Chapter 17 : Dispersal from Microbial Biofilms

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in

Dispersal from Microbial Biofilms, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555817466/9781555817459_Chap17-1.gif /docserver/preview/fulltext/10.1128/9781555817466/9781555817459_Chap17-2.gif


For all organisms the ability to spread and colonize new habitats is crucial to ensure species continuity and prevent extinction ( ). In sessile organisms this constraint has led to the evolution of a motile, dispersal phase in their life cycle, which in plants and corals involves the release of differentiated and often phenotypically diverse seeds or propagules. Similarly, sessile microbial biofilms have developed mechanisms to release differentiated, highly motile dispersal cells into the bulk liquid.

Citation: Barraud N, Kjelleberg S, Rice S. 2015. Dispersal from Microbial Biofilms, p 343-362. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0015-2014
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


Image of Figure 1
Figure 1

Microscopic images of biofilm microcolonies during seeding dispersal. (A-B) Motile cells appear in mature biofilm microcolonies. (A) Single frame of a mature microcolony. (B) Picture showing the average of 30 frames captured over a 1-second period. The highly motile cells “average” out and appear blurred in the center of the microcolony, demonstrating the extent of the motile region (white arrow in panels A and B). The sessile “wall” region is indicated by the black arrows in panel A (taken from reference , with permission from the publisher). (C) Live/dead staining of a 7-day-old biofilm reveals patterns of cell death inside biofilm structures that occur simultaneously with biofilm dispersal, as indicated by the formation of hollow biofilm structures. Live cells are green and dead cells are red (adapted from reference , copyright © American Society for Microbiology). (D) XZ cross-view of the biofilm in panel C (XY view) at the location indicated by the white line.

Citation: Barraud N, Kjelleberg S, Rice S. 2015. Dispersal from Microbial Biofilms, p 343-362. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0015-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 2
Figure 2

Effectors of biofilm dispersal. Bacteria within the center of microcolonies induce a number of mechanisms to degrade and solubilize the biofilm EPS matrix and extracellular appendages such as fimbriae that immobilize cells. When the interior of the microcolony becomes fluid, cells begin to show signs of motility, and a breach is made in the microcolony wall through which dispersal cells are released.

Citation: Barraud N, Kjelleberg S, Rice S. 2015. Dispersal from Microbial Biofilms, p 343-362. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0015-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 3
Figure 3

Physiological traits of planktonic, biofilm, and dispersal cells. Symbols are defined in Figure 2 .

Citation: Barraud N, Kjelleberg S, Rice S. 2015. Dispersal from Microbial Biofilms, p 343-362. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0015-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 4
Figure 4

A range of strategies targeting dispersal have been developed to control biofilms and biofilm-related infections. (a) BdcA protein with enhanced c-di-GMP binding ( ). (b) Oroidin and synthetic derivatives that were identified as potent dispersal inducers after screening chemical libraries ( ). (c) Diffusible fatty acid signal cis-2-decenoic acid ( ). (d) Furanone 30, a synthetic QS inhibitor derived from natural furanone compounds isolated from the red alga ( ). (e) Fimbrolide-nitroester with dual action QS inhibition and NO release ( ). (f) β-lactam-NO prodrugs for the targeted delivery of NO to infectious biofilms ( ). (g) Controlled delivery of NO using nanoparticles ( ). (h) Catalytic generation of NO from endogenous nitrite sources to disperse and prevent biofilm for long-term applications ( ).

Citation: Barraud N, Kjelleberg S, Rice S. 2015. Dispersal from Microbial Biofilms, p 343-362. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0015-2014
Permissions and Reprints Request Permissions
Download as Powerpoint


