchi S, et al. (2003). Biofilm formation by a fimbriae-deficient mutant of Actinobacillus actinomycetemcomitans. Microbiol Immunol47:877–881.
49.
Irie Y, Parsek MR (2008). Quorum sensing and microbial biofilms. Curr Top Microbiol Immunol322:67–84.
50.
Irie Y, O’Toole GA, Yuk MH (2005). Pseudomonas aeruginosa rhamnolipids disperse Bordetella bronchiseptica biofilms. FEMS Microbiol Lett250:237–243.
51.
Itoh Y, Wang X, Hinnebusch BJ, Preston JF 3rd, Romeo T (2005). Depolymerization of β-1,6-N-acetyl-D-glucosamine disrupts the integrity of diverse bacterial biofilms. J Bacteriol187:382–387.
52.
Izano EA, Wang H, Ragunath C, Ramasubbu N, Kaplan JB (2007). Detachment and killing of Aggregatibacter actinomycetemcomitans biofilms by dispersin B and SDS. J Dent Res86:618–622.
53.
Izano EA, Amarante MA, Kher WB, Kaplan JB (2008a). Differential roles of poly-N-acetylglucosamine surface polysaccharide and extracellular DNA in Staphylococcus aureus and Staphylococcus epidermidis biofilms. Appl Environ Microbiol74:470–476.
54.
Izano EA, Sadovskaya I, Wang H, Vinogradov E, Ragunath C, Ramasubbu N, et al. (2008b). Poly-N-acetylglucosamine mediates biofilm formation and detergent resistance in Aggregatibacter actinomycetemcomitans. Microb Pathogen44:52–60.
55.
Jackson DW, Suzuki K, Oakford L, Simecka JW, Hart ME, Romeo T (2002). Biofilm formation and dispersal under the influence of the global regulator CsrA of Escherichia coli. J Bacteriol184:290–301.
56.
James GA, Korber DR, Caldwell DE, Costerton JW (1995). Digital image analysis of growth and starvation responses of a surface-colonizing Acinetobacter sp. J Bacteriol177:907–915.
57.
Ji G, Beavis R, Novick RP (1997). Bacterial interference caused by autoinducing peptide variants. Science276:2027–2030.
58.
Kachlany SC, Planet PJ, Desalle R, Fine DH, Figurski DH, Kaplan JB (2001). flp-1, the first representative of a new pilin gene subfamily, is required for non-specific adherence of Actinobacillus actinomycetemcomitans. Mol Microbiol40:542–554.
59.
Kaplan JB, Fine DH (2002). Biofilm dispersal of Neisseria subflava and other phylogenetically diverse oral bacteria. Appl Environ Microbiol68:4943–4950.
60.
Kaplan JB, Meyenhofer MF, Fine DH (2003a). Biofilm growth and detachment of Actinobacillus actinomycetemcomitans. J Bacteriol185:1399–1404.
61.
Kaplan JB, Ragunath C, Ramasubbu N, Fine DH (2003b). Detachment of Actinobacillus actinomycetemcomitans biofilm cells by an endogenous β-hexosaminidase activity. J Bacteriol185:4692–4698.
62.
Kaplan JB, Velliyagounder K, Ragunath C, Fine DH, Ramasubbu N (2004a). Enzymatic detachment of Staphylococcus epidermidis biofilms. Antimicrob Agents Chemother48:2633–2636.
63.
Kaplan JB, Velliyagounder K, Ragunath C, Rohde H, Mack D, Knobloch JK, et al. (2004b). Genes involved in the synthesis and degradation of matrix polysaccharide in Actinobacillus actinomycetemcomitans and Actinobacillus pleuropneumoniae biofilms. J Bacteriol186:8213–8220.
64.
Karatan E, Watnick P (2009). Signals, regulatory networks, and materials that build and break bacterial biofilms. Microbiol Molec Biol Rev73:310–347.
65.
Kinane DF, Riggio MP, Walker KF, MacKenzie D, Shearer B (2005). Bacteraemia following periodontal procedures. J Clin Periodontol32:708–713.
66.
