The Survivors of the Extreme: Bacterial Biofilms

  • Neha Dubey
  • Raja Singh
  • Aditya K. Sharma
  • Sharmila Basu-Modak
  • Yogendra Singh


Biofilms are bacteria’s way of behaving like a multi-cellular organism. Bacteria have been constantly evolving in the face of myriad natural challenges since the first life form appeared. Over the centuries, they have survived under extreme conditions by virtue of their ability to form biofilms. Biofilms have proved to be an immensely strong collaborative effort of bacteria, and this interaction is administered via their quorum-sensing mechanism. A biofilm plays a crucial role in survival, dispersal, transfer of resistance genes, and generation of diversity among bacteria. It can also act as a pathogenic factor for virulent bacteria and biofilms are often listed as the major cause of many diseases, such as endocarditis, cystic fibrosis, etc. Bacterial biofilms can be formed on almost every surface and, thus, have deleterious effects on many indwelling medical devices and industrial equipment. Many methods—from antibiotics to ultraviolet (UV) radiation—are currently being used to eliminate or reduce biofilm. However, the most effective and eco-friendly measure involves the targeting of the root phenomenon, quorum sensing. Biofilm formation and dispersal mechanisms are being studied to increase the efficiency of biofilm elimination. Despite the many harms they can pose, these biofilms have been efficiently manipulated to be used for various purposes such as wastewater treatment, microbial fuel cells, drug delivery, nanobiotechnology, etc. Biofilms bring about a very detailed level of complexity that helps for better persistence of the bacterial population and at the same time, provides us a valuable tool to address several important environmental issues. Thus, it will be appropriate to term bacterial biofilms as remarkably proficient assemblies of the life forms.


Cystic Fibrosis Transmembrane Conductance Regulator Microbial Fuel Cell Dental Plaque Acyl Homoserine Lactone Quorum Quencher 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



The authors are thankful to Dr. V.C. Kalia and Dr. Yogendra Singh for providing us the opportunity to contribute a chapter to this book. ND, RS, SK and AKS are thankful to ICMR, CSIR, and UGC for providing fellowships. We are also thankful to the Dean, Department of Zoology, Delhi University, and the Director, CSIR-IGIB for providing necessary facilities and support for this work.


  1. Albrecht MT, Schiller NL (2005) Alginate lyase (AlgL) activity is required for alginate biosynthesis in pseudomonas aeruginosa. J Bacteriol 187:3869–3872. doi: 10.1128/JB.187.11.3869-3872.2005 PubMedCentralPubMedCrossRefGoogle Scholar
  2. Amit K, Dewulf J, Wiele TV, Langenhove HV (2009) Bacterial dynamics of biofilm development during toluene degradation by Burkholderia vietnamiensis G4 in a gas phase membrane bioreactor. J Microbiol Biotechnol 19:1028–1033PubMedCrossRefGoogle Scholar
  3. Archer EJ, Robinson AB, Süel GM (2012) Engineered E. coli that detect and respond to gut inflammation through nitric oxide sensing. ACS Synth Biol 1:451–457. doi: 10.1021/sb3000595 PubMedCrossRefGoogle Scholar
  4. Bjarnsholt T, Tolker-Nielsen T, Høiby N, Givskov M (2010) Interference of Pseudomonas aeruginosa signalling and biofilm formation for infection control. Expert Rev Mol Med 12:e11. doi: 10.1017/S1462399410001420 PubMedCrossRefGoogle Scholar
  5. 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. doi: 10.1111/j.1365-2958.2009.06991.x PubMedCentralPubMedCrossRefGoogle Scholar
  6. Bowden GH, Li YH (1997) Nutritional influences on biofilm development. Adv Dent Res 11:81–99PubMedCrossRefGoogle Scholar
  7. Brackman G, Coenye T (2015) Quorum sensing inhibitors as anti-biofilm agents. Curr Pharm Des 21:5–11. doi: 10.2174/1381612820666140905114627#sthash.Z926xlPS.dpuf PubMedCrossRefGoogle Scholar
  8. Caiazza NC, O’Toole GA (2004) SadB is required for the transition from reversible to irreversible attachment during biofilm formation by Pseudomonas aeruginosa PA14. J Bacteriol 186:4476–4485. doi: 10.1128/JB.186.14.4476-4485.2004 PubMedCentralPubMedCrossRefGoogle Scholar
