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Pseudomonas aeruginosa Biofilm, a Programmed Bacterial Life for Fitness

  • Lee, Keehoon (Department of Microbiology and Immunology, Yonsei University College of Medicine) ;
  • Yoon, Sang Sun (Department of Microbiology and Immunology, Yonsei University College of Medicine)
  • Received : 2016.11.21
  • Accepted : 2017.03.17
  • Published : 2017.06.28

Abstract

A biofilm is a community of microbes that typically inhabit on surfaces and are encased in an extracellular matrix. Biofilms display very dissimilar characteristics to their planktonic counterparts. Biofilms are ubiquitous in the environment and influence our lives tremendously in both positive and negative ways. Pseudomonas aeruginosa is a bacterium known to produce robust biofilms. P. aeruginosa biofilms cause severe problems in immunocompromised patients, including those with cystic fibrosis or wound infection. Moreover, the unique biofilm properties further complicate the eradication of the biofilm infection, leading to the development of chronic infections. In this review, we discuss the history of biofilm research and general characteristics of bacterial biofilms. Then, distinct features pertaining to each stage of P. aeruginosa biofilm development are highlighted. Furthermore, infections caused by biofilms on their own or in association with other bacterial species (i.e., multispecies biofilms) are discussed in detail.

Acknowledgement

Supported by : National Research Foundation (NRF)

References

  1. Henrici AT. 1933. Studies of freshwater bacteria: i. a direct microscopic technique. J. Bacteriol. 25: 277-287.
  2. ZoBell CE. 1943. The effect of solid surfaces upon bacterial activity. J. Bacteriol. 46: 39-56.
  3. Mack WE. 1975. Microbial film development in a trickling filter. Microb. Ecol. 2: 215-226. https://doi.org/10.1007/BF02010441
  4. Geesey GG, Richardson WT, Yeomans HG, Irvin RT, Costerton JW. 1978. Microscopic examination of natural sessile bacterial populations from an alpine stream. Can. J. Microbiol. 23: 1733-1736.
  5. Hall-Stoodley L, Costerton JW, Stoodley P. 2004. Bacterial biofilms: from the natural environment to infectious diseases. Nat. Rev. Microbiol. 2: 95-108. https://doi.org/10.1038/nrmicro821
  6. Costerton JW, Lewandowski Z, DeBeer D, Caldwell D, Korber D, James G. 1994. Biofilms, the customized microniche. J. Bacteriol. 176: 2137-2142. https://doi.org/10.1128/jb.176.8.2137-2142.1994
  7. Latifi A, Winson MK, Foglino M, Bycroft BW, Stewart GS, Lazdunski A, et al. 1995. Multiple homologues of LuxR and LuxI control expression of virulence determinants and secondary metabolites through quorum sensing in Pseudomonas aeruginosa PAO1. Mol. Microbiol. 17: 333-343. https://doi.org/10.1111/j.1365-2958.1995.mmi_17020333.x
  8. Pearson JP, Pesci EC, Iglewski BH. 1997. Roles of Pseudomonas aeruginosa las and rhl quorum-sensing systems in control of elastase and rhamnolipid biosynthesis genes. J. Bacteriol. 179: 5756-5767. https://doi.org/10.1128/jb.179.18.5756-5767.1997
  9. O'Toole G, Kaplan HB, Kolter R. 2000. Biofilm formation as microbial development. Annu. Rev. Microbiol. 54: 49-79. https://doi.org/10.1146/annurev.micro.54.1.49
  10. Wei Q, Ma LZ. 2013. Biofilm matrix and its regulation in Pseudomonas aeruginosa. Int. J. Mol. Sci. 14: 20983-21005. https://doi.org/10.3390/ijms141020983
  11. Costerton JW, Stewart PS, Greenberg EP. 1999. Bacterial biofilms: a common cause of persistent infections. Science 21: 1318-1322.