Kirov SM, Webb JS, O’May CY, Reid DW, Woo JK, Rice SA, et al. (2007). Biofilm differentiation and dispersal in mucoid Pseudomonas aeruginosa isolates from patients with cystic fibrosis. Microbiology153(Pt 10):3264–3274.
67.
Klausen M, Gjermansen M, Kreft JU, Tolker-Nielsen T (2006). Dynamics of development and dispersal in sessile microbial communities: examples from Pseudomonas aeruginosa and Pseudomonas putida model biofilms. FEMS Microbiol Lett261:1–11.
68.
Knutton S, Shaw RK, Anantha RP, Donnenberg MS, Zorgani AA (1999). The type IV bundle-forming pilus of enteropathogenic Escherichia coli undergoes dramatic alterations in structure associated with bacterial adherence, aggregation and dispersal. Mol Microbiol33:499–509.
69.
Koh KS, Lam KW, Alhede M, Queck SY, Labbate M, Kjelleberg S, et al. (2007). Phenotypic diversification and adaptation of Serratia marcescens MG1 biofilm-derived morphotypes. J Bacteriol189:119–130.
70.
Lamont RJ, El-Sabaeny A, Park Y, Cook GS, Costerton JW, Demuth DR (2002). Role of the Streptococcus gordonii SspB protein in the development of Porphyromonas gingivalis biofilms on streptococcal substrates. Microbiology148:1627–1636.
71.
Lappin-Scott HM, Bass C (2001). Biofilm formation: attachment, growth, and detachment of microbes from surfaces. Am J Infect Control29:250–251.
72.
Lauderdale KJ, Malone CL, Boles BR, Morcuende J, Horswill AR (2009). Biofilm dispersal of community-associated methicillin-resistant Staphylococcus aureus on orthopedic implant material. J Orthop Res28:55–61.
Lawrence JR, Scharf B, Packroff G, Neu TR (2002). Microscale evaluation of the effects of grazing by invertebrates with contrasting feeding modes on river biofilm architecture and composition. Microb Ecol44:199–207.
75.
Lee SF, Li YH, Bowden GH (1996). Detachment of Streptococcus mutans biofilm cells by an endogenous enzymatic activity. Infect Immun64:1035–1038.
Lu TK, Collins JJ (2007). Dispersing biofilms with engineered enzymatic bacteriophage. Proc Natl Acad Sci USA104:11197–11202.
78.
Ma L, Conover M, Lu H, Parsek MR, Bayles K, Wozniak DJ (2009). Assembly and development of the Pseudomonas aeruginosa biofilm matrix. PLoS Pathog5:e1000354.
79.
Maddula VS, Pierson EA, Pierson LS 3rd (2008). Altering the ratio of phenazines in Pseudomonas chlororaphis (aureofaciens) strain 30–84 effects on biofilm formation and pathogen inhibition. J Bacteriol190:2759–2766.
80.
Mah TF, O’Toole GA (2001). Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol9:34–39.
81.
Mai-Prochnow A, Evans F, Dalisay-Saludes D, Stelzer S, Egan S, James S, et al. (2004). Biofilm development and cell death in the marine bacterium Pseudoalteromonas tunicata. Appl Environ Microbiol70:3232–3238.
82.
Mai-Prochnow A, Lucas-Elio P, Egan S, Thomas T, Webb JS, Sanchez-Amat A, et al. (2008). Hydrogen peroxide linked to lysine oxidase activity facilitates biofilm differentiation and dispersal in several gram-negative bacteria. J Bacteriol190:5493–5501.
83.
Mann EE, Rice KC, Boles BR, Endres JL, Ranjit D, Chandramohan L, et al. (2009). Modulation of eDNA release and degradation affects Staphylococcus aureus biofilm maturation. PLoS One4:e5822.
84.
Marsh PD (2004). Dental plaque as a microbial biofilm. Caries Res38:204–211.
85.
Marsh PD (2006). Dental plaque as a biofilm and a microbial community— implications for health and disease. BMC Oral Health6(Suppl 1):14.
86.
Marshall KC (1988). Adhesion and growth of bacteria at surfaces in oligotrophic habitats. Can J Microbiol34:503–506.
87.
Mathoera RB, Kok DJ, Nijman RJ (2000). Bladder calculi in augmentation cystoplasty in children. Urology56:482–487.