  9. Capodaglio AG, Molognoni D, Dallago E, Liberale A, Cella R, Longoni P, Pantaleoni L (2013) Microbial fuel cells for direct electrical energy recovery from urban wastewaters. Sci World J 2013:634738. doi: 10.1155/2013/634738 CrossRefGoogle Scholar
  10. Cardines R, Giufrè M, Pompilio A, Fiscarelli E, Ricciotti G, Di Bonaventura G, Cerquetti M (2012) Haemophilus influenzae in children with cystic fibrosis: antimicrobial susceptibility, molecular epidemiology, distribution of adhesins and biofilm formation. Int J Med Microbiol 302:45–52. doi: 10.1016/j.ijmm.2011.08.003e PubMedCrossRefGoogle Scholar
  11. Chandran P, Das N (2011) Degradation of diesel oil by immobilized Candida tropicalis and biofilm formed on gravels. Biodegradation 22:1181–1189. doi: 10.1007/s10532-011-9473-1 PubMedCrossRefGoogle Scholar
  12. Chang IS, Jang JK, Gil GC, Kim M, Kim HJ, Cho BW, Kim BH (2004) Continuous determination of biochemical oxygen demand using microbial fuel cell type biosensor. Biosens Bioelectron 19:607–613. doi: 10.1016/S0956-5663(03)00272-0 PubMedCrossRefGoogle Scholar
  13. Chen J, Yang B, Cheng X, QiaoY TB, Chen G, Wei J, Liu X, Cheng W, Du P, Huang X, JiangW HQ, Hu Y, Li J, Hua ZC (2012) Salmonella-mediated tumor-targeting TRAIL gene therapy significantly suppresses melanoma growth in mouse model. Cancer Sci 103:325–333. doi: 10.1111/j.1349-7006.2011.02147.x PubMedCrossRefGoogle Scholar
  14. Claesen J, Fischbach MA (2014) Synthetic microbes as drug delivery systems. ACS Synth Biol. doi: 10.1021/sb500258b PubMedCentralPubMedGoogle Scholar
  15. Clark Ehlers GA, Turner SJ (2012) “Chapter 6: Abstract.” Microbial biofilms current research and applications. Caister Academic Pr,. Web. 21 Jan 2012Google Scholar
  16. Cohen B (1931) The bacterial culture as an electrical half-cell. J Bacteriol 21:18–19Google Scholar
  17. Costerton JW, Geesey GG, Cheng KJ (1978) How bacteria stick? Sci Am 238:86–95PubMedCrossRefGoogle Scholar
  18. Costley SC, Wallis FM (2001) Bioremediation of heavy metals in a synthetic wastewater using a rotating biological contactor. Water Res 35:3715–3723. doi: 10.1016/S0043-1354(01)00072-0 PubMedCrossRefGoogle Scholar
  19. Cristina Q, Zelia R, Bruna F, Hugo F, Teresa T (2009) Biosorptive performance of an Escherichia coli biofilm supported on zeolite NaY for the removal of Cr(VI), Cd(II), Fe(III) and Ni(II). Chem Eng J 152:110–115. doi: 10.1016/j.cej.2009.03.039 CrossRefGoogle Scholar
  20. Darveau RP (2010) Periodontitis: a polymicrobial disruption of host homeostasis. Nat Rev Microbiol 8:481–490. doi: 10.1038/nrmicro2337 PubMedCrossRefGoogle Scholar
  21. Dasgupta D, Ghosh R, Sengupta TK (2013) Biofilm-mediated enhanced crude oil degradation by newly isolated Pseudomonas species. ISRN Biotechnol 2013:250749. doi: 10.5402/2013/250749 PubMedCentralPubMedCrossRefGoogle Scholar
  22. 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. doi: 10.1126/science.280.5361.295 PubMedCrossRefGoogle Scholar
  23. De Kievit TR, Gillis R, Marx S, Brown C, Iglewski BH (2001) Quorum-sensing genes in Pseudomonas aeruginosa biofilms: their role and expression patterns. Appl Environ Microbiol 67:1865–1873. doi: 10.1128/AEM.67.4.1865-1873.2001 PubMedCentralPubMedCrossRefGoogle Scholar
  24. de Lannoy CF, Jassby D, Gloe K, Gordon AD, Wiesner MR (2013) Aquatic biofouling prevention by electrically charged nanocomposite polymer thin film membranes. Environ Sci Technol 47:2760–2768. doi: 10.1021/es3045168 PubMedCrossRefGoogle Scholar
  25. Diels L, Spaans PH, Van Roy S, Hooyberghs L, Wouters H, Walter E, Winters J, Macaskie L, Pernfuss B, Woebking H, Pümpel T (2001) Heavy metals removal by sand filters inoculated with metal sorbing and precipitating bacteria. Biohydro metall Fundam Technol and Sustain Dev 11:317–326. doi: 10.1016/S0304-386X(03)00161-0, part BGoogle Scholar
  26. Donlan RM (2002) Biofilms: microbial life on surfaces. Emerg Infect Dis 8:881–890PubMedCentralPubMedCrossRefGoogle Scholar
  27. Donlan RM (2011) Biofilm elimination on intravascular catheters: important considerations for the infectious disease practitioner. Clin Infect Dis 52:1038–1045. doi: 10.1093/cid/cir077 PubMedCrossRefGoogle Scholar