1. Ronce O . 2007. How does it feel to be like a rolling stone? Ten questions about dispersal evolution. Annu Rev Ecol Evol Syst 38 : 231 253.[CrossRef]
2. Nadell CD,, Bassler BL . 2011. A fitness trade-off between local competition and dispersal in Vibrio cholerae biofilms. Proc Natl Acad Sci USA 108 : 14181 14185.[PubMed] [CrossRef]
3. Kisdi E . 2002. Dispersal: risk spreading versus local adaptation. Am Nat 159 : 579 596.[PubMed] [CrossRef]
4. Kerr B,, Neuhauser C,, Bohannan BJ,, Dean AM . 2006. Local migration promotes competitive restraint in a host-pathogen ‘tragedy of the commons.’ Nature 442 : 75 78.[PubMed] [CrossRef]
5. Gyllenberg M,, Parvinen K,, Dieckmann U . 2002. Evolutionary suicide and evolution of dispersal in structured metapopulations. J Math Biol 45 : 79 105.[PubMed] [CrossRef]
6. Petrova OE,, Sauer K . 2009. A novel signaling network essential for regulating Pseudomonas aeruginosa biofilm development. PLoS Pathog 5 : e1000668. doi:10.1371/journal.ppat.1000668. [PubMed] [CrossRef]
7. Petrova OE,, Sauer K . 2012. Sticky situations: key components that control bacterial surface attachment. J Bacteriol 194 : 2413 2425.[PubMed] [CrossRef]
8. Whiteley M,, Bangera MG,, Bumgarner RE,, Parsek MR,, Teitzel GM,, Lory S,, Greenberg EP . 2001. Gene expression in Pseudomonas aeruginosa biofilms. Nature 413 : 860 864.[PubMed] [CrossRef]
9. Klausen M,, Aaes-Jorgensen A,, Molin S,, Tolker-Nielsen T . 2003. Involvement of bacterial migration in the development of complex multicellular structures in Pseudomonas aeruginosa biofilms. Mol Microbiol 50 : 61 68.[PubMed] [CrossRef]
10. Yang L,, Hu Y,, Liu Y,, Zhang J,, Ulstrup J,, Molin S . 2011. Distinct roles of extracellular polymeric substances in Pseudomonas aeruginosa biofilm development. Environ Microbiol 13 : 1705 1717.[PubMed] [CrossRef]
11. Irie Y,, Borlee BR,, O’Connor JR,, Hill PJ,, Harwood CS,, Wozniak DJ,, Parsek MR . 2012. Self-produced exopolysaccharide is a signal that stimulates biofilm formation in Pseudomonas aeruginosa . Proc Natl Acad Sci USA 109 : 20632 20636.[PubMed] [CrossRef]
12. Lenz AP,, Williamson KS,, Pitts B,, Stewart PS,, Franklin MJ . 2008. Localized gene expression in Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 74 : 4463 4471.[PubMed] [CrossRef]
13. Stewart PS,, Franklin MJ . 2008. Physiological heterogeneity in biofilms. Nat Rev Microbiol 6 : 199 210.[PubMed] [CrossRef]
14. Williamson KS,, Richards LA,, Perez-Osorio AC,, Pitts B,, McInnerney K,, Stewart PS,, Franklin MJ . 2012. Heterogeneity in Pseudomonas aeruginosa biofilms includes expression of ribosome hibernation factors in the antibiotic-tolerant subpopulation and hypoxia-induced stress response in the metabolically active population. J Bacteriol 194 : 2062 2073.[PubMed] [CrossRef]
15. McDougald D,, Rice SA,, Barraud N,, Steinberg PD,, Kjelleberg S . 2012. Should we stay or should we go: mechanisms and ecological consequences for biofilm dispersal. Nat Rev Microbiol 10 : 39 50.[PubMed]
16. 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.[PubMed] [CrossRef]
17. Tolker-Nielsen T,, Brinch UC,, Ragas PC,, Andersen JB,, Jacobsen CS,, Molin S . 2000. Development and dynamics of Pseudomonas sp. biofilms. J Bacteriol 182 : 6482 6489.[PubMed] [CrossRef]
18. Entcheva-Dimitrov P,, Spormann AM . 2004. Dynamics and control of biofilms of the oligotrophic bacterium Caulobacter crescentus . J Bacteriol 186 : 8254 8266.[PubMed] [CrossRef]
19. Lawrence JR,, Chenier MR,, Roy R,, Beaumier D,, Fortin N,, Swerhone GD,, Neu TR,, Greer CW . 2004. Microscale and molecular assessment of impacts of nickel, nutrients, and oxygen level on structure and function of river biofilm communities. Appl Environ Microbiol 70 : 4326 4339.[PubMed] [CrossRef]
20. Manteca A,, Fernandez M,, Sanchez J . 2005. A death round affecting a young compartmentalized mycelium precedes aerial mycelium dismantling in confluent surface cultures of Streptomyces antibioticus . Microbiology 151 : 3689 3697.[PubMed] [CrossRef]
21. Bayles KW . 2007. The biological role of death and lysis in biofilm development. Nat Rev Microbiol 5 : 721 726.[PubMed] [CrossRef]
22. Mai-Prochnow A,, Lucas-Elio P,, Egan S,, Thomas T,, Webb JS,, Sanchez-Amat A,, Kjelleberg S . 2008. Hydrogen peroxide linked to lysine oxidase activity facilitates biofilm differentiation and dispersal in several Gram-negative bacteria. J Bacteriol 190 : 5493 5501.[PubMed] [CrossRef]
