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Chapter 3 : Biofilm Development

Author: Tim Tolker-Nielsen1
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Affiliations: 1: Department of Immunology and Microbiology, Faculty of Health and Medical Sciences, University of Copenhagen, DK 2000 Copenhagen, Denmark
Content Type: Monograph
Publication Year: 2015

Category: Environmental Microbiology

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Biofilm Development, Page 1 of 2

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Abstract:

Experimental approaches primarily focused on genetic and microscopic techniques have laid the foundation for our current models of bacterial biofilm formation. This work has enabled researchers to define biofilm formation as a process that consists of specific stages. The biofilm developmental cycle is believed to include (i) initial attachment of microbes to a surface or each other, (ii) formation of microcolonies, (iii) maturation of the biofilm, and (iv) dispersal of the biofilm (e.g., reference ). The different biofilm stages include bacterial physiology and phenotypic responses suggestive of the existence of a unique biofilm biology which is not found for planktonic bacteria.

Citation: Tolker-Nielsen T. 2015. Biofilm Development, p 51-66. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0001-2014
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Biofilm Development
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Citation: Tolker-Nielsen T. 2015. Biofilm Development, p 51-66. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0001-2014
/content/10.1128/9781555817466.chap3.fig3-1
Figure 1
Confocal laser scanning microscopy (CLSM) images showing spatial structures in flow-chamber-grown 5-day-old biofilms formed by (A) Gfp-tagged (green fluorescent) , (B) Gfp-tagged , and (C) a mixture of Gfp-tagged and DsRed-tagged (red fluorescent) . Bars, 20 μm. Adapted from reference with permission from the American Society for Microbiology.
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10.1128/9781555817466/fig3-1.gif
Image of Figure 1
Figure 1

Confocal laser scanning microscopy (CLSM) images showing spatial structures in flow-chamber-grown 5-day-old biofilms formed by (A) Gfp-tagged (green fluorescent) , (B) Gfp-tagged , and (C) a mixture of Gfp-tagged and DsRed-tagged (red fluorescent) . Bars, 20 μm. Adapted from reference with permission from the American Society for Microbiology.

Citation: Tolker-Nielsen T. 2015. Biofilm Development, p 51-66. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0001-2014
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Figure 2
CLSM micrographs acquired in 5-day-old PAO1 biofilms grown on (A) glucose minimal medium and (B) citrate minimal medium. The central pictures show-top down fluorescence projections, and the flanking pictures show vertical sections. Bars, 20 μm. Adapted from reference with permission from Wiley-Blackwell publishing.
10.1128/9781555817466/fig3-2_thmb.gif
10.1128/9781555817466/fig3-2.gif
Image of Figure 2
Figure 2

CLSM micrographs acquired in 5-day-old PAO1 biofilms grown on (A) glucose minimal medium and (B) citrate minimal medium. The central pictures show-top down fluorescence projections, and the flanking pictures show vertical sections. Bars, 20 μm. Adapted from reference with permission from Wiley-Blackwell publishing.

Citation: Tolker-Nielsen T. 2015. Biofilm Development, p 51-66. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0001-2014
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Figure 3
CLSM vertical sections acquired in a color-coded biofilm grown in a flow chamber on glucose minimal medium. The CLSM micrographs were acquired in a 4-day-old biofilm which was initiated with a 1:1 mixture of Yfp-tagged (yellow fluorescent) PAO1 wild type and Cfp-tagged (cyan fluorescent) mutants. Bars, 20 μm. Adapted from reference with permission from Wiley-Blackwell publishing.
10.1128/9781555817466/fig3-3_thmb.gif
10.1128/9781555817466/fig3-3.gif
Image of Figure 3
Figure 3

CLSM vertical sections acquired in a color-coded biofilm grown in a flow chamber on glucose minimal medium. The CLSM micrographs were acquired in a 4-day-old biofilm which was initiated with a 1:1 mixture of Yfp-tagged (yellow fluorescent) PAO1 wild type and Cfp-tagged (cyan fluorescent) mutants. Bars, 20 μm. Adapted from reference with permission from Wiley-Blackwell publishing.