  28. Donlan RM, Costerton JW (2002) Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 15:167–193. doi: 10.1128/CMR.15.2.167-193.2002 PubMedCentralPubMedCrossRefGoogle Scholar
  29. Donovan C, Dewan A, Heo D, Beyenal H (2008) Batteryless, wireless sensor powered by a sediment microbial fuel cell. Environ Sci Technol 42:8591–8596. doi: 10.1021/es801763g PubMedCrossRefGoogle Scholar
  30. Elkins MR, Robinson M, Rose BR, Harbour C, Moriarty CP, Marks GB, Belousova EG, Xuan W, Bye PT, National Hypertonic Saline in Cystic Fibrosis (NHSCF) Study Group (2006) A controlled trial of long-term inhaled hypertonic saline in patients with cystic fibrosis. N Engl J Med 354:229–240. doi: 10.1056/NEJMoa043900 PubMedCrossRefGoogle Scholar
  31. Else TA, Pantle CR, Amy PS (2003) Boundaries for biofilm formation: humidity and temperature. Appl Environ Microbiol 69:5006–5010. doi: 10.1128/AEM.69.8.5006-5010.2003 PubMedCentralPubMedCrossRefGoogle Scholar
  32. Engelhardt MA, Daly K, Swannell RPJ, Head IM (2001) Isolation and characterization of a novel hydrocarbon-degrading, gram-positive bacterium, isolated from intertidal beach sediment, and description of Planococcus alkanoclasticus sp. nov. J Appl Microbiol 90:237–247. doi: 10.1046/j.1365-2672.2001.01241.x PubMedCrossRefGoogle Scholar
  33. Farzaneh H, Fereidon M, Noor A, Naser G (2010) Biodegradation of dodecyl benzenesulfonate sodium by Stenotrophomonas maltophilia biofilm. Afr J Biotechnol 9:55–62Google Scholar
  34. Fernández M, Duque E, Pizarro-Tobías P, Van Dillewijn P, Wittich RM, Ramos JL (2009) Microbial responses to xenobiotic compounds. Identification of genes that allow Pseudomonas putida KT2440 to cope with 2,4,6-trinitrotoluene. Microb Biotechnol 2:287–294. doi: 10.1111/j.1751-7915.2009.00085.x PubMedCentralPubMedCrossRefGoogle Scholar
  35. Flemming HC (2002) Biofouling in water systems – cases, causes and countermeasures. Appl Microbiol Biotechnol 59:629–640. doi: 10.1007/s00253-002-1066-9 PubMedCrossRefGoogle Scholar
  36. Flemming HC, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8:623–633. doi: 10.1038/nrmicro2415 PubMedGoogle Scholar
  37. Fletcher M (1988) Attachment of Pseudomonas fluorescens to glass and influence of electrolytes on bacterium-substratum separation distance. J Bacteriol 170:2027–2030PubMedCentralPubMedGoogle Scholar
  38. Fleuchot B, Gitton C, Guillot A, Vidic J, Nicolas P, Besset C, Fontaine L, Hols P, Leblond-Bourget N, Monnet V, Gardan R (2011) Rgg proteins associated with internalized small hydrophobic peptides: a new quorum-sensing mechanism in Streptococci. Mol Microbiol 80:1102–1119. doi: 10.1111/j.1365-2958.2011.07633.x PubMedCrossRefGoogle Scholar
  39. Gamboa F, Acosta A, García DA, Velosa J, Araya N, Ledergerber R (2014) Occurrence of Porphyromonas gingivalis and its antibacterial susceptibility to metronidazole and tetracycline in patients with chronic periodontitis. Acta Odontol Latinoam 27:137–144. doi: 10.1590/S1852-48342014000300007 PubMedGoogle Scholar
  40. García-Contreras R, Martínez-Vázquez M, Velázquez Guadarrama N, Villegas Pañeda AG, Hashimoto T, Maeda T, Quezada H, Wood TK (2013) Resistance to the quorum-quenching compounds brominated furanone C-30 and 5-fluorouracil in Pseudomonas aeruginosa clinical isolates. Pathog Dis 68:8–11. doi: 10.1111/2049-632X.12039 PubMedCrossRefGoogle Scholar
  41. Guardiola FA, Cuesta A, Meseguer J, Esteban MA (2012) Risks of using antifouling biocides in aquaculture. Int J Mol Sci 13:1541–1560. doi: 10.3390/ijms13021541 PubMedCentralPubMedCrossRefGoogle Scholar
  42. Gupta K, Barua S, Hazarika SN, Manhar AK, Nath D, Karak N, Namsa ND, Mukhopadhyay R, Kalia VC, Mandal M (2014) Green silver nanoparticles: enhanced antimicrobial and antibiofilm activity with effects on DNA replication and cell cytotoxicity. RSC Adv 4:52845–52855. doi: 10.1039/C4RA08791G CrossRefGoogle Scholar
  43. Hadad D, Geresh S, Sivan A (2005) Biodegradation of polyethylene by the thermophilic bacterium Brevibacillusborstelensis. J Appl Microbiol 98:1093–1100. doi: 10.1111/j.1365-2672.2005.02553.x PubMedCrossRefGoogle Scholar