Morgan R, Kohn S, Hwang SH, Hassett DJ, Sauer K (2006). BdlA, a chemotaxis regulator essential for biofilm dispersion in Pseudomonas aeruginosa. J Bacteriol188:7335–7343.
Mrsny RJ, Lazazzera BA, Daugherty AL, Schiller NL, Patapoff TW (1994). Addition of a bacterial alginate lyase to purulent CF sputum in vitro can result in the disruption of alginate and modification of sputum viscoelasticity. Pulm Pharmacol7:357–366.
92.
Navarro MV, De N, Bae N, Wang Q, Sondermann H (2009). Structural analysis of the GGDEF-EAL domain-containing c-di-GMP receptor FimX. Structure17:1104–1116.
93.
Neu TR (1996). Significance of bacterial surface-active compounds in inter-action of bacteria with interfaces. Microbiol Rev60:151–166.
94.
Newell PD, Monds RD, O’Toole GA (2009). LapD is a bis-(3′,5′)-cyclic dimeric GMP-binding protein that regulates surface attachment by Pseudomonas fluorescens Pf 0-1. Proc Natl Acad Sci USA106:3461–3466.
95.
Nielsen AT, Dolganov NA, Otto G, Miller MC, Wu CY, Schoolnik GK (2008). RpoS controls the Vibrio cholerae mucosal escape response. PLoS Pathog2:e109.
96.
O’Toole GA, Kolter R (1998). Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol30:295–304.
97.
Ott CM, Day DF, Koenig DW, Pierson DL (2001). The release of alginate lyase from growing Pseudomonas syringae pathovar phaseolicola. Curr Microbiol42:78–81.
98.
Pamp SJ, Tolker-Nielsen T (2007). Multiple roles of biosurfactants in structural biofilm development by Pseudomonas aeruginosa. J Bacteriol189:2531–2539.
99.
Parsek MR, Singh PK (2003). Bacterial biofilms: an emerging link to disease pathogenesis. Annu Rev Microbiol57:677–701.
100.
Pecharki D, Petersen FC, Scheie AA (2008). Role of hyaluronidase in Streptococcus intermedius biofilm. Microbiology154(Pt 3):932–938.
101.
Pesci EC, Milbank JB, Pearson JP, McKnight S, Kende AS, Greenberg EP, et al. (1999) Quinolone signaling in the cell-to-cell communication system of Pseudomonas aeruginosa. Proc Natl Acad Sci USA96:11229–11234.
102.
Petersen FC, Pecharki D, Scheie AA (2004). Biofilm mode of growth of Streptococcus intermedius favored by a competence-stimulating signaling peptide. J Bacteriol186:6327–6331.
103.
Petersen FC, Tao L, Scheie AA (2005). DNA binding-uptake system: a link between cell-to-cell communication and biofilm formation. J Bacteriol187:4392–4400.
104.
Preston LA, Wong TY, Bender CL, Schiller NL (2000). Characterization of alginate lyase from Pseudomonas syringae pv. syringae. J Bacteriol182:6268–6271.
105.
Purevdorj-Gage B, Costerton WJ, Stoodley P (2005). Phenotypic differentiation and seeding dispersal in non-mucoid Pseudomonas aeruginosa biofilms. Microbiology151(Pt 5):1569–1576.
106.
Puskas A, Greenberg EP, Kaplan S, Schaefer AL (1997). A quorum-sensing system in the free-living photosynthetic bacterium Rhodobacter sphaeroides. J Bacteriol179:7530–7537.
107.
Rice KC, Mann EE, Endres JL, Weiss EC, Cassat JE, Smeltzer MS, et al. (2007). The cidA murein hydrolase regulator contributes to DNA release and biofilm development in Staphylococcus aureus. Proc Natl Acad Sci USA104:8113–8118.
108.
Rice SA, Koh KS, Queck SY, Labbate M, Lam KW, Kjelleberg S (2005). Biofilm formation and sloughing in Serratia marcescens are controlled by quorum sensing and nutrient cues. J Bacteriol187:3477–3485.
109.