Citation: Tolker-Nielsen T. 2015. Biofilm Development, p 51-66. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0001-2014
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References

/content/book/10.1128/9781555817466.chap3
1. 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]
2. Whitchurch CB,, Tolker-Nielsen T,, Ragas PC,, Mattick JS . 2002. Extracellular DNA required for bacterial biofilm formation. Science 295 : 1487. [PubMed] [CrossRef]
3. Ma L,, Jackson KD,, Landry RM,, Parsek MR,, Wozniak DJ . 2006. Analysis of Pseudomonas aeruginosa conditional psl variants reveals roles for the psl polysaccharide in adhesion and maintaining biofilm structure postattachment. J Bacteriol 188 : 8213– 8221.[PubMed] [CrossRef]
4. Yang L,, Nilsson M,, Gjermansen M,, Givskov M,, Tolker-Nielsen T . 2009. Pyoverdine and PQS mediated subpopulation interactions involved in Pseudomonas aeruginosa biofilm formation. Mol Microbiol 74 : 1380– 1392.[PubMed] [CrossRef]
5. 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– 261.[PubMed] [CrossRef]
6. Friedman L,, Kolter R . 2003. Genes involved in matrix formation in Pseudomonas aeruginosa PA14 biofilms. Mol Microbiol 51 : 675– 690.[PubMed] [CrossRef]
7. Jackson KD,, Starkey M,, Kremer S,, Parsek MR,, Wozniak DJ . 2004. Identification of psl, a locus encoding a potential exopolysaccharide that is essential for Pseudomonas aeruginosa PAO1 biofilm formation. J Bacteriol 186 : 4466– 4475.[PubMed] [CrossRef]
8. Pamp SJ,, Gjermansen M,, Tolker-Nielsen T, . 2007. The biofilm matrix: a sticky framework, p 37– 69. In Kjelleberg S,, Givskov M (ed), The Biofilm Mode of Life: Mechanisms and Adaptations. Horizon Bioscience, Norfolk, UK.
9. 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]
10. 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]
11. Gjermansen M,, Ragas P,, Tolker-Nielsen T . 2006. Proteins with GGDEF and EAL domains regulate Pseudomonas putida biofilm formation and dispersal. FEMS Microbiol Lett 265 : 215– 224.[PubMed] [CrossRef]
12. Ryan RP,, Lucey J,, O’Donovan K,, McCarthy Y,, Yang L,, Tolker-Nielsen T,, Dow JM . 2009. HD-GYP domain proteins regulate biofilm formation and virulence in Pseudomonas aeruginosa . Environ Microbiol 11 : 1126– 1136.[PubMed] [CrossRef]
13. Simm R,, Morr M,, Kader A,, Nimtz M,, Romling U . 2004. GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility. Mol Microbiol 53 : 1123– 1134.[PubMed] [CrossRef]
14. Ross P,, Weinhouse H,, Aloni Y,, Michaeli D,, Weinberger-Ohana P,, Mayer R,, Braun S,, de Vroom E,, van der Marel GA,, van Boom JH,, Benziman M . 1987. Regulation of cellulose synthesis in Acetobacter xylinum by cyclic diguanylic acid. Nature 325 : 279– 281.[PubMed] [CrossRef]
15. Garcia B,, Latasa C,, Solano C,, Garcia-del Portillo F,, Gamazo C,, Lasa I . 2004. Role of the GGDEF protein family in Salmonella cellulose biosynthesis and biofilm formation. Mol Microbiol 54 : 264– 277.[PubMed] [CrossRef]
16. Tischler AD,, Camilli A . 2004. Cyclic diguanylate (c-di-GMP) regulates Vibrio cholerae biofilm formation. Mol Microbiol 53 : 857– 869.[PubMed] [CrossRef]