  12. Donlan RM. 2002. Biofilms: microbial life on surfaces. Emerg. Infect. Dis. 8: 881-890. https://doi.org/10.3201/eid0809.020063
  13. Flemming HC. 2002. Biofouling in water systems: cases, causes and countermeasures. Appl. Microbiol. Biotechnol. 59: 629-640. https://doi.org/10.1007/s00253-002-1066-9
  14. Carpentier B, Cerf O. 1993. Biofilms and their consequences, with particular reference to hygiene in the food industry. J. Appl. Bacteriol. 75: 499-511. https://doi.org/10.1111/j.1365-2672.1993.tb01587.x
  15. Singh R, Paul D, Jain RK. 2006. Biofilms: implications in bioremediation. Trends Microbiol. 14: 389-397. https://doi.org/10.1016/j.tim.2006.07.001
  16. Munoz R, Guieysse B. 2006. Algal-bacterial processes for the treatment of hazardous contaminants: a review. Water Res. 40: 2799-2815. https://doi.org/10.1016/j.watres.2006.06.011
  17. Murray TS, Egan M, Kazmierczak BI. 2007. Pseudomonas aeruginosa chronic colonization in cystic fibrosis patients. Curr. Opin. Pediatr. 19: 83-88. https://doi.org/10.1097/MOP.0b013e3280123a5d
  18. Yoon SS, Hasset DJ. 2004. Chronic Pseudomonas aeruginosa infection in cystic fibrosis airway disease: metabolic changes that unravel novel drug targets. Expert Rev. Anti- Infect. Ther. 2: 611-623. https://doi.org/10.1586/14787210.2.4.611
  19. Rieber N, Brand A, Hector A, Graepler-Mainka U, Ost M, Schafer I, et al. 2013. Flagellin induces myeloid-derived suppressor cells: implications for Pseudomonas aeruginosa infection in cystic fibrosis lung disease. J. Immunol. 190: 1276-1284. https://doi.org/10.4049/jimmunol.1202144
  20. Hahn HP. 1997. The type-4 pilus is the major virulenceassociated adhesin of Pseudomonas aeruginosa: a review. Gene 192: 99-108. https://doi.org/10.1016/S0378-1119(97)00116-9
  21. Laarman AJ, Bardoel BW, Ruyken M, Fernie J, Milder FJ, van Strijp JA, et al. 2012. Pseudomonas aeruginosa alkaline protease blocks complement activation via the classical and lectin pathways. J. Immunol. 188: 386-393. https://doi.org/10.4049/jimmunol.1102162
  22. Braun P, Ockhuijsen C, Eppens E, Koster M, Bitter W, Tommassen J. 2001. Maturation of Pseudomonas aeruginosa elastase. Formation of the disulfide bonds. J. Biol. Chem. 276: 26030-26035. https://doi.org/10.1074/jbc.M007122200
  23. Le Berre R, Nguyen S, Nowak E, Kipnis E, Pierre M, Quenee L, et al. 2011. Relative contribution of three main virulence factors in Pseudomonas aeruginosa pneumonia. Crit. Care Med. 39: 2113-2120. https://doi.org/10.1097/CCM.0b013e31821e899f
  24. Wargo MJ, Gross MJ, Rajamani S, Allard JL, Lundblad LKA, Allen GB, et al. 2011. Hemolytic phospholipase C inhibition protects lung function during Pseudomonas aeruginosa infection. Am. J. Respir. Crit. Care Med. 184: 345-354. https://doi.org/10.1164/rccm.201103-0374OC
  25. Ramachandran G. 2014. Gram-positive and gram-negative bacterial toxins in sepsis: a brief review. Virulence 5: 213-218. https://doi.org/10.4161/viru.27024
  26. Llamas MA, Sparrius M, Kloet R, Jimenez CR, Vandenbroucke-Grauls C, Bitter W. 2006. The heterologous siderophores ferrioxamine B and ferrichrome activate signaling pathways in Pseudomonas aeruginosa. J. Bacteriol. 188: 1882-1891. https://doi.org/10.1128/JB.188.5.1882-1891.2006
  27. 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. https://doi.org/10.1111/j.1365-2958.2009.06934.x
  28. Sharma G, Rao S, Bansal A, Dang S, Gupta S, Gabrani R. 2014. Pseudomonas aeruginosa biofilm: potential therapeutic targets. Biologicals 42: 1-7. https://doi.org/10.1016/j.biologicals.2013.11.001