  44. Hall-Stoodley L, Costerton JW, Stoodley P (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2:95–108. doi: 10.1038/nrmicro821 PubMedCrossRefGoogle Scholar
  45. Hannan S, Ready D, Jasni AS, Rogers M, Pratten J, Roberts AP (2010) Transfer of antibiotic resistance by transformation with eDNA within oral biofilms. FEMS Immunol Med Microbiol 59:345–349. doi: 10.1111/j.1574-695X.2010.00661.x PubMedGoogle Scholar
  46. Harayama S, Kasai Y, Hara A (2004) Microbial communities in oil-contaminated seawater. Curr Opin Biotechnol 15:205–214. doi: 10.1016/j.copbio.2004.04.002 PubMedCrossRefGoogle Scholar
  47. Hatch RA, Schiller NL (1998) Alginate lyase promotes diffusion of aminoglycosides through the extracellular polysaccharide of mucoid Pseudomonas aeruginosa. Antimicrob Agents Chemother 42:974–977PubMedCentralPubMedGoogle Scholar
  48. Hay ID, Rehman ZU, Moradali MF, Wang Y, Rehm BHA (2013) Microbial alginate production, modification and its applications. Microb Biotechnol 6:637–650. doi: 10.1111/1751-7915.12076 PubMedCentralPubMedGoogle Scholar
  49. Herrmann G, Yang L, Wu H, Song Z, Wang H, Høiby N, Ulrich M, Molin S, Riethmüller J, Döring G (2010) Colistin-tobramycin combinations are superior to monotherapy concerning the killing of biofilm Pseudomonas aeruginosa. J Infect Dis 202:1585–1592. doi: 10.1086/656788 PubMedCrossRefGoogle Scholar
  50. Heydorn A, Ersbøll 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. doi: 10.1128/AEM.68.4.2008-2017.2002 PubMedCentralPubMedCrossRefGoogle Scholar
  51. Hickman JW, Tifrea DF, Harwood CS (2005) A chemosensory system that regulates biofilm formation through modulation of cyclic diguanylate levels. Proc Natl Acad Sci 102:14422–14427. doi: 10.1073/pnas.0507170102 PubMedCentralPubMedCrossRefGoogle Scholar
  52. Hinsa SM, Espinosa-Urgel M, Ramos JL, O’Toole GA (2003) Transition from reversible to irreversible attachment during biofilm formation by Pseudomonas fluorescens WCS365 requires an ABC transporter and a large secreted protein. Mol Microbiol 49:905–918. doi: 10.1046/j.1365-2958.2003.03615.x PubMedCrossRefGoogle Scholar
  53. Hirschhausen N, Block D, Bianconi I, Bragonzi A, Birtel J, Lee JC, Dübbers A, Küster P, Kahl J, Peters G, Kahl BC (2013) Extended Staphylococcus aureus persistence in cystic fibrosis is associated with bacterial adaptation. Int J Med Microbiol 303:685–692. doi: 10.1016/j.ijmm.2013.09.012 PubMedCrossRefGoogle Scholar
  54. Høiby N, Ciofu O, Bjarnsholt T (2010) Pseudomonas aeruginosa biofilms in cystic fibrosis. Future Microbiol 5:1663–1674. doi: 10.2217/fmb.10.125 PubMedCrossRefGoogle Scholar
  55. Holá V, Ruzicka F, Horka M (2010) Microbial diversity in biofilm infections of the urinary tract with the use of sonication techniques. FEMS Immunol Med Microbiol 59:525–528. doi: 10.1111/j.1574-695X.2010.00703.x PubMedGoogle Scholar
  56. Huma N, Shankar P, Kushwah J, Bhushan A, Joshi J, Mukherjee T, Raju SC, Purohit HJ, Kalia VC (2011) Diversity and polymorphism in AHL-lactonase gene (aiiA) of Bacillus. J Microbiol Biotechnol 21:1001–1011. doi: 10.4014/jmb.1105.05056 PubMedCrossRefGoogle Scholar
  57. Hussain M, Steinbacher T, Peters G, Heilmann C, Becker K (2015) The adhesive properties of the Staphylococcus lugdunensis multifunctional autolysin AtlL and its role in biofilm formation and internalization. Int J Med Microbiol 305:129–139. doi: 10.1016/j.ijmm.2014.11.010 PubMedCrossRefGoogle Scholar
  58. Incani V, Omar A, Prosperi-Porta G, Nadworny P (2014) Ag5IO6: novel antibiofilm activity of a silver compound with application to medical devices. Int J Antimicrob Agents S0924–8579(14):00295–00297. doi: 10.1016/j.ijantimicag.2014.09.008 Google Scholar
  59. Jimenez JC, Federle MJ (2014) Quorum sensing in group a Streptococcus. Front Cell Infect Microbiol 4:127. doi: 10.3389/fcimb.2014.00127 PubMedCentralPubMedGoogle Scholar
  60. Kalia VC (2013) Quorum sensing inhibitors: an overview. Biotechnol Adv 31:224–245. doi: 10.1016/j.biotechadv.2012.10.004 PubMedCrossRefGoogle Scholar
  61. Kalia VC (2014a) Microbes, antimicrobials and resistance: the battle goes on. Indian J Microbiol 54:1–2. doi: 10.1007/s12088-013-0443-7 PubMedCentralPubMedCrossRefGoogle Scholar