23. Davies DG,, Marques CN . 2009. A fatty acid messenger is responsible for inducing dispersion in microbial biofilms. J Bacteriol 191 : 1393 1403.[PubMed] [CrossRef]
24. Mai-Prochnow A,, Evans F,, Dalisay-Saludes D,, Stelzer S,, Egan S,, James S,, Webb JS,, Kjelleberg S . 2004. Biofilm development and cell death in the marine bacterium Pseudoalteromonas tunicata . Appl Environ Microbiol 70 : 3232 3238.[PubMed] [CrossRef]
25. Huynh TT,, McDougald D,, Klebensberger J,, Al Qarni B,, Barraud N,, Rice SA,, Kjelleberg S,, Schleheck D . 2012. Glucose starvation-induced dispersal of Pseudomonas aeruginosa biofilms is cAMP and energy dependent. PLoS One 7 : e42874. doi:10.1371/journal.pone.0042874. [PubMed] [CrossRef]
26. Purevdorj-Gage B,, Costerton WJ,, Stoodley P . 2005. Phenotypic differentiation and seeding dispersal in non-mucoid and mucoid Pseudomonas aeruginosa biofilms. Microbiology 151 : 1569 1576.[PubMed] [CrossRef]
27. Sauer K,, Camper AK,, Ehrlich GD,, Costerton JW,, Davies DG . 2002. Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm. J Bacteriol 184 : 1140 1154.[PubMed] [CrossRef]
28. Morgan R,, Kohn S,, Hwang SH,, Hassett DJ,, Sauer K . 2006. BdlA, a chemotaxis regulator essential for biofilm dispersion in Pseudomonas aeruginosa . J Bacteriol 188 : 7335 7343.[PubMed] [CrossRef]
29. Barraud N,, Schleheck D,, Klebensberger J,, Webb JS,, Hassett DJ,, Rice SA,, Kjelleberg S . 2009. Nitric oxide signaling in Pseudomonas aeruginosa biofilms mediates phosphodiesterase activity, decreased cyclic di-GMP levels, and enhanced dispersal. J Bacteriol 191 : 7333 7342.[PubMed] [CrossRef]
30. Rollet C,, Gal L,, Guzzo J . 2009. Biofilm-detached cells, a transition from a sessile to a planktonic phenotype: a comparative study of adhesion and physiological characteristics in Pseudomonas aeruginosa . FEMS Microbiol Lett 290 : 135 142.[PubMed] [CrossRef]
31. Gjermansen M,, Ragas P,, Sternberg C,, Molin S,, Tolker-Nielsen T . 2005. Characterization of starvation-induced dispersion in Pseudomonas putida biofilms. Environ Microbiol 7 : 894 906.[PubMed] [CrossRef]
32. Schleheck D,, Barraud N,, Klebensberger J,, Webb JS,, McDougald D,, Rice SA,, Kjelleberg S . 2009. Pseudomonas aeruginosa PAO1 preferentially grows as aggregates in liquid batch cultures and disperses upon starvation. PLoS One 4 : e5513. doi:10.1371/journal.pone.0005513. [PubMed] [CrossRef]
33. Newell PD,, Boyd CD,, Sondermann H,, O’Toole GA . 2011. A c-di-GMP effector system controls cell adhesion by inside-out signaling and surface protein cleavage. PLoS Biol 9 : e1000587. doi:10.1371/journal.pbio.1000587. [PubMed] [CrossRef]
34. Banin E,, Brady KM,, Greenberg EP . 2006. Chelator-induced dispersal and killing of Pseudomonas aeruginosa cells in a biofilm. Appl Environ Microbiol 72 : 2064 2069.[PubMed] [CrossRef]
35. Thormann KM,, Saville RM,, Shukla S,, Spormann AM . 2005. Induction of rapid detachment in Shewanella oneidensis MR-1 biofilms. J Bacteriol 187 : 1014 1021.[PubMed] [CrossRef]
36. An S,, Wu J,, Zhang LH . 2010. Modulation of Pseudomonas aeruginosa biofilm dispersal by a cyclic-di-GMP phosphodiesterase with a putative hypoxia-sensing domain. Appl Environ Microbiol 76 : 8160 8173.[PubMed] [CrossRef]
37. Saville RM,, Rakshe S,, Haagensen JA,, Shukla S,, Spormann AM . 2011. Energy-dependent stability of Shewanella oneidensis MR-1 biofilms. J Bacteriol 193 : 3257 3264.[PubMed] [CrossRef]
38. Sauer K,, Cullen MC,, Rickard AH,, Zeef LA,, Davies DG,, Gilbert P . 2004. Characterization of nutrient-induced dispersion in Pseudomonas aeruginosa PAO1 biofilm. J Bacteriol 186 : 7312 7326.[PubMed] [CrossRef]
39. Musk DJ,, Banko DA,, Hergenrother PJ . 2005. Iron salts perturb biofilm formation and disrupt existing biofilms of Pseudomonas aeruginosa . Chem Biol 12 : 789 796.[PubMed] [CrossRef]
40. Chatterjee S,, Wistrom C,, Lindow SE . 2008. A cell-cell signaling sensor is required for virulence and insect transmission of Xylella fastidiosa . Proc Natl Acad Sci USA 105 : 2670 2675.[PubMed] [CrossRef]
41. Hagai E,, Dvora R,, Havkin-Blank T,, Zelinger E,, Porat Z,, Schulz S,, Helman Y . 2014. Surface-motility induction, attraction and hitchhiking between bacterial species promote dispersal on solid surfaces. ISME J 8 : 1147 1151.[PubMed] [CrossRef]