  29. Gellatly SL, Hancock RE. 2013. Pseudomonas aeruginosa: new insights into pathogenesis and host defenses. Pathog. Dis. 67: 159-173. https://doi.org/10.1111/2049-632X.12033
  30. Romling U, Balsalobre C. 2012. Biofilm infections, their resilience to therapy and innovative treatment strategies. J. Intern. Med. 272: 541-561. https://doi.org/10.1111/joim.12004
  31. Mulcahy LR, Burns JL, Lory S, Lewis K. 2010. Emergence of Pseudomonas aeruginosa strains producing high levels of persister cells in patients with cystic fibrosis. J. Bacteriol. 192: 6191-6199. https://doi.org/10.1128/JB.01651-09
  32. Rybtke MT, Jensen PO, Hoiby N, Givskov M, Tolker Nielsen T, Bjarnsholt T. 2011. The implication of Pseudomonas aeruginosa biofilms in infections. Inflamm. Allergy Drug Targets 10: 141-157. https://doi.org/10.2174/187152811794776222
  33. Hengzhuang W, Wu H, Ciofu O, Song Z, Hoiby N. 2012. In vivo pharmacokinetics/pharmacodynamics of colistin and imipenem in Pseudomonas aeruginosa biofilm infection. Antimicrob. Agents Chemother. 56: 2683-2690. https://doi.org/10.1128/AAC.06486-11
  34. Tolker-Nielsen T. 2015. Biofilm development. Microbiol. Spectr. 3: MB-0001-2014.
  35. 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. https://doi.org/10.1111/j.1365-2958.2009.06793.x
  36. Tischler AD, Camilli A. 2004. Cyclic diguanylate (c-di-GMP) regulates Vibrio cholerae biofilm formation. Mol. Microbiol. 53: 857-869. https://doi.org/10.1111/j.1365-2958.2004.04155.x
  37. 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. https://doi.org/10.1111/j.1365-2958.2006.05106.x
  38. 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. https://doi.org/10.1073/pnas.0507170102
  39. Kulasakara H, Lee V, Brencic A, Liberati N, Urbach J, Miyata S, et al. 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. https://doi.org/10.1073/pnas.0511090103
  40. 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. https://doi.org/10.1111/mmi.12013
  41. 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. https://doi.org/10.1111/j.1365-2958.2009.06991.x
  42. Chambers JR, Sauer K. 2013. Small RNAs and their role in biofilm formation. Trends Microbiol. 21: 39-49. https://doi.org/10.1016/j.tim.2012.10.008
  43. Petrova OE, Sauer K. 2009. A novel signaling network essential for regulating Pseudomonas aeruginosa biofilm development. PLoS Pathog. 5: e1000668. https://doi.org/10.1371/journal.ppat.1000668
  44. Petrova OE, Sauer K. 2011. SagS contributes to the motilesessile switch and acts in concert with BfiSR to enable Pseudomonas aeruginosa biofilm formation. J. Bacteriol. 193: 6614-6628. https://doi.org/10.1128/JB.00305-11
  45. Kim SK, Lee JH. 2016. Biofilm dispersion in Pseudomonas aeruginosa. J. Microbiol. 54: 71-85. https://doi.org/10.1007/s12275-016-5528-7
  46. 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. https://doi.org/10.1111/j.1574-695X.2010.00690.x
  47. Fullagar JL, Garner AL, Struss AK, Day JA, Martin DP, Yu J, et al. 2013. Antagonism of a zinc metalloprotease using a unique metal-chelating scaffold: tropolones as inhibitors of P. aeruginosa elastase. Chem. Commun. (Camb.). 49: 3197-3199. https://doi.org/10.1039/c3cc41191e
  48. Oglesby-Sherrouse AG, Djapgne L, Nguyen AT, Vasil AI, Vasil ML. 2014. The complex interplay of iron, biofilm formation, and mucoidy affecting antimicrobial resistance of Pseudomonas aeruginosa. Pathog. Dis. 70: 307-320. https://doi.org/10.1111/2049-632X.12132
  49. Calfee MW, Coleman JP, Pesci EC. 2001. Interference with Pseudomonas quinolone signal synthesis inhibits virulence factor expression by Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 98: 11633-11637. https://doi.org/10.1073/pnas.201328498