  62. Kalia VC (2014b) In search of versatile organisms for quorum‐sensing inhibitors: acyl homoserine lactones (AHL)‐acylase and AHL‐lactonase. FEMS Microbiol Lett 359:143. doi: 10.1111/1574-6968.12585 PubMedCrossRefGoogle Scholar
  63. Kalia VC, Kumar P (2015a) Potential applications of quorum sensing inhibitors in diverse fields. In: Kalia VC (ed) Quorum sensing vs quorum quenching: a battle with no end in sight. Springer, New Delhi, pp 359–370. doi: 10.1007/978-81-322-1982-8_29 Google Scholar
  64. Kalia VC, Kumar P (2015b) The Battle: quorum-sensing inhibitors versus evolution of bacterial resistance. In: Kalia VC (ed) Quorum sensing vs quorum quenching: a battle with no end in sight. Springer, New Delhi, pp 385–391. doi: 10.1007/978-81-322-1982-8_31 Google Scholar
  65. Kalia VC, Purohit HJ (2011) Quenching the quorum sensing system: potential antibacterial drug targets. Crit Rev Microbiol 37:121–140. doi: 10.3109/1040841X.2010.532479 PubMedCrossRefGoogle Scholar
  66. Kalia VC, Raju SC, Purohit HJ (2011) Genomic analysis reveals versatile organisms for quorum quenching enzymes: acyl-homoserine lactone-acylase and -lactonase. Open Microbiol J 5:1–13. doi: 10.2174/187428580110501000 PubMedCentralPubMedCrossRefGoogle Scholar
  67. Kalia VC, Wood TK, Kumar P (2014) Evolution of resistance to quorum-sensing inhibitors. Microb Ecol 68:13–23. doi: 10.1007/s00248-013-0316-y PubMedCentralPubMedCrossRefGoogle Scholar
  68. Kalia VC, Kumar P, Pandian SK, Sharma P (2015) Biofouling control by quorum quenching. In: Kim SK (ed) Hb25_handbook of marine biotechnology, vol 15. Springer, New Delhi, India, pp 431–440. doi:  10.1007/978-3-642-53971-8_15
  69. Karatan E, Watnick P (2009) Signals, regulatory networks, and materials that build and break bacterial biofilms. Microbiol Mol Biol Rev 73:310–347. doi: 10.1128/MMBR.00041-08 PubMedCentralPubMedCrossRefGoogle Scholar
  70. Karube I, Tadashi M, Shinya T, Shuichi S (1977) Biochemical cells utilizing immobilized cells of Clostridium butyricum. Biotechnol Bioeng 19:1727–1733. doi: 10.1002/bit.260191112 CrossRefGoogle Scholar
  71. Kim BH, Kim HJ, Hyun MS, Park DH (1999) Direct electrode reaction of Fe (III) reducing bacterium, Shewanella putrefacience. J Microbiol Biotechnol 9:127–131Google Scholar
  72. Kim SR, Oh HS, Jo SJ, Yeon KM, Lee CH, Lim DJ, Lee CH, Lee JK (2013) Biofouling control with bead-entrapped quorum quenching bacteria in membrane bioreactors: physical and biological effects. Environ Sci Technol 47:836–842. doi: 10.1021/es303995s PubMedCrossRefGoogle Scholar
  73. Kjelleberg S, McDougald D, Rasmussen TB, Givskov M (2008) Quorum-sensing inhibition. In: Winans SC, Bassler BL (eds) Chemical communication among bacteria. ASM Press, Washington, D.C., pp 393–416CrossRefGoogle Scholar
  74. Kumar P, Patel SKS, Lee JK, Kalia VC (2013) Extending the limits of Bacillus for novel biotechnological applications. Biotechnol Adv 31:1543–1561. doi: 10.1016/j.biotechadv.2013.08.007 PubMedCrossRefGoogle Scholar
  75. Kumar P, Koul S, Patel SKS, Lee JK, Kalia VC (2015) Heterologous expression of quorum sensing inhibitory genes in diverse organisms. In: Kalia VC (ed) Quorum sensing vs quorum quenching: a battle with no end in sight. Springer, New Delhi, pp 343–356. doi: 10.1007/978-81-322-1982-8_28 Google Scholar
  76. Laverty G, Gorman SP, Gilmore BF (2014) Biomolecular mechanisms of Pseudomonas aeruginosa and Escherichia coli biofilm formation. Pathogens 3:596–632. doi: 10.3390/pathogens3030596 PubMedCentralPubMedCrossRefGoogle Scholar
  77. Logan BE, Hamelers B, Rozendal R, Schröder U, Keller J, Freguia S, Aelterman P, Verstraete W, Rabaey K (2006) Microbial fuel cells: methodology and technology. Environ Sci Technol 40:5181–5192. doi: 10.1021/es0605016 PubMedCrossRefGoogle Scholar
  78. Love RM (2010) Biofilm – substrate interaction: from initial adhesion to complex interactions and biofilm maturity. Topics 22:50–57. doi: 10.1111/j.1601-1546.2012.00280.x CrossRefGoogle Scholar
  79. Lovley DR (2006) Bug juice: harvesting electricity with microorganisms. Nat Rev Microbiol 4:497–508. doi: 10.1038/nrmicro1442 PubMedCrossRefGoogle Scholar