42. Solano C,, Echeverz M,, Lasa I . 2014. Biofilm dispersion and quorum sensing. Curr Opin Microbiol 18c : 96 104.[PubMed] [CrossRef]
43. Zhu J,, Mekalanos JJ . 2003. Quorum sensing-dependent biofilms enhance colonization in Vibrio cholerae . Dev Cell 5 : 647 656.[CrossRef]
44. Kim SM,, Park JH,, Lee HS,, Kim WB,, Ryu JM,, Han HJ,, Choi SH . 2013. LuxR homologue SmcR is essential for Vibrio vulnificus pathogenesis and biofilm detachment, and its expression is induced by host cells. Infect Immun 81 : 3721 3730.[PubMed] [CrossRef]
45. 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 Bacteriol 187 : 3477 3485.[PubMed] [CrossRef]
46. Puskas A,, Greenberg EP,, Kaplan S,, Schaefer AL . 1997. A quorum-sensing system in the free-living photosynthetic bacterium Rhodobacter sphaeroides . J Bacteriol 179 : 7530 7537.[PubMed]
47. Boles BR,, Horswill AR . 2008. agr-Mediated dispersal of Staphylococcus aureus biofilms. PLoS Pathog 4 : e1000052. doi:10.1371/journal.ppat.1000052. [PubMed] [CrossRef]
48. Hammer BK,, Bassler BL . 2003. Quorum sensing controls biofilm formation in Vibrio cholerae . Mol Microbiol 50 : 101 104.[PubMed] [CrossRef]
49. Bari SM,, Roky MK,, Mohiuddin M,, Kamruzzaman M,, Mekalanos JJ,, Faruque SM . 2013. Quorum-sensing autoinducers resuscitate dormant Vibrio cholerae in environmental water samples. Proc Natl Acad Sci USA 110 : 9926 9931.[PubMed] [CrossRef]
50. Dow JM,, Crossman L,, Findlay K,, He YQ,, Feng JX,, Tang JL . 2003. Biofilm dispersal in Xanthomonas campestris is controlled by cell-cell signaling and is required for full virulence to plants. Proc Natl Acad Sci USA 100 : 10995 11000.[PubMed] [CrossRef]
51. Deng Y,, Wu J,, Tao F,, Zhang LH . 2011. Listening to a new language: DSF-based quorum sensing in Gram-negative bacteria. Chem Rev 111 : 160 173.[PubMed] [CrossRef]
52. Hentzer M,, Riedel K,, Rasmussen TB,, Heydorn A,, Andersen JB,, Parsek MR,, Rice SA,, Eberl L,, Molin S,, Hoiby N,, Kjelleberg S,, Givskov M . 2002. Inhibition of quorum sensing in Pseudomonas aeruginosa biofilm bacteria by a halogenated furanone compound. Microbiology 148 : 87 102.[PubMed]
53. Lonn-Stensrud J,, Landin MA,, Benneche T,, Petersen FC,, Scheie AA . 2009. Furanones, potential agents for preventing Staphylococcus epidermidis biofilm infections? J Antimicrob Chemother 63 : 309 316.[PubMed] [CrossRef]
54. Kolodkin-Gal I,, Romero D,, Cao S,, Clardy J,, Kolter R,, Losick R . 2010. d-Amino acids trigger biofilm disassembly. Science 328 : 627 629.[PubMed] [CrossRef]
55. Leiman SA,, May JM,, Lebar MD,, Kahne D,, Kolter R,, Losick R . 2013. d-Amino acids indirectly inhibit biofilm formation in Bacillus subtilis by interfering with protein synthesis. J Bacteriol 195 : 5391 5395.[PubMed] [CrossRef]
56. Barraud N,, Hassett DJ,, Hwang SH,, Rice SA,, Kjelleberg S,, Webb JS . 2006. Involvement of nitric oxide in biofilm dispersal of Pseudomonas aeruginosa . J Bacteriol 188 : 7344 7353.[PubMed] [CrossRef]
57. Barraud N,, Kelso MJ,, Rice SA,, Kjelleberg S . 2014. Nitric oxide: a key mediator of biofilm dispersal with applications in infectious diseases. Curr Pharm Design 21 : 31 42.[PubMed] [CrossRef]
58. Sondermann H,, Shikuma NJ,, Yildiz FH . 2012. You’ve come a long way: c-di-GMP signaling. Curr Opin Microbiol 15 : 140 146.[PubMed] [CrossRef]
59. Römling U,, Galperin MY,, Gomelsky M . 2013. Cyclic di-GMP: the first 25 years of a universal bacterial second messenger. Microbiol Mol Biol Rev 77 : 1 52.[PubMed] [CrossRef]
60. Kalivoda EJ,, Brothers KM,, Stella NA,, Schmitt MJ,, Shanks RM . 2013. Bacterial cyclic AMP-phosphodiesterase activity coordinates biofilm formation. PLoS One 8 : e71267. doi:10.1371/journal.pone.0071267. [PubMed] [CrossRef]
61. Galperin MY,, Higdon R,, Kolker E . 2010. Interplay of heritage and habitat in the distribution of bacterial signal transduction systems. Mol Biosyst 6 : 721 728.[PubMed] [CrossRef]
62. Gomelsky M . 2011. cAMP, c-di-GMP, c-di-AMP and now cGMP: bacteria use them all! Mol Microbiol 79 : 562 565.[PubMed] [CrossRef]
63. Liu N,, Xu Y,, Hossain S,, Huang N,, Coursolle D,, Gralnick JA,, Boon EM . 2012. Nitric oxide regulation of cyclic di-GMP synthesis and hydrolysis in Shewanella woodyi . Biochemistry 51 : 2087 2099.[PubMed] [CrossRef]