  50. Ryder C, Byrd M, Wozniak DJ. 2007. Role of polysaccharides in Pseudomonas aeruginosa biofilm development. Curr. Opin. Microbiol. 10: 644-648. https://doi.org/10.1016/j.mib.2007.09.010
  51. 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. https://doi.org/10.1128/JB.186.14.4466-4475.2004
  52. 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. https://doi.org/10.1128/JB.186.14.4457-4465.2004
  53. 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. https://doi.org/10.1111/j.1462-2920.2011.02503.x
  54. Yang L, Hengzhuang W, Wu H, Damkiaer S, Jochumsen N, Song Z, et al. 2012. Polysaccharides serve as scaffold of biofilms formed by mucoid Pseudomonas aeruginosa. FEMS Immunol. Med. Microbiol. 65: 366-376. https://doi.org/10.1111/j.1574-695X.2012.00936.x
  55. Wang S, Liu X, Liu H, Zhang L, Guo Y, Yu S, et al. 2015. The exopolysaccharide Psl-eDNA interaction enables the formation of a biofilm skeleton in Pseudomonas aeruginosa. Environ. Microbiol. Rep. 7: 330-340. https://doi.org/10.1111/1758-2229.12252
  56. Vasseur P, Vallet-Gely I, Soscia C, Genin S, Filloux A. 2005. The pel genes of the Pseudomonas aeruginosa PAK strain are involved at early and late stages of biofilm formation. Microbiology 151: 985-997. https://doi.org/10.1099/mic.0.27410-0
  57. Colvin KM, Gordon VD, Murakami K, Borlee BR, Wozniak DJ, Wong GC, et al. 2011. The Pel polysaccharide can serve a structural and protective role in the biofilm matrix of Pseudomonas aeruginosa. PLoS Pathog. 7: e1001264. https://doi.org/10.1371/journal.ppat.1001264
  58. Jennings LK, Storek KM, Ledvina HE, Coulon C, Marmont LS, Sadovskaya I, et al. 2015. Pel is a cationic exopolysaccharide that cross-links extracellular DNA in the Pseudomonas aeruginosa biofilm matrix. Proc. Natl. Acad. Sci. USA 112: 11353-11358. https://doi.org/10.1073/pnas.1503058112
  59. Baker P, Hill PJ, Snarr BD, Alnabelseya N, Pestrak MJ, Lee MJ, et al. 2016. Exopolysaccharide biosynthetic glycoside hydrolases can be utilized to disrupt and prevent Pseudomonas aeruginosa biofilms. Sci. Adv. 2: e1501632. https://doi.org/10.1126/sciadv.1501632
  60. Wozniak DJ, Wyckoff TJ, Starkey M, Keyser R, Azadi P, O'Toole GA, et al. 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. https://doi.org/10.1073/pnas.1231792100
  61. Bagge N, Schuster M, Hentzer M, Ciofu O, Givskov M, Greenberg EP, et al. 2004. Pseudomonas aeruginosa biofilms exposed to imipenem exhibit changes in global gene expression and ${\beta}$-lactamase and alginate production. Antimicrob. Agents Chemother. 48: 1175-1187. https://doi.org/10.1128/AAC.48.4.1175-1187.2004
  62. Hoiby N, Bjarnsholt T, Givskov M, Molin S, Ciofu O. 2010. Antibiotic resistance of bacterial biofilms. Int. J. Antimicrob. Agents 35: 322-332. https://doi.org/10.1016/j.ijantimicag.2009.12.011
  63. Leid JG, Willson CJ, Shirtliff ME, Hassett DJ, Parsek MR, Jeffers AK. 2005. The exopolysaccharide alginate protects Pseudomonas aeruginosa biofilm bacteria from IFN-${\gamma}$- mediated macrophage killing. J. Immunol. 175: 7512-7518. https://doi.org/10.4049/jimmunol.175.11.7512
  64. 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. Microbiol. 59: 1114-1128. https://doi.org/10.1111/j.1365-2958.2005.05008.x
  65. Mulcahy H, Charron-Mazenod L, Lewenza S. 2010. Pseudomonas aeruginosa produces an extracellular deoxyribonuclease that is required for utilization of DNA as a nutrient source. Environ. Microbiol. 12: 1621-1629.