  80. Lye DCB, Hughes A, Brien D, Athan E (2005) Candida glabrata prosthetic valve endocarditis treated successfully with fluconazole plus caspofungin without surgery: a case report and literature review. Eur J Clin Microbiol Infect Dis 24:753–755. doi: 10.1007/s10096-005-0038-2 PubMedCrossRefGoogle Scholar
  81. Lynch MJ, Swift S, Kirke DF, Keevil GW, Dodd CER, Williams P (2002) The regulation of biofilm development by quorum sensing in Aeromonas hydrophila. Environ Microbiol 4:18–28. doi: 10.1128/JB.186.3.692-698.2004 PubMedCrossRefGoogle Scholar
  82. Lyon GJ, Wright JS, Muir TW, Novick RP (2002) Key determinants of receptor activation in the agr autoinducing peptides of Staphylococcus aureus. Biochemistry 41:10095–10104. doi: 10.1021/bi026049u PubMedCrossRefGoogle Scholar
  83. Mancl K (2002) Model for success in on-site wastewater management. J Environ Health 64:29–31PubMedGoogle Scholar
  84. Mitchell A (2001) Quorum quenching. Nat Rev Mol Cell Biol 2:488. doi: 10.1038/35080025 CrossRefGoogle Scholar
  85. 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. doi: 10.1016/S0958-1669(03)00036-3 PubMedCrossRefGoogle Scholar
  86. Monnet V, Juillard V, Gardan R (2014) Peptide conversations in Gram-positive bacteria. Crit Rev Microbiol 2:100–105. doi: 10.3109/1040841X.2014.948804
  87. Mor R, Sivan A (2008) Biofilm formation and partial biodegradation of polystyrene by the actinomycete Rhodococcus ruber: biodegradation of polystyrene. Biodegradation 19:851–858. doi: 10.1007/s10532-008-9188-0 PubMedCrossRefGoogle Scholar
  88. Mounier J, Camus A, Mitteau I, Vaysse PJ, Goulas P, Grimaud R, Sivadon P (2014) The marine bacterium Marinobacter hydrocarbonoclasticus SP17 degrades a wide range of lipids and hydrocarbons through the formation of oleolytic biofilms with distinct gene expression profiles. FEMS Microbiol Ecol 90:816–831. doi: 10.1111/1574-6941.12439 PubMedCrossRefGoogle Scholar
  89. Nguyen KT, Piastro K, Gray TA, Derbyshire KM (2010) Mycobacterial biofilms facilitate horizontal DNA transfer between strains of Mycobacterium smegmatis. J Bacteriol 192:5134–5142. doi: 10.1128/JB.00650-10 PubMedCentralPubMedCrossRefGoogle Scholar
  90. Nguyen PQ, Botyanszki Z, Tay PK, Joshi NS (2014) Programmable biofilm-based materials from engineered curli nanofibres. Nat Commun 5:4945. doi: 10.1038/ncomms5945 PubMedCrossRefGoogle Scholar
  91. Nwodo UU, Green E, Okoh AI (2012) Bacterial exopolysaccharides: functionality and prospects. Int J Mol Sci 13:14002–14015. doi: 10.3390/ijms131114002 PubMedCentralPubMedCrossRefGoogle Scholar
  92. O’Loughlin CT, Miller LC, Siryaporn A, Drescher K, Semmelhack MF, Bassler BL (2013) A quorum-sensing inhibitor blocks Pseudomonas aeruginosa virulence and biofilm formation. Proc Natl Acad Sci 110:17981–17986. doi: 10.1073/pnas.1316981110 PubMedCentralPubMedCrossRefGoogle Scholar
  93. Orr IG, Hadar Y, Sivan A (2004) Colonization, biofilm formation and biodegradation of polyethylene by a strain of Rhodococcus ruber. Appl Microbiol Biotechnol 65:97–104. doi: 10.1007/s00253-004-1584-8 PubMedGoogle Scholar
  94. Otsuka R, Imai S, Murata T, Nomura Y, Okamoto M, Tsumori H, Kakuta E, Hanada N, Momoi Y (2015) Application of chimeric glucanase comprising mutanase and dextranase for prevention of dental biofilm formation. Microbiol Immunol 59:28–36. doi: 10.1111/1348-0421.12214 PubMedCrossRefGoogle Scholar
  95. Pant D, Van Bogaert G, Diels L, Vanbroekhoven K (2010) A review of the substrates used in microbial fuel cells (MFCs) for sustainable energy production. Bioresour Technol 101:1533–1543. doi: 10.1016/j.biortech.2009.10.017 PubMedCrossRefGoogle Scholar
  96. Park HS, Kim HS (2000) Identification and characterization of the nitrobenzene catabolic plasmids pNB1 and pNB2 in Pseudomonas putida HS12. J Bacteriol 82:573–580. doi: 10.1128/JB.182.3.573-580.2000 CrossRefGoogle Scholar
  97. Park HS, Lim SJ, Chang YK, Livingston AG, Kim HS (1999) Degradation of chloronitrobenzenes by a coculture of Pseudomonas putida and a Rhodococcus spp. Appl Environ Microbiol 65:1083–1091PubMedCentralPubMedGoogle Scholar
  98. Pei R, Lamas-Samanamud GR (2014) Inhibition of biofilm formation by T7 bacteriophages producing quorum-quenching enzymes. Appl Environ Microbiol 80:5340–5348. doi: 10.1128/AEM.01434-14 PubMedCentralPubMedCrossRefGoogle Scholar