64. Carlson HK,, Vance RE,, Marletta MA . 2010. H-NOX regulation of c-di-GMP metabolism and biofilm formation in Legionella pneumophila . Mol Microbiol 77 : 930 942.[PubMed]
65. Roy AB,, Petrova OE,, Sauer K . 2012. The phosphodiesterase DipA (PA5017) is essential for Pseudomonas aeruginosa biofilm dispersion. J Bacteriol 194 : 2904 2915.[PubMed] [CrossRef]
66. Li Y,, Heine S,, Entian M,, Sauer K,, Frankenberg-Dinkel N . 2013. NO-induced biofilm dispersion in Pseudomonas aeruginosa is mediated by an MHYT domain-coupled phosphodiesterase. J Bacteriol 195 : 3531 3542.[PubMed] [CrossRef]
67. Nioche P,, Berka V,, Vipond J,, Minton N,, Tsai AL,, Raman CS . 2004. Femtomolar sensitivity of a NO sensor from Clostridium botulinum . Science 306 : 1550 1553.[PubMed] [CrossRef]
68. Plate L,, Marletta MA . 2013. Nitric oxide-sensing H-NOX proteins govern bacterial communal behavior. Trends Biochem Sci 38 : 566 575.[PubMed] [CrossRef]
69. Tanaka A,, Takahashi H,, Shimizu T . 2007. Critical role of the heme axial ligand, Met 95, in locking catalysis of the phosphodiesterase from Escherichia coli ( Ec DOS) toward cyclic diGMP. J Biol Chem 282 : 21301 21307.[PubMed] [CrossRef]
70. Tuckerman JR,, Gonzalez G,, Sousa EH,, Wan X,, Saito JA,, Alam M,, Gilles-Gonzalez MA . 2009. An oxygen-sensing diguanylate cyclase and phosphodiesterase couple for c-di-GMP control. Biochemistry 48 : 9764 9774.[PubMed] [CrossRef]
71. Petrova OE,, Sauer K . 2012. Dispersion by Pseudomonas aeruginosa requires an unusual posttranslational modification of BdlA. Proc Natl Acad Sci USA 109 : 16690 16695.[PubMed] [CrossRef]
72. Kaplan JB,, Meyenhofer MF,, Fine DH . 2003. Biofilm growth and detachment of Actinobacillus actinomycetemcomitans . J Bacteriol 185 : 1399 1404.[PubMed] [CrossRef]
73. Kaplan JB,, Ragunath C,, Velliyagounder K,, Fine DH,, Ramasubbu N . 2004. Enzymatic detachment of Staphylococcus epidermidis biofilms. Antimicrob Agents Chemother 48 : 2633 2636.[PubMed] [CrossRef]
74. Boyd A,, Chakrabarty AM . 1994. Role of alginate lyase in cell detachment of Pseudomonas aeruginosa . Appl Environ Microbiol 60 : 2355 2359.[PubMed]
75. Whitchurch CB,, Tolker-Nielsen T,, Ragas PC,, Mattick JS . 2002. Extracellular DNA required for bacterial biofilm formation. Science 295 : 1487. [PubMed] [CrossRef]
76. Mann EE,, Rice KC,, Boles BR,, Endres JL,, Ranjit D,, Chandramohan L,, Tsang LH,, Smeltzer MS,, Horswill AR,, Bayles KW . 2009. Modulation of eDNA release and degradation affects Staphylococcus aureus biofilm maturation. PLoS One 4 : e5822. doi:10.1371/journal.pone.0005822. [PubMed] [CrossRef]
77. Nijland R,, Hall MJ,, Burgess JG . 2010. Dispersal of biofilms by secreted, matrix degrading, bacterial DNase. PLoS One 5 : e15668. doi:10.1371/journal.pone.0015668. [PubMed] [CrossRef]
78. Gjermansen M,, Nilsson M,, Yang L,, Tolker-Nielsen T . 2010. Characterization of starvation-induced dispersion in Pseudomonas putida biofilms: genetic elements and molecular mechanisms. Mol Microbiol 75 : 815 826.[PubMed] [CrossRef]
79. Sheikh J,, Czeczulin JR,, Harrington S,, Hicks S,, Henderson IR,, Le Bouguenec C,, Gounon P,, Phillips A,, Nataro JP . 2002. A novel dispersin protein in enteroaggregative Escherichia coli . J Clin Invest 110 : 1329 1337.[PubMed] [CrossRef]
80. 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 Microbiol 33 : 499 509.[PubMed] [CrossRef]
81. Boles BR,, Thoendel M,, Singh PK . 2005. Rhamnolipids mediate detachment of Pseudomonas aeruginosa from biofilms. Mol Microbiol 57 : 1210 1223.[PubMed] [CrossRef]
82. Kuiper I,, Lagendijk EL,, Pickford R,, Derrick JP,, Lamers GEM,, Thomas-Oates JE,, Lugtenberg BJJ,, Bloemberg GV . 2004. Characterization of two Pseudomonas putida lipopeptide biosurfactants, putisolvin I and II, which inhibit biofilm formation and break down existing biofilms. Mol Microbiol 51 : 97 113.[PubMed] [CrossRef]
83. 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 Bacteriol 184 : 290 301.[PubMed] [CrossRef]
84. Gibiansky ML,, Conrad JC,, Jin F,, Gordon VD,, Motto DA,, Mathewson MA,, Stopka WG,, Zelasko DC,, Shrout JD,, Wong GC . 2010. Bacteria use type IV pili to walk upright and detach from surfaces. Science 330 : 197. [PubMed] [CrossRef]
85. Mai-Prochnow A,, Ferrari BC,, Webb JS,, Kjelleberg S . 2006. Ecological advantages of autolysis during the development and dispersal of Pseudoalteromonas tunicata biofilms. Appl Environ Microbiol 72 : 5414 5420.[PubMed] [CrossRef]