  66. Tseng BS, Zhang W, Harrison JJ, Quach TP, Song JL, Penterman J, et al. 2013. The extracellular matrix protects Pseudomonas aeruginosa biofilms by limiting the penetration of tobramycin. Environ. Microbiol. 15: 2865-2878.
  67. Drenkard E, Ausubel FM. 2002. Pseudomonas biofilm formation and antibiotic resistance are linked to phenotypic variation. Nature 416: 740-743. https://doi.org/10.1038/416740a
  68. Fuxman Bass JI, Russo DM, Gabelloni ML, Geffner JR, Giordano M, Catalano M, et al. 2010. Extracellular DNA: a major proinflammatory component of Pseudomonas aeruginosa biofilms. J. Immunol. 184: 6386-6395. https://doi.org/10.4049/jimmunol.0901640
  69. O'Toole GA, Kolter R. 1998. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol. 30: 295-304. https://doi.org/10.1046/j.1365-2958.1998.01062.x
  70. Skerker JM, Berg HC. 2001. Direct observation of extension and retraction of type IV pili. Proc. Natl. Acad. Sci. USA 98: 6901-6904. https://doi.org/10.1073/pnas.121171698
  71. Ruer S, Stender S, Filloux A, de Bentzmann S. 2007. Assembly of fimbrial structures in Pseudomonas aeruginosa: functionality and specificity of chaperone-usher machineries. J. Bacteriol. 189: 3547-3555. https://doi.org/10.1128/JB.00093-07
  72. Juhas M, Eberl L, Tummler B. 2005. Quorum sensing: the power of cooperation in the world of Pseudomonas. Environ. Microbiol. 7: 459-471. https://doi.org/10.1111/j.1462-2920.2005.00769.x
  73. Fuqua C, Greenberg EP. 2002. Listening in on bacteria: acyl-homoserine lactone signalling. Nat. Rev. Mol. Cell Biol. 3: 685-695. https://doi.org/10.1038/nrm907
  74. 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. https://doi.org/10.1126/science.280.5361.295
  75. Wagner VE, Gillis RJ, Iglewski BH. 2004. Transcriptome analysis of quorum-sensing regulation and virulence factor expression in Pseudomonas aeruginosa. Vaccine 22 Suppl 1: S15-S20. https://doi.org/10.1016/j.vaccine.2004.08.011
  76. Lee J, Zhang L. 2015. The hierarchy quorum sensing network in Pseudomonas aeruginosa. Protein Cell 6: 26-41. https://doi.org/10.1007/s13238-014-0100-x
  77. Schuster M, Greenberg EP. 2006. A network of networks: quorum-sensing gene regulation in Pseudomonas aeruginosa. Int. J. Med. Microbiol. 296: 73-81. https://doi.org/10.1016/j.ijmm.2006.01.036
  78. Patriquin GM, Banin E, Gilmour C, Tuchman R, Greenberg EP, Poole K. 2008. Influence of quorum sensing and iron on twitching motility and biofilm formation in Pseudomonas aeruginosa. J. Bacteriol. 190: 662-671. https://doi.org/10.1128/JB.01473-07
  79. Wade DS, Calfee MW, Rocha ER, Ling EA, Engstrom E, Coleman JP, et al. 2005. Regulation of Pseudomonas quinolone signal synthesis in Pseudomonas aeruginosa. J. Bacteriol. 187: 4372-4380. https://doi.org/10.1128/JB.187.13.4372-4380.2005