  99. Peyyala R, Ebersole JL (2013) Multispecies biofilms and host responses: “Discriminating the trees from the forest.”. Cytokine 61:15–25. doi: 10.1016/j.cyto.2012.10.006 PubMedCentralPubMedCrossRefGoogle Scholar
  100. Pham CA, Jung SJ, Phung NT, Lee J, Chang IS, Kim BH, Yi H, Chun J (2003) A novel electrochemically active and Fe(III)-reducing bacterium phylogenetically related to Aeromonas hydrophila, isolated from a microbial fuel cell. FEMS Microbiol Lett 223:129–134. doi: 10.1016/S0378-1097(03)00354-9 PubMedCrossRefGoogle Scholar
  101. Piola RF, Hopkins GA (2012) Thermal treatment as a method to control transfers of invasive biofouling species via vessel sea chests. Mar Pollut Bull 64:1620–1630. doi: 10.1016/j.marpolbul.2012.05.028 PubMedCrossRefGoogle Scholar
  102. Potter MC (1911) Electrical effects accompanying the decomposition of organic compounds. Proc R Soc B Biol Sci 84:260–276CrossRefGoogle Scholar
  103. Pous N, Puig S, Coma M, Balaguer MD, Colprim J (2013) Bioremediation of nitrate-polluted groundwater in a microbial fuel cell. J Chem Technol Biotechnol 88:1690–1696. doi: 10.1002/jctb.4020 CrossRefGoogle Scholar
  104. Rabei MG, Gad-Elrab SMF, Abskharon RNN, Hassan SHA, Shoreit AAM (2009) Biosorption of hexavalent chromium using biofilm of E. coli supported on granulated activated carbon. World J Microbiol Biotechnol 25:1695–1703. doi: 10.1007/s11274-009-0063-x CrossRefGoogle Scholar
  105. Raghukumar C, Vipparty V, David JJ, Chandramohan D (2001) Degradation of crude oil by marine cyanobacteria. Appl Microbiol Biotechnol 57:433–436. doi: 10.1007/s002530100784 PubMedCrossRefGoogle Scholar
  106. Reeser RJ, Medler RT, Billington SJ, Jost BH, Joens LA (2007) Characterization of Campylobacter jejuni biofilms under defined growth conditions. Appl Environ Microbiol 73:1908–1913. doi: 10.1128/AEM.00740-06 PubMedCentralPubMedCrossRefGoogle Scholar
  107. Riedel DJ, Weekes E, Forrest GN (2008) Addition of rifampin to standard therapy for treatment of native valve infective endocarditis caused by Staphylococcus aureus. Antimicrob Agents Chemother 52:2463–2467. doi: 10.1128/AAC.00300-08 PubMedCentralPubMedCrossRefGoogle Scholar
  108. Robles-Price A, Wong TY, Sletta H, Valla S, Schiller NL (2004) AlgX is a periplasmic protein required for alginate biosynthesis in Pseudomonas aeruginosa. J Bacteriol 186:7369–7377. doi: 10.1128/JB.186.21.7369-7377.2004 PubMedCentralPubMedCrossRefGoogle Scholar
  109. Rodrigues DF, Elimelech M (2009) Role of type 1 fimbriae and mannose in the development of Escherichia coli K12 biofilm: from initial cell adhesion to biofilm formation. Biofouling 25:401–411. doi: 10.1080/08927010902833443 PubMedCrossRefGoogle Scholar
  110. Rosen R, Bachrach G, Bronshteyn M, Gedalia I, Steinberg D (2005) The role of fructans on dental biofilm formation by Streptococcus sobrinus, Streptococcus mutans, Streptococcus gordonii and Actinomyces viscosus. FEMS Microbiol Lett 195:205–210. doi: 10.1016/S0378-1097(01)00009-x CrossRefGoogle Scholar
  111. Rosenhahn A, Schilp S, Kreuzer HJ, Grunze M (2010) The role of “inert” surface chemistry in marine biofouling prevention. Phys Chem Chem Phys 12:4275–4286. doi: 10.1039/c001968m PubMedCrossRefGoogle Scholar
  112. Saeidi N, Wong CK, Lo TM, Nguyen HX, Ling H, Leong SSJ, Poh CL, Chang MW (2011) Engineering microbes to sense and eradicate Pseudomonas aeruginosa, a human pathogen. Mol Syst Biol 7:521. doi: 10.1038/msb.2011.55 PubMedCentralPubMedCrossRefGoogle Scholar
  113. Scott JA, Karanjkar AM, Rowe DL (1995) Biofilm covered granular activated carbon for decontamination of streams containing heavy metals and organic chemicals. Miner Eng 8:221–230. doi: 10.1016/0892-6875(94)00115-S CrossRefGoogle Scholar
  114. Sharma VK, Bearson SM, Bearson BL (2010) Evaluation of the effects of sdiA, a luxR homologue, on adherence and motility of Escherichia coli O157:H7. Microbiology 156:1303–1312. doi: 10.1099/mic.0.034330-0 PubMedCrossRefGoogle Scholar
  115. Shantaram A, Beyenal H, Raajan R, Veluchamy A, Lewandowskiz Z (2005) Wireless sensors powered by microbial fuel cells. Environ Sci Technol 39(13):5037–5042. doi:10-1021/es0480668Google Scholar