Rice SA, Tan CH, Mikkelsen PJ, Kung V, Woo J, Tay M, et al. (2009). The biofilm life cycle and virulence of Pseudomonas aeruginosa are dependent on a filamentous prophage. ISME J3:271–282.
110.
Romeo T (2006). When the party is over: a signal for dispersal of Pseudomonas aeruginosa biofilms. J Bacteriol188:7325–7327.
Ryan RP, Dow JM (2008). Diffusible signals and interspecies communication in bacteria. Microbiology154(Pt 7):1845–1858.
113.
Sauer K, Camper AK (2001). Characterization of phenotypic changes in Pseudomonas putida in response to surface-associated growth. J Bacteriol183:6579–6589.
114.
Sauer K, Camper AK, Ehrlich GD, Costerton JW, Davies DG (2002). Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm. J Bacteriol184:1140–1154.
115.
Sauer K, Cullen MC, Rickard AH, Zeef LAH, Davies DG, Gilbert P (2004). Characterization of nutrient-induced dispersion in Pseudomonas aeruginosa PAO1 biofilms. J Bacteriol186:7312–7326.
116.
Sawyer LK, Hermanowicz SW (1998). Detachment of biofilm bacteria due to variations in nutrient supply. Wat Sci Tech37:211–214.
117.
Schooling S, Charaf UK, Allison DG, Gilbert P (2004). A role for rhamnolipid in biofilm dispersion. Biofilms1:91–99.
118.
Sheikh J, Czeczulin JR, Harrington S, Hicks S, Henderson IR, Le Bouguénec C, et al. (2002). A novel dispersin protein in enteroaggregative Escherichia coli. J Clin Invest110:1329–1337.
119.
Simm R, Morr M, Kader A, Nimtz M, Römling U (2004). GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility. Mol Microbiol53:1123–1134.
120.
Soberón-Chávez G, Lépine F, Déziel E (2005). Production of rhamnolipids by Pseudomonas aeruginosa. Appl Microbiol Biotechnol68:718–725.
121.
Stabholz A, Mann J, Agmon S, Soskolne WA (1998). The description of a unique population with a very high prevalence of localized juvenile periodontitis. J Clin Periodontol25(11 Pt 1):872–878.
122.
Stanley NR, Lazazzera BA (2004). Environmental signals and regulatory pathways that influence biofilm formation. Mol Microbiol52:917–924.
123.
Stoodley P, Wilson S, Hall-Stoodley L, Boyle JD, Lappin-Scott HM, Costerton JW (2001). Growth and detachment of cell clusters from mature mixed-species biofilms. Appl Environ Microbiol67:5608–5613.
124.
Stoodley P, Sauer K, Davies DG, Costerton JW (2002). Biofilms as complex differentiated communities. Annu Rev Microbiol56:187–209.
125.
Svanberg ML, Loesche WJ (1978). Intraoral spread of Streptococcus mutans in man. Arch Oral Biol23:557–561.
126.
Tam K, Kinsinger N, Ayala P, Qi F, Shi W, Myung NV (2007). Real-time monitoring of Streptococcus mutans biofilm formation using a quartz crystal microbalance. Caries Res41:474–483.
127.
Thormann KM, Saville RM, Shukla S, Spormann AM (2005). Induction of rapid detachment in Shewanella oneidensis MR-1 biofilms. J Bacteriol187:1014–1021.
128.
Thormann KM, Duttler S, Saville RM, Hyodo M, Shukla S, Hayakawa Y, et al. (2006). Control of formation and cellular detachment from Shewanella oneidensis MR-1 biofilms by cyclic di-GMP. J Bacteriol188:2681–2691.
129.
Tolker-Nielsen T, Brinch UC, Ragas PC, Andersen JB, Jacobsen CS, Molin S (2000). Development and dynamics of Pseudomonas sp. biofilms. J Bacteriol182:6482–6489.
130.
VanDevanter DR, Van Dalfsen JM (2005). How much do Pseudomonas biofilms contribute to symptoms of pulmonary exacerbation in cystic fibrosis? Pediatr Pulmonol39:504–506.
131.
Vats N, Lee SF (2000). Active detachment of Streptococcus mutans cells adhered to epon-hydroxylapatite surfaces coated with salivary proteins in vitro. Arch Oral Biol45:305–314.