17. Kirillina O,, Fetherston JD,, Bobrov AG,, Abney J,, Perry RD . 2004. HmsP, a putative phosphodiesterase, and HmsT, a putative diguanylate cyclase, control Hms-dependent biofilm formation in Yersinia pestis . Mol Microbiol 54 : 75– 88.[PubMed] [CrossRef]
18. Hickman JW,, Tifrea DF,, Harwood CS . 2005. A chemosensory system that regulates biofilm formation through modulation of cyclic diguanylate levels. Proc Natl Acad Sci USA 102 : 14422– 14427.[PubMed] [CrossRef]
19. Kulasakara H,, Lee V,, Brencic A,, Liberati N,, Urbach J,, Miyata S,, Lee DG,, Neely AN,, Hyodo M,, Hayakawa Y,, Ausubel FM,, Lory S . 2006. Analysis of Pseudomonas aeruginosa diguanylate cyclases and phosphodiesterases reveals a role for bis-(3′-5′)-cyclic-GMP in virulence. Proc Natl Acad Sci USA 103 : 2839– 2844.[PubMed] [CrossRef]
20. Goymer P,, Kahn SG,, Malone JG,, Gehrig SM,, Spiers AJ,, Rainey PB . 2006. Adaptive divergence in experimental populations of Pseudomonas fluorescens. II. Role of the GGDEF regulator WspR in evolution and development of the wrinkly spreader phenotype. Genetics 173 : 515– 526.[PubMed] [CrossRef]
21. Lim B,, Beyhan S,, Meir J,, Yildiz FH . 2006. Cyclic-diGMP signal transduction systems in Vibrio cholerae: modulation of rugosity and biofilm formation. Mol Microbiol 60 : 331– 348.[PubMed] [CrossRef]
22. Fazli M,, O’Connell A,, Nilsson M,, Niehaus K,, Dow JM,, Givskov M,, Ryan RP,, Tolker-Nielsen T . 2011. The CRP/FNR family protein Bcam1349 is a c-di-GMP effector that regulates biofilm formation in the respiratory pathogen Burkholderia cenocepacia . Mol Microbiol 82 : 327– 341.[PubMed] [CrossRef]
23. Chen Y,, Chai Y,, Guo JH,, Losick R . 2012. Evidence for cyclic Di-GMP-mediated signaling in Bacillus subtilis . J Bacteriol 194 : 5080– 5090.[PubMed] [CrossRef]
24. Purcell EB,, McKee RW,, McBride SM,, Waters CM,, Tamayo R . 2012. Cyclic diguanylate inversely regulates motility and aggregation in Clostridium difficile . J Bacteriol 194 : 3307– 3316.[PubMed] [CrossRef]
25. Hengge R . 2009. Principles of c-di-GMP signalling in bacteria. Nat Rev Microbiol 7 : 263– 273.[PubMed] [CrossRef]
26. Massie JP,, Reynolds EL,, Koestler BJ,, Cong JP,, Agostoni M,, Waters CM . 2012. Quantification of high-specificity cyclic diguanylate signaling. Proc Natl Acad Sci USA 109 : 12746– 12751.[PubMed] [CrossRef]
27. O’Connor JR,, Kuwada NJ,, Huangyutitham V,, Wiggins PA,, Harwood CS . 2012. Surface sensing and lateral subcellular localization of WspA, the receptor in a chemosensory-like system leading to c-di-GMP production. Mol Microbiol 86 : 720– 729.[PubMed] [CrossRef]
28. Monds RD,, Newell PD,, Gross RH,, O’Toole GA . 2007. Phosphate-dependent modulation of c-di-GMP levels regulates Pseudomonas fluorescens Pf0-1 biofilm formation by controlling secretion of the adhesin LapA. Mol Microbiol 63 : 656– 679.[PubMed] [CrossRef]
29. Guvener ZT,, Harwood CS . 2007. Subcellular location characteristics of the Pseudomonas aeruginosa GGDEF protein, WspR, indicate that it produces cyclic-di-GMP in response to growth on surfaces. Mol Microbiol 66 : 1459– 1473.[PubMed] [CrossRef]