  80. Haussler S, Becker T. 2008. The Pseudomonas quinolone signal (PQS) balances life and death in Pseudomonas aeruginosa populations. PLoS Pathog. 4: e1000166. https://doi.org/10.1371/journal.ppat.1000166
  81. Pamp SJ, Tolker-Nielsen T. 2007. Multiple roles of biosurfactants in structural biofilm development by Pseudomonas aeruginosa. J. Bacteriol. 189: 2531-2539. https://doi.org/10.1128/JB.01515-06
  82. Senturk S, Ulusoy S, Bosgelmez-Tinaz G, Yagci A. 2012. Quorum sensing and virulence of Pseudomonas aeruginosa during urinary tract infections. J. Infect. Dev. Ctries 6: 501-507.
  83. Inaba T, Oura H, Morinaga K, Toyofuku M, Nomura N. 2015. The Pseudomonas quinolone signal inhibits biofilm development of Streptococcus mutans. Microbes Environ. 30: 189-191. https://doi.org/10.1264/jsme2.ME14140
  84. Reen FJ, Mooij MJ, Holcombe LJ, McSweeney CM, McGlacken GP, Morrissey JP, et al. 2011. The Pseudomonas quinolone signal (PQS), and its precursor HHQ, modulate interspecies and interkingdom behaviour. FEMS Microbiol. Ecol. 77: 413-428. https://doi.org/10.1111/j.1574-6941.2011.01121.x
  85. Lee J, Wu J, Deng Y, Wang J, Wang C, Wang J, et al. 2013. A cell-cell communication signal integrates quorum sensing and stress response. Nat. Chem. Biol. 9: 406.
  86. Dekimpe V, Deziel E. 2009. Revisiting the quorum-sensing hierarchy in Pseudomonas aeruginosa: the transcriptional regulator RhlR regulates LasR-specific factors. Microbiology 155: 712-723. https://doi.org/10.1099/mic.0.022764-0
  87. Jensen V, Lons D, Zaoui C, Bredenbruch F, Meissner A, Dieterich G, et al. 2006. RhlR expression in Pseudomonas aeruginosa is modulated by the Pseudomonas quinolone signal via PhoB-dependent and -independent pathways. J. Bacteriol. 188: 8601-8606. https://doi.org/10.1128/JB.01378-06
  88. Schafhauser J, Lepine F, McKay G, Ahlgren HG, Khakimova M, Nguyen D. 2014. The stringent response modulates 4-hydroxy-2-alkylquinoline biosynthesis and quorum-sensing hierarchy in Pseudomonas aeruginosa. J. Bacteriol. 196: 1641-1650. https://doi.org/10.1128/JB.01086-13
  89. Oglesby AG, Farrow JM 3rd, Lee JH, Tomaras AP, Greenberg EP, Pesci EC, et al. 2008. The influence of iron on Pseudomonas aeruginosa physiology: a regulatory link between iron and quorum sensing. J. Biol. Chem. 283: 15558-15567. https://doi.org/10.1074/jbc.M707840200
  90. Donlan RM. 2001. Biofilms and device-associated infections. Emerg. Infect. Dis. 7: 277-281. https://doi.org/10.3201/eid0702.010226
  91. Stewart PS. 1996. Theoretical aspects of antibiotic diffusion into microbial biofilms. Antimicrob. Agents Chemother. 40: 2517-2522.