86. Woo JK,, Webb JS,, Kirov SM,, Kjelleberg S,, Rice SA . 2012. Biofilm dispersal cells of a cystic fibrosis Pseudomonas aeruginosa isolate exhibit variability in functional traits likely to contribute to persistent infection. FEMS Immunol Med Microbiol 66 : 251 264.[PubMed] [CrossRef]
87. Liu J,, Ling JQ,, Zhang K,, Wu CD . 2013. Physiological properties of Streptococcus mutans UA159 biofilm-detached cells. FEMS Microbiol Lett 340 : 11 18.[PubMed] [CrossRef]
88. Vaysse PJ,, Sivadon P,, Goulas P,, Grimaud R . 2011. Cells dispersed from Marinobacter hydrocarbonoclasticus SP17 biofilm exhibit a specific protein profile associated with a higher ability to reinitiate biofilm development at the hexadecane-water interface. Environ Microbiol 13 : 737 746.[PubMed] [CrossRef]
89. Behnke S,, Parker AE,, Woodall D,, Camper AK . 2011. Comparing the chlorine disinfection of detached biofilm clusters with those of sessile biofilms and planktonic cells in single- and dual-species cultures. Appl Environ Microbiol 77 : 7176 7184.[PubMed] [CrossRef]
90. Kirov SM,, Webb JS,, O’May CY,, Reid DW,, Woo JK,, Rice SA,, Kjelleberg S . 2007. Biofilm differentiation and dispersal in mucoid Pseudomonas aeruginosa isolates from patients with cystic fibrosis. Microbiology 153 : 3264 3274.[PubMed] [CrossRef]
91. Koh KS,, Lam KW,, Alhede M,, Queck SY,, Labbate M,, Kjelleberg S,, Rice SA . 2007. Phenotypic diversification and adaptation of Serratia marcescens MG1 biofilm derived morphotypes. J Bacteriol 189 : 119 130.[PubMed] [CrossRef]
92. Koh KS,, Matz C,, Tan CH,, Le HL,, Rice SA,, Marshall DJ,, Steinberg PD,, Kjelleberg S . 2012. Minimal increase in genetic diversity enhances predation resistance. Mol Ecol 21 : 1741 1753.[PubMed] [CrossRef]
93. Lee KW,, Periasamy S,, Mukherjee M,, Xie C,, Kjelleberg S,, Rice SA . 2014. Biofilm development and enhanced stress resistance of a model, mixed-species community biofilm. ISME J 8 : 894 907.[PubMed] [CrossRef]
94. McElroy KE,, Hui JG,, Woo JK,, Luk AW,, Webb JS,, Kjelleberg S,, Rice SA,, Thomas T . 2014. Strain-specific parallel evolution drives short-term diversification during Pseudomonas aeruginosa biofilm formation. Proc Natl Acad Sci USA 111 : E1419 E1427.[PubMed] [CrossRef]
95. Boles BR,, Singh PK . 2008. Endogenous oxidative stress produces diversity and adaptability in biofilm communities. Proc Natl Acad Sci USA 105 : 12503 12508.[PubMed] [CrossRef]
96. Webb JS,, Lau M,, Kjelleberg S . 2004. Bacteriophage and phenotypic variation in Pseudomonas aeruginosa biofilm development. J Bacteriol 186 : 8066 8073.[PubMed] [CrossRef]
97. Fang H,, Toyofuku M,, Kiyokawa T,, Ichihashi A,, Tateda K,, Nomura N . 2013. The impact of anaerobiosis on strain-dependent phenotypic variations in Pseudomonas aeruginosa . Biosci Biotechnol Biochem 77 : 1747 1752.[PubMed] [CrossRef]
98. Webb JS,, Givskov M,, Kjelleberg S . 2003. Bacterial biofilms: prokaryotic adventures in multicellularity. Curr Opin Microbiol 6 : 578 585.[PubMed] [CrossRef]
99. Hochberg ME,, Rankin DJ,, Taborsky M . 2008. The coevolution of cooperation and dispersal in social groups and its implications for the emergence of multicellularity. BMC Evol Biol 8 : 238. [PubMed] [CrossRef]
100. Boots M,, Mealor M . 2007. Local interactions select for lower pathogen infectivity. Science 315 : 1284 1286.[PubMed] [CrossRef]
101. Wild G,, Gardner A,, West SA . 2009. Adaptation and the evolution of parasite virulence in a connected world. Nature 459 : 983 986.[PubMed] [CrossRef]
102. Barraud N,, Buson A,, Jarolimek W,, Rice SA . 2013. Mannitol enhances antibiotic sensitivity of persister bacteria in Pseudomonas aeruginosa biofilms. PLoS One 8 : e84220. doi:10.1371/journal.pone.0084220. [PubMed] [CrossRef]
103. Hoiby N,, Bjarnsholt T,, Givskov M,, Molin S,, Ciofu O . 2010. Antibiotic resistance of bacterial biofilms. Int J Antimicrob Agents 35 : 322 332.[PubMed] [CrossRef]
104. Roberts AP,, Mullany P . 2010. Oral biofilms: a reservoir of transferable, bacterial, antimicrobial resistance. Expert Rev Anti-Infect Ther 8 : 1441 1450.[PubMed] [CrossRef]
105. Smith EE,, Buckley DG,, Wu Z,, Saenphimmachak C,, Hoffman LR,, D’Argenio DA,, Miller SI,, Ramsey BW,, Speert DP,, Moskowitz SM,, Burns JL,, Kaul R,, Olson MV . 2006. Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc Natl Acad Sci USA 103 : 8487 8492.[PubMed] [CrossRef]