30. Guvener ZT,, Tifrea DF,, Harwood CS . 2006. Two different Pseudomonas aeruginosa chemosensory signal transduction complexes localize to cell poles and form and remould in stationary phase. Mol Microbiol 61 : 106– 118.[PubMed] [CrossRef]
31. Borlee BR,, Goldman AD,, Murakami K,, Samudrala R,, Wozniak DJ,, Parsek MR . 2010. Pseudomonas aeruginosa uses a cyclic-di-GMP-regulated adhesin to reinforce the biofilm extracellular matrix. Mol Microbiol 75 : 827– 842.[PubMed] [CrossRef]
32. Chambers JR,, Sauer K . 2013. Small RNAs and their role in biofilm formation. Trends Microbiol 21 : 39– 49.[PubMed] [CrossRef]
33. Goodman AL,, Kulasekara B,, Rietsch A,, Boyd D,, Smith RS,, Lory S . 2004. A signaling network reciprocally regulates genes associated with acute infection and chronic persistence in Pseudomonas aeruginosa . Dev Cell 7 : 745– 754.[PubMed] [CrossRef]
34. Goodman AL,, Merighi M,, Hyodo M,, Ventre I,, Filloux A,, Lory S . 2009. Direct interaction between sensor kinase proteins mediates acute and chronic disease phenotypes in a bacterial pathogen. Genes Dev 23 : 249– 259.[PubMed] [CrossRef]
35. Ventre I,, Goodman AL,, Vallet-Gely I,, Vasseur P,, Soscia C,, Molin S,, Bleves S,, Lazdunski A,, Lory S,, Filloux A . 2006. Multiple sensors control reciprocal expression of Pseudomonas aeruginosa regulatory RNA and virulence genes. Proc Natl Acad Sci USA 103 : 171– 176.[PubMed] [CrossRef]
36. Brencic A,, Lory S . 2009. Determination of the regulon and identification of novel mRNA targets of Pseudomonas aeruginosa RsmA. Mol Microbiol 72 : 612– 632.[PubMed] [CrossRef]
37. Brencic A,, McFarland KA,, McManus HR,, Castang S,, Mogno I,, Dove SL,, Lory S . 2009. The GacS/GacA signal transduction system of Pseudomonas aeruginosa acts exclusively through its control over the transcription of the RsmY and RsmZ regulatory small RNAs. Mol Microbiol 73 : 434– 445.[PubMed] [CrossRef]
38. Irie Y,, Starkey M,, Edwards AN,, Wozniak DJ,, Romeo T,, Parsek MR . 2010. Pseudomonas aeruginosa biofilm matrix polysaccharide Psl is regulated transcriptionally by RpoS and post-transcriptionally by RsmA. Mol Microbiol 78 : 158– 172.[PubMed] [CrossRef]
39. 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]
40. Petrova OE,, Sauer K . 2010. The novel two-component regulatory system BfiSR regulates biofilm development by controlling the small RNA rsmZ through CafA. J Bacteriol 192 : 5275– 5288.[PubMed] [CrossRef]
41. Petrova OE,, Sauer K . 2011. SagS contributes to the motile-sessile switch and acts in concert with BfiSR to enable Pseudomonas aeruginosa biofilm formation. J Bacteriol 193 : 6614– 6628.[PubMed] [CrossRef]
42. 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]
43. 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]
44. Nilsson M,, Chiang WC,, Fazli M,, Gjermansen M,, Givskov M,, Tolker-Nielsen T . 2011. Influence of putative exopolysaccharide genes on Pseudomonas putida KT2440 biofilm stability. Environ Microbiol 13 : 1357– 1369.[PubMed] [CrossRef]
45. Matsukawa M,, Greenberg EP . 2004. Putative exopolysaccharide synthesis genes influence Pseudomonas aeruginosa biofilm development. J Bacteriol 186 : 4449– 4456.[PubMed] [CrossRef]