  92. Nguyen D, Joshi-Datar A, Lepine F, Bauerle E, Olakanmi O, Beer K, et al. 2011. Active starvation responses mediate antibiotic tolerance in biofilms and nutrient-limited bacteria. Science 334: 982-986. https://doi.org/10.1126/science.1211037
  93. Sadovskaya I, Vinogradov E, Li J, Hachani A, Kowalska K, Filloux A. 2010. High-level antibiotic resistance in Pseudomonas aeruginosa biofilm: the ndvB gene is involved in the production of highly glycerol-phosphorylated beta-(1->3)-glucans, which bind aminoglycosides. Glycobiology 20: 895-904. https://doi.org/10.1093/glycob/cwq047
  94. Zhang L, Mah TF. 2008. Involvement of a novel efflux system in biofilm-specific resistance to antibiotics. J. Bacteriol. 190: 4447-4452. https://doi.org/10.1128/JB.01655-07
  95. Mah TF. 2012. Regulating antibiotic tolerance within biofilm microcolonies. J. Bacteriol. 194: 4791-4792. https://doi.org/10.1128/JB.01187-12
  96. Chen M, Yu Q, Sun H. 2013. Novel strategies for the prevention and treatment of biofilm related infections. Int. J. Mol. Sci. 14: 18488-18501. https://doi.org/10.3390/ijms140918488
  97. Yoon SS, Hennigan RF, Hilliard GM, Ochsner UA, Parvatiyar K, Kamani MC, et al. 2002. Pseudomonas aeruginosa anaerobic respiration in biofilms: relationships to cystic fibrosis pathogenesis. Dev. Cell 3: 593-603. https://doi.org/10.1016/S1534-5807(02)00295-2
  98. Tolker-Nielsen T. 2014. Pseudomonas aeruginosa biofilm infections: from molecular biofilm biology to new treatment possibilities. APMIS Suppl. 122: 1-51.
  99. Burmolle M, Thomsen TR, Fazli M, Dige I, Christensen L, Homoe P, et al. 2010. Biofilms in chronic infections - a matter of opportunity - monospecies biofilms in multispecies infections. FEMS Immunol. Med. Microbiol. 59: 324-336. https://doi.org/10.1111/j.1574-695X.2010.00714.x
  100. Eming SA, Krieg T, Davidson JM. 2007. Inflammation in wound repair: molecular and cellular mechanisms. J. Invest. Dermatol. 127: 514-525. https://doi.org/10.1038/sj.jid.5700701
  101. Pastar I, Nusbaum AG, Gil J, Patel SB, Chen J, Valdes J, et al. 2013. Interactions of methicillin resistant Staphylococcus aureus USA300 and Pseudomonas aeruginosa in polymicrobial wound infection. PLoS One 8: e56846. https://doi.org/10.1371/journal.pone.0056846
  102. Banu A, Noorul Hassan MM, Rajkumar J, Srinivasa S. 2015. Spectrum of bacteria associated with diabetic foot ulcer and biofilm formation: a prospective study. Australas. Med. J. 8: 280-285.
  103. Wolcott R, Costerton JW, Raoult D, Cutler SJ. 2013. The polymicrobial nature of biofilm infection. Clin. Microbiol. Infect. 19: 107-112. https://doi.org/10.1111/j.1469-0691.2012.04001.x
  104. Peters BM, Jabra-Rizk MA, O'May GA, Costerton JW, Shirtliff ME. 2012. Polymicrobial interactions: impact on pathogenesis and human disease. Clin. Microbiol. Rev. 25: 193-213. https://doi.org/10.1128/CMR.00013-11
  105. Harriott MM, Noverr MC. 2009. Candida albicans and Staphylococcus aureus form polymicrobial biofilms: effects on antimicrobial resistance. Antimicrob. Agents Chemother. 53: 3914-3922. https://doi.org/10.1128/AAC.00657-09
  106. Colombo AV, Barbosa GM, Higashi D, di Micheli G, Rodrigues PH, Simionato MR. 2013. Quantitative detection of Staphylococcus aureus, Enterococcus faecalis and Pseudomonas aeruginosa in human oral epithelial cells from subjects with periodontitis and periodontal health. J. Med. Microbiol. 62: 1592-1600. https://doi.org/10.1099/jmm.0.055830-0
  107. Waters CM, Bassler BL. 2005. Quorum sensing: cell-to-cell communication in bacteria. Annu. Rev. Cell Dev. Biol. 21: 319-346. https://doi.org/10.1146/annurev.cellbio.21.012704.131001
  108. Federle MJ. 2009. Autoinducer-2-based chemical communication in bacteria: complexities of interspecies signaling. Contrib. Microbiol. 16: 18-32.