106. Yang L,, Jelsbak L,, Marvig RL,, Damkiaer S,, Workman CT,, Rau MH,, Hansen SK,, Folkesson A,, Johansen HK,, Ciofu O,, Hoiby N,, Sommer MO,, Molin S . 2011. Evolutionary dynamics of bacteria in a human host environment. Proc Natl Acad Sci USA 108 : 7481 7486.[PubMed] [CrossRef]
107. Folkesson A,, Jelsbak L,, Yang L,, Johansen HK,, Ciofu O,, Hoiby N,, Molin S . 2012. Adaptation of Pseudomonas aeruginosa to the cystic fibrosis airway: an evolutionary perspective. Nat Rev Microbiol 10 : 841 851.[PubMed] [CrossRef]
108. Poltak SR,, Cooper VS . 2011. Ecological succession in long-term experimentally evolved biofilms produces synergistic communities. ISME J 5 : 369 378.[PubMed] [CrossRef]
109. Traverse CC,, Mayo-Smith LM,, Poltak SR,, Cooper VS . 2013. Tangled bank of experimentally evolved Burkholderia biofilms reflects selection during chronic infections. Proc Natl Acad Sci USA 110 : E250 E259.[PubMed] [CrossRef]
110. Wendehenne D,, Pugin A,, Klessig DF,, Durner J . 2001. Nitric oxide: comparative synthesis and signaling in animal and plant cells. Trends Plant Sci 6 : 177 183.[PubMed] [CrossRef]
111. Rice SA,, Tan CH,, Mikkelsen PJ,, Kung V,, Woo J,, Tay M,, Hauser A,, McDougald D,, Webb JS,, Kjelleberg S . 2009. The biofilm life cycle and virulence of Pseudomonas aeruginosa are dependent on a filamentous prophage. ISME J 3 : 271 282.[PubMed] [CrossRef]
112. Brockhurst MA,, Buckling A,, Rainey PB . 2005. The effect of a bacteriophage on diversification of the opportunistic bacterial pathogen, Pseudomonas aeruginosa . Proc Biol Sci 272 : 1385 1391.[PubMed] [CrossRef]
113. Hall-Stoodley L,, Stoodley P . 2005. Biofilm formation and dispersal and the transmission of human pathogens. Trends Microbiol 13 : 7 10.[PubMed] [CrossRef]
114. Chamot-Rooke J,, Mikaty G,, Malosse C,, Soyer M,, Dumont A,, Gault J,, Imhaus AF,, Martin P,, Trellet M,, Clary G,, Chafey P,, Camoin L,, Nilges M,, Nassif X,, Dumenil G . 2011. Posttranslational modification of pili upon cell contact triggers N. meningitidis dissemination. Science 331 : 778 782.[PubMed] [CrossRef]
115. Li Y,, Petrova OE,, Su S,, Lau GW,, Panmanee W,, Na R,, Hassett DJ,, Davies DG,, Sauer K . 2014. BdlA, DipA and induced dispersion contribute to acute virulence and chronic persistence of Pseudomonas aeruginosa . PLoS Pathog 10 : e1004168. doi:10.1371/journal.ppat.1004168. [PubMed] [CrossRef]
116. Moscoso JA,, Mikkelsen H,, Heeb S,, Williams P,, Filloux A . 2011. The Pseudomonas aeruginosa sensor RetS switches type III and type VI secretion via c-di-GMP signalling. Environ Microbiol 13 : 3128 3138.[PubMed] [CrossRef]
117. Besemer K,, Singer G,, Hodl I,, Battin TJ . 2009. Bacterial community composition of stream biofilms in spatially variable-flow environments. Appl Environ Microbiol 75 : 7189 7195.[PubMed] [CrossRef]
118. Székely AJ,, Berga M,, Langenheder S . 2013. Mechanisms determining the fate of dispersed bacterial communities in new environments. ISME J 7 : 61 71.[PubMed] [CrossRef]
119. Darouiche RO,, Mansouri MD,, Gawande PV,, Madhyastha S . 2009. Antimicrobial and antibiofilm efficacy of triclosan and dispersinB combination. J Antimicrob Chemother 64 : 88 93.[PubMed] [CrossRef]
120. Lamppa JW,, Griswold KE . 2013. Alginate lyase exhibits catalysis-independent biofilm dispersion and antibiotic synergy. Antimicrob Agents Chemother 57 : 137 145.[PubMed] [CrossRef]
121. Flemming HC,, Wingender J . 2010. The biofilm matrix. Nat Rev Microbiol 8 : 623 633.[PubMed] [CrossRef]
122. Byrd MS,, Pang B,, Hong W,, Waligora EA,, Juneau RA,, Armbruster CE,, Weimer KE,, Murrah K,, Mann EE,, Lu H,, Sprinkle A,, Parsek MR,, Kock ND,, Wozniak DJ,, Swords WE . 2011. Direct evaluation of Pseudomonas aeruginosa biofilm mediators in a chronic infection model. Infect Immun 79 : 3087 3095.[PubMed] [CrossRef]
123. Christensen LD,, van Gennip M,, Rybtke MT,, Wu H,, Chiang WC,, Alhede M,, Hoiby N,, Nielsen TE,, Givskov M,, Tolker-Nielsen T . 2013. Clearance of Pseudomonas aeruginosa foreign-body biofilm infections through reduction of the cyclic di-GMP level in the bacteria. Infect Immun 81 : 2705 2713.[PubMed] [CrossRef]