46. Wozniak DJ,, Wyckoff TJ,, Starkey M,, Keyser R,, Azadi P,, O’Toole GA,, Parsek MR . 2003. Alginate is not a significant component of the extracellular polysaccharide matrix of PA14 and PAO1 Pseudomonas aeruginosa biofilms. Proc Natl Acad Sci USA 100 : 7907– 7912.[PubMed] [CrossRef]
47. Klausen M,, Heydorn A,, Ragas P,, Lambertsen L,, Aaes-Jorgensen A,, Molin S,, Tolker-Nielsen T . 2003. Biofilm formation by Pseudomonas aeruginosa wild type, flagella and type IV pili mutants. Mol Microbiol 48 : 1511– 1524.[PubMed] [CrossRef]
48. Nielsen AT,, Tolker-Nielsen T,, Barken KB,, Molin S . 2000. Role of commensal relationships on the spatial structure of a surface-attached microbial consortium. Environ Microbiol 2 : 59– 68.[PubMed] [CrossRef]
49. Wolfaardt GM,, Lawrence JR,, Robarts RD,, Caldwell SJ,, Caldwell DE . 1994. Multicellular organization in a degradative biofilm community. Appl Environ Microbiol 60 : 434– 446.[PubMed]
50. 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]
51. 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.[PubMed] [CrossRef]
52. Hoiby N . 1974. Pseudomonas aeruginosa infection in cystic fibrosis. Relationship between mucoid strains of Pseudomonas aeruginosa and the humoral immune response. Acta Pathol Microbiol Scand B Microbiol Immunol 82 : 551– 558.[PubMed] [CrossRef]
53. O’Toole GA,, Kolter R . 1998. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol 30 : 295– 304.[PubMed] [CrossRef]
54. Vallet I,, Olson JW,, Lory S,, Lazdunski A,, Filloux A . 2001. The chaperone/usher pathways of Pseudomonas aeruginosa: identification of fimbrial gene clusters (cup) and their involvement in biofilm formation. Proc Natl Acad Sci USA 98 : 6911– 6916.[PubMed] [CrossRef]
55. Dueholm MS,, Sondergaard MT,, Nilsson M,, Christiansen G,, Stensballe A,, Overgaard MT,, Givskov M,, Tolker-Nielsen T,, Otzen DE,, Nielsen PH . 2013. Expression of Fap amyloids in Pseudomonas aeruginosa, P. fluorescens, and P. putida results in aggregation and increased biofilm formation. Microbiologyopen 2 : 365– 382.[PubMed] [CrossRef]
56. Tielker D,, Hacker S,, Loris R,, Strathmann M,, Wingender J,, Wilhelm S,, Rosenau F,, Jaeger KE . 2005. Pseudomonas aeruginosa lectin LecB is located in the outer membrane and is involved in biofilm formation. Microbiology 151 : 1313– 1323.[PubMed] [CrossRef]
57. Diggle SP,, Stacey RE,, Dodd C,, Camara M,, Williams P,, Winzer K . 2006. The galactophilic lectin, LecA, contributes to biofilm development in Pseudomonas aeruginosa . Environ Microbiol 8 : 1095– 1104.[PubMed] [CrossRef]
58. 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.[PubMed] [CrossRef]
59. Murakawa T . 1973. Slime production by Pseudomonas aeruginosa. IV. Chemical analysis of two varieties of slime produced by Pseudomonas aeruginosa . Jpn J Microbiol 17 : 513– 520.[PubMed] [CrossRef]
60. Murakawa T . 1973. Slime production by Pseudomonas aeruginosa. III. Purification of slime and its physicochemical properties. Jpn J Microbiol 17 : 273– 281.[PubMed] [CrossRef]