  109. Rickard AH, Palmer RJ Jr, Blehert DS, Campagna SR, Semmelhack MF, Egland PG, et al. 2006. Autoinducer 2: a concentration-dependent signal for mutualistic bacterial biofilm growth. Mol. Microbiol. 60: 1446-1456. https://doi.org/10.1111/j.1365-2958.2006.05202.x
  110. Deng Y, Wu J, Eberl L, Zhang LH. 2010. Structural and functional characterization of diffusible signal factor family quorum-sensing signals produced by members of the Burkholderia cepacia complex. Appl. Environ. Microbiol. 76: 4675-4683. https://doi.org/10.1128/AEM.00480-10
  111. Ryan RP, Fouhy Y, Garcia BF, Watt SA, Niehaus K, Yang L, et al. 2008. Interspecies signalling via the Stenotrophomonas maltophilia diffusible signal factor influences biofilm formation and polymyxin tolerance in Pseudomonas aeruginosa. Mol. Microbiol. 68: 75-86. https://doi.org/10.1111/j.1365-2958.2008.06132.x
  112. Elias S, Banin E. 2012. Multi-species biofilms: living with friendly neighbors. FEMS Microbiol. Rev. 36: 990-1004. https://doi.org/10.1111/j.1574-6976.2012.00325.x
  113. Ghadakpour M, Bester E, Liss SN, Gardam M, Droppo I, Hota S, et al. 2014. Integration and proliferation of Pseudomonas aeruginosa PA01 in multispecies biofilms. Microb. Ecol. 68: 121-131. https://doi.org/10.1007/s00248-014-0398-1
  114. Trejo-Hernandez A, Andrade-Dominguez A, Hernandez M, Encarnacion S. 2014. Interspecies competition triggers virulence and mutability in Candida albicans-Pseudomonas aeruginosa mixed biofilms. ISME J. 8: 1974-1988. https://doi.org/10.1038/ismej.2014.53
  115. Yang L, Liu Y, Markussen T, Hoiby N, Tolker-Nielsen T, Molin S. 2011. Pattern differentiation in co-culture biofilms formed by Staphylococcus aureus and Pseudomonas aeruginosa. FEMS Immunol. Med. Microbiol. 62: 339-347. https://doi.org/10.1111/j.1574-695X.2011.00820.x
  116. Mashburn LM, Jett AM, Akins DR, Whiteley M. 2005. Staphylococcus aureus serves as an iron source for Pseudomonas aeruginosa during in vivo coculture. J. Bacteriol. 187: 554-566. https://doi.org/10.1128/JB.187.2.554-566.2005
  117. Smith K, Rajendran R, Kerr S, Lappin DF, Mackay WG, Williams C, et al. 2015. Aspergillus fumigatus enhances elastase production in Pseudomonas aeruginosa co-cultures. Med. Mycol. 53: 645-655. https://doi.org/10.1093/mmy/myv048
  118. Tsuchimor N, Hayashi R, Shino A, Yamazaki T, Okonogi K. 1994. Enterococcus faecalis aggravates pyelonephritis caused by Pseudomonas aeruginosa in experimental ascending mixed urinary tract infection in mice. Infect. Immun. 62: 4534-4541.