  116. Shimada K, Itoh Y, Washio K, Morikawa M (2012) Efficacy of forming biofilms by naphthalene degrading Pseudomonas stutzeri T102 toward bioremediation technology and its molecular mechanisms. Chemosphere 87:226–233. doi: 10.1016/j.chemosphere.2011.12.078 PubMedCrossRefGoogle Scholar
  117. Sio CF, Otten LG, Cool RH, Diggle SP, Braun PG, Bos R, Daykin M, Cámara M, Williams P, Quax WJ (2006) Quorum quenching by an N-acyl-homoserine lactone acylase from Pseudomonas aeruginosa PAO1. Infect Immun 74:1673–1682. doi: 10.1128/IAI.74.3.1673-1682.2006 PubMedCentralPubMedCrossRefGoogle Scholar
  118. Soini SM, Koskinen KT, Vilenius MJ, Puhakka JA (2002) Effects of fluid-flow velocity and water quality on planktonic and sessile microbial growth in water hydraulic system. Water Res 3:3812–3820. doi: 10.1016/S0043-1354(02)00099-4 CrossRefGoogle Scholar
  119. Stapper AP, Narasimhan G, Ohman DE, Barakat J, Hentzer M, Molin S, Kharazmi A, Høiby N, Mathee K (2004) Alginate production affects Pseudomonas aeruginosa biofilm development and architecture, but is not essential for biofilm formation. J Med Microbiol 53:679–690. doi: 10.1099/jmm.0.45539-45540 PubMedCrossRefGoogle Scholar
  120. Starner TD, Zhang N, Kim G, Apicella MA, McCray PB Jr (2006) Haemophilus influenzae forms biofilms on airway epithelia: implications in cystic fibrosis. Am J Respir Crit Care Med 174:213–220. doi: 10.1164/rccm.200509-1459OC PubMedCentralPubMedCrossRefGoogle Scholar
  121. Steidler L, Hans W, Schotte L, Neirynck S, Obermeier F, Falk W, Fiers W, Remaut E (2000) Treatment of murine colitis by Lactococcus lactis secreting interleukin-10. Science 289:1352–1355. doi: 10.1126/science.289.5483.1352 PubMedCrossRefGoogle Scholar
  122. Sundar K, Sadiq IM, Mukherjee A, Chandrasekaran N (2011) Bioremoval of trivalent chromium using Bacillus biofilms through continuous flow reactor. J Hazard Mater 30:44–51. doi: 10.1016/j.jhazmat.2011.08.066 CrossRefGoogle Scholar
  123. Suseela MR, Toppo K (2007) Algal biofilms on polythene and its possible degradation. Curr Sci 92:285–287Google Scholar
  124. Sutherland I (2001) Biofilm exopolysaccharides: a strong and sticky framework. Microbiology 147:3–9PubMedCrossRefGoogle Scholar
  125. Tao J, Mancl KM, Tuovinen OH (2010) Attenuation of pollutants in sanitary sewer overflow: comparative evaluation of treatment with fixed media bioreactors. Bioresour Technol 101:1781–1786. doi: 10.1016/j.biortech.2009.10.038 PubMedCrossRefGoogle Scholar
  126. Tchouaffi-Nana F, Ballard TE, Cary CH, Macdonald TL, Sifri CD, Hoffman PS (2010) Nitazoxanide inhibits biofilm formation by Staphylococcus epidermidis by blocking accumulation on surfaces. Antimicrob Agents Chemother 54:2767–2774. doi: 10.1128/AAC.00901-09 PubMedCentralPubMedCrossRefGoogle Scholar
  127. Teitzel GM, Parsek MR (2003) Heavy metal resistance of biofilm and planktonic Pseudomonas aeruginosa. Appl Environ Microbiol 69:2313–2320. doi: 10.1128/AEM.69.4.2313-2320.2003 PubMedCentralPubMedCrossRefGoogle Scholar
  128. Toner B, Manceau A, Marcus MA, Millet DB, Sposito G (2005) Zinc sorption by a bacterial biofilm. Environ Sci Technol 39:8288–8294. doi: 10.1021/es050528+ PubMedCrossRefGoogle Scholar
  129. Torlak E, Sert D (2013) Combined effect of benzalkonium chloride and ultrasound against Listeria monocytogenes biofilm on plastic surface. Lett Appl Microbiol 57:220–226. doi: 10.1111/lam.12100 PubMedCrossRefGoogle Scholar
  130. Trautner BW, Darouiche RO (2004) Role of biofilm in catheter-associated urinary tract infection. Am J Infect Control 32:177–183. doi: 10.1016/j.ajic.2003.08.005 PubMedCentralPubMedCrossRefGoogle Scholar
  131. Tunkel AR, Mandell GL (1992) Infecting microorganisms. In: Kaye D (ed) Infective endocarditis, 2nd edn., pp 85–97Google Scholar
  132. Uhlich GA, Gunther NW 4th, Bayles DO, Mosier DA (2009) The CsgA and Lpp proteins of an Escherichia coli O157:H7 strain affect HEp-2 Ccll invasion, motility, and biofilm formation. Infect Immun 77:1543–1552. doi: 10.1128/IAI.00949-08 PubMedCentralPubMedCrossRefGoogle Scholar
  133. Vazquez V, Liang X, Horndahl JK, Ganesh VK