61. Costerton JW,, Stewart PS,, Greenberg EP . 1999. Bacterial biofilms: a common cause of persistent infections. Science 284 : 1318– 1322.[PubMed] [CrossRef]
62. Ciofu O,, Tolker-Nielsen T, . 2010. Antibiotic tolerance and resistance in biofilms, p 215– 230. In Høiby N,, Jensen PØ,, Moser C (ed), Biofilm Infections. Springer, New York. [CrossRef]
63. Mah TF,, Pitts B,, Pellock B,, Walker GC,, Stewart PS,, O’Toole GA . 2003. A genetic basis for Pseudomonas aeruginosa biofilm antibiotic resistance. Nature 426 : 306– 310.[PubMed] [CrossRef]
64. Hentzer M,, Eberl L,, Givskov M . 2005. Transcriptome analysis of Pseudomonas aeruginosa biofilm development: anaerobic respiration and iron limitation. Biofilms 2 : 37– 61.[CrossRef]
65. Chiang WC,, Nilsson M,, Jensen PO,, Hoiby N,, Nielsen TE,, Givskov M,, Tolker-Nielsen T . 2013. Extracellular DNA shields against aminoglycosides in Pseudomonas aeruginosa biofilms. Antimicrob Agents Chemother 57 : 2352– 2361.[PubMed] [CrossRef]
66. 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.[PubMed] [CrossRef]
67. 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]
68. 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.[PubMed] [CrossRef]
69. 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.[PubMed] [CrossRef]
70. Diggle SP,, Winzer K,, Chhabra SR,, Worrall KE,, Camara M,, Williams P . 2003. The Pseudomonas aeruginosa quinolone signal molecule overcomes the cell density-dependency of the quorum sensing hierarchy, regulates rhl-dependent genes at the onset of stationary phase and can be produced in the absence of LasR. Mol Microbiol 50 : 29– 43.[PubMed] [CrossRef]
71. Haussler S,, Becker T . 2008. The pseudomonas quinolone signal (PQS) balances life and death in Pseudomonas aeruginosa populations. PLoS Pathog 4 : e1000166. doi:10.1371/journal.ppat.1000166. [PubMed] [CrossRef]
72. Davey ME,, Caiazza NC,, O’Toole GA . 2003. Rhamnolipid surfactant production affects biofilm architecture in Pseudomonas aeruginosa PAO1. J Bacteriol 185 : 1027– 1036.[PubMed] [CrossRef]
73. Boles BR,, Thoendel M,, Singh PK . 2005. Rhamnolipids mediate detachment of Pseudomonas aeruginosa from biofilms. Mol Microbiol 57 : 1210– 1223.[PubMed] [CrossRef]
74. Pamp SJ,, Tolker-Nielsen T . 2007. Multiple roles of biosurfactants in structural biofilm development by Pseudomonas aeruginosa . J Bacteriol 189 : 2531– 2539.[PubMed] [CrossRef]
75. Winzer K,, Falconer C,, Garber NC,, Diggle SP,, Camara M,, Williams P . 2000. The Pseudomonas aeruginosa lectins PA-IL and PA-IIL are controlled by quorum sensing and by RpoS. J Bacteriol 182 : 6401– 6411.[PubMed] [CrossRef]
76. Banin E,, Vasil ML,, Greenberg EP . 2005. Iron and Pseudomonas aeruginosa biofilm formation. Proc Natl Acad Sci USA 102 : 11076– 11081.[PubMed] [CrossRef]
77. Heydorn A,, Ersboll B,, Kato J,, Hentzer M,, Parsek MR,, Tolker-Nielsen T,, Givskov M,, Molin S . 2002. Statistical analysis of Pseudomonas aeruginosa biofilm development: impact of mutations in genes involved in twitching motility, cell-to-cell signaling, and stationary-phase sigma factor expression. Appl Environ Microbiol 68 : 2008– 2017.[PubMed] [CrossRef]