124. Ma Q,, Yang Z,, Pu M,, Peti W,, Wood TK . 2011. Engineering a novel c-di-GMP-binding protein for biofilm dispersal. Environ Microbiol 13 : 631 642.[PubMed] [CrossRef]
125. Rogers SA,, Huigens RW 3rd,, Cavanagh J,, Melander C . 2010. Synergistic effects between conventional antibiotics and 2-aminoimidazole-derived antibiofilm agents. Antimicrob Agents Chemother 54 : 2112 2118.[PubMed] [CrossRef]
126. Frei R,, Breitbach AS,, Blackwell HE . 2012. 2-Aminobenzimidazole derivatives strongly inhibit and disperse Pseudomonas aeruginosa biofilms. Angew Chem-Int Edit 51 : 5226 5229.[PubMed] [CrossRef]
127. Cai PJ,, Xiao X,, He YR,, Li WW,, Yu L,, Yu HQ . 2013. Disintegration of aerobic granules induced by trans-2-decenoic acid. Bioresour Technol 128 : 823 826.[PubMed] [CrossRef]
128. Yeon KM,, Cheong WS,, Oh HS,, Lee WN,, Hwang BK,, Lee CH,, Beyenal H,, Lewandowski Z . 2009. Quorum sensing: a new biofouling control paradigm in a membrane bioreactor for advanced wastewater treatment. Environ Sci Technol 43 : 380 385.[PubMed] [CrossRef]
129. Tan CH,, Koh KS,, Xie C,, Tay M,, Zhou Y,, Williams R,, Ng WJ,, Rice SA,, Kjelleberg S . 2014. The role of quorum sensing signalling in EPS production and the assembly of a sludge community into aerobic granules. ISME J. [Epub ahead of print.] doi:10.1038/ismej.2013.240. [PubMed] [CrossRef]
130. Hentzer M,, Givskov M . 2003. Pharmacological inhibition of quorum sensing for the treatment of chronic bacterial infections. J Clin Invest 112 : 1300 1307.[PubMed] [CrossRef]
131. Hentzer M,, Wu H,, Andersen JB,, Riedel K,, Rasmussen TB,, Bagge N,, Kumar N,, Schembri MA,, Song Z,, Kristoffersen P,, Manefield M,, Costerton JW,, Molin S,, Eberl L,, Steinberg P,, Kjelleberg S,, Hoiby N,, Givskov M . 2003. Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. EMBO J 22 : 3803 3815.[PubMed] [CrossRef]
132. Barraud N,, Kardak BG,, Yepuri NR,, Howlin RP,, Webb JS,, Faust SN,, Kjelleberg S,, Rice SA,, Kelso MJ . 2012. Cephalosporin-3′-diazeniumdiolates: targeted NO-donor prodrugs for dispersing bacterial biofilms. Angew Chem-Int Edit 51 : 9057 9060.[PubMed] [CrossRef]
133. Yepuri NR,, Barraud N,, Shah Mohammadi N,, Kardak BG,, Kjelleberg S,, Rice SA,, Kelso MJ . 2013. Synthesis of cephalosporin-3′-diazeniumdiolates: biofilm dispersing NO-donor prodrugs activated by β-lactamase. Chem Commun 49 : 4791 4793.[PubMed] [CrossRef]
134. Kutty SK,, Barraud N,, Pham A,, Iskander G,, Rice SA,, Black DS,, Kumar N . 2013. Design, synthesis, and evaluation of fimbrolide-nitric oxide donor hybrids as antimicrobial agents. J Med Chem 56 : 9517 9529.[PubMed] [CrossRef]
135. Duong HT,, Jung K,, Kutty SK,, Agustina S,, Adnan NN,, Basuki JS,, Kumar N,, Davis TP,, Barraud N,, Boyer C . 2014. Nanoparticle (star polymer) delivery of nitric oxide effectively negates Pseudomonas aeruginosa biofilm formation. Biomacromolecules. [Epub ahead of print.] doi:10.1021/bm500422v. [CrossRef]
136. Barraud N,, Storey MV,, Moore ZP,, Webb JS,, Rice SA,, Kjelleberg S . 2009. Nitric oxide-mediated dispersal in single- and multi-species biofilms of clinically and industrially relevant microorganisms. Microb Biotechnol 2 : 370 378.[PubMed] [CrossRef]
137. Barnes RJ,, Bandi RR,, Wong WS,, Barraud N,, McDougald D,, Fane A,, Kjelleberg S,, Rice SA . 2013. Optimal dosing regimen of nitric oxide donor compounds for the reduction of Pseudomonas aeruginosa biofilm and isolates from wastewater membranes. Biofouling 29 : 203 212.[PubMed] [CrossRef]
138. Ren H,, Wu J,, Xi C,, Lehnert N,, Major T,, Bartlett RH,, Meyerhoff ME . 2014. Electrochemically modulated nitric oxide (NO) releasing biomedical devices via copper(II)-tri(2-pyridylmethyl)amine mediated reduction of nitrite. ACS Appl Mater Interfaces 6 : 3779 3783.[PubMed] [CrossRef]
139. Cathie K,, Howlin RP,, Barraud N,, Carroll MP,, Clarke SC,, Connett GJ,, Cornelius V,, Daniels TW,, Duignan C,, Feelisch M,, Fernandez B,, Hall-Stoodley L,, Jefferies JMC,, Kelso MJ,, Kjelleberg S,, Legg JP,, Pink S,, Rice SA,, Rogers G,, Salib RJ,, Smith C,, Stoodley P,, Sukhtankar P,, Webb JS,, Faust SN . 2014. Low dose nitric oxide as adjunctive therapy to reduce antimicrobial tolerance of Pseudomonas aeruginosa biofilms in the treatment of patients with cystic fibrosis: report of a proof of concept clinical trial. Am J Respir Crit Care Med 189 : A2843.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error