132.
Velarde JJ, Varney KM, Inman KG, Farfan M, Dudley E, Fletcher J, et al. (2007). Solution structure of the novel dispersin protein of enteroaggregative Escherichia coli. Mol Microbiol66:1123–1135.
133.
Venketaraman V, Lin AK, Le A, Kachlany SC, Connell ND, Kaplan JB (2008). Both leukotoxin and poly-N-acetylglucosamine surface polysaccharide protect Aggregatibacter actinomycetemcomitans biofilm cells from macrophage killing. Microb Pathogen45:173–180.
134.
Vuong C, Saenz HL, Götz F, Otto M (2000). Impact of the agr quorumsensing system on adherence to polystyrene in Staphylococcus aureus. J Infect Dis182:1688–1693.
135.
Vuong C, Gerke C, Somerville GA, Fischer ER, Otto M (2003). Quorumsensing control of biofilm factors in Staphylococcus epidermidis. J Infect Dis188:706–718.
136.
Wang LH, He Y, Gao Y, Wu JE, Dong YH, He C, et al. (2004). A bacterial cell-cell communication signal with cross-kingdom structural analogues. Mol Microbiol51:903–912.
137.
Wassmann P, Chan C, Paul R, Beck A, Heerklotz H, Jenal U, et al. (2007). Structure of BeF3–modified response regulator PleD: implications for diguanylate cyclase activation, catalysis and feedback inhibition. Structure15:915–927.
138.
Webb JS, Thompson LS, James S, Charlton T, Tolker-Nielsen T, Koch B, et al. (2003). Cell death in Pseudomonas aeruginosa biofilm development. J Bacteriol185:4585–4592.
139.
Whiteley M, Bangera MG, Bumgarner RE, Parsek MR, Teitzel GM, Lory S, et al. (2001). Gene expression in Pseudomonas aeruginosa biofilms. Nature413:860–864.
140.
Wilson S, Hamilton MA, Hamilton GC, Schumann MR, Stoodley P (2004). Statistical quantification of detachment rates and size distributions of cell clumps from wild-type (PAO1) and cell signaling mutant (JP1) Pseudomonas aeruginosa biofilms. Appl Environ Microbiol70: 5847–5852.
141.
Wong TY, Preston LA, Schiller NL (2000). Alginate lyase: review of major sources and enzyme characteristics, structure-function analysis, biological roles, and applications. Annu Rev Microbiol54:289–340.
142.
Wrangstadh M, Conway PL, Kjelleberg S (1989). The role of an extracellular polysaccharide produced by the marine Pseudomonas sp. S9 in cellular detachment during starvation. Can J Microbiol35: 309–312.
143.
Xun LY, Mah RA, Boone DR (1990). Isolation and characterization of disaggregatase from Methanosarcina mazei LYC. Appl Environ Microbiol56:3693–3698.
144.
Yao Y, Sturdevant DE, Otto M (2005). 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 Dis191:289–298.
145.
Yarwood JM, Bartels DJ, Volper EM, Greenberg EP (2004). Quorum sensing in Staphylococcus aureus biofilms. J Bacteriol186:1838–1850.
146.
Yildiz FH (2008). Cyclic dimeric GMP signaling and regulation of surface associated developmental programs. J Bacteriol190:781–783.
147.
Yildiz FH, Visick KL (2009). Vibrio biofilms: so much the same yet so different. Trends Microbiol17:109–118.
148.
Ymele-Leki P, Ross JM (2007). Erosion from Staphylococcus aureus biofilms grown under physiologically relevant fluid shear forces yields bacterial cells with reduced avidity to collagen. Appl Environ Microbiol73:1834–1841.
149.
Yu C, Lee AM, Bassler BL, Roseman S (1991). Chitin utilization by marine bacteria. J Biol Chem266:24260–24267.
150.
Zaitseva J, Granik V, Belik A, Koksharova O, Khmel I (2009). Effect of nitrofurans and NO generators on biofilm formation by Pseudomonas aeruginosa PAO1 and Burkholderia cenocepacia 370. Res Microbiol160:353–357.