78. Inhülsen S,, Aguilar C,, Schmid N,, Suppiger A,, Riedel K,, Eberl L . 2012. Identification of functions linking quorum sensing with biofilm formation in Burkholderia cenocepacia H111. Microbiologyopen 1 : 225– 242.[PubMed] [CrossRef]
79. Schmid N,, Pessi G,, Deng Y,, Aguilar C,, Carlier AL,, Grunau A,, Omasits U,, Zhang LH,, Ahrens CH,, Eberl L . 2012. The AHL- and BDSF-dependent quorum sensing systems control specific and overlapping sets of genes in Burkholderia cenocepacia H111. PLoS One 7 : e49966. doi:10.1371/journal.pone.0049966. [PubMed] [CrossRef]
80. McCarthy Y,, Yang L,, Twomey KB,, Sass A,, Tolker-Nielsen T,, Mahenthiralingam E,, Dow JM,, Ryan RP . 2010. A sensor kinase recognizing the cell-cell signal BDSF (cis-2-dodecenoic acid) regulates virulence in Burkholderia cenocepacia . Mol Microbiol 77 : 1220– 1236.[PubMed] [CrossRef]
81. O’Toole G,, Kaplan HB,, Kolter R . 2000. Biofilm formation as microbial development. Annu Rev Microbiol 54 : 49– 79.[PubMed] [CrossRef]
82. Costerton JW,, Lewandowski Z,, Caldwell DE,, Korber DR,, Lappin-Scott HM . 1995. Microbial biofilms. Annu Rev Microbiol 49 : 711– 745.[PubMed] [CrossRef]
83. Pamp SJ,, Gjermansen M,, Johansen HK,, Tolker-Nielsen T . 2008. Tolerance to the antimicrobial peptide colistin in Pseudomonas aeruginosa biofilms is linked to metabolically active cells, and depends on the pmr and mexAB-oprM genes. Mol Microbiol 68 : 223– 240.[PubMed] [CrossRef]
84. 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.[PubMed] [CrossRef]
85. Harmsen M,, Yang L,, Pamp SJ,, Tolker-Nielsen T . 2010. An update on Pseudomonas aeruginosa biofilm formation, tolerance, and dispersal. FEMS Immunol Med Microbiol 59 : 253– 268.[PubMed] [CrossRef]
86. 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]
87. Waite RD,, Papakonstantinopoulou A,, Littler E,, Curtis MA . 2005. Transcriptome analysis of Pseudomonas aeruginosa growth: comparison of gene expression in planktonic cultures and developing and mature biofilms. J Bacteriol 187 : 6571– 6576.[PubMed] [CrossRef]
88. Folsom JP,, Richards L,, Pitts B,, Roe F,, Ehrlich GD,, Parker A,, Mazurie A,, Stewart PS . 2010. Physiology of Pseudomonas aeruginosa in biofilms as revealed by transcriptome analysis. BMC Microbiol 10 : 294. [PubMed] [CrossRef]
89. Redfield RJ . 2002. Is quorum sensing a side effect of diffusion sensing? Trends Microbiol 10 : 365– 370.[PubMed] [CrossRef]
90. Lopez-Sanchez A,, Jimenez-Fernandez A,, Calero P,, Gallego LD,, Govantes F . 2013. New methods for the isolation and characterization of biofilm-persistent mutants in Pseudomonas putida . Environ Microbiol Rep 5 : 679– 685.[PubMed]
91. Navarro MV,, Newell PD,, Krasteva PV,, Chatterjee D,, Madden DR,, O’Toole GA,, Sondermann H . 2011. Structural basis for c-di-GMP-mediated inside-out signaling controlling periplasmic proteolysis. PLoS Biol 9 : e1000588. doi:10.1371/journal.pbio.1000588. [PubMed] [CrossRef]
92. 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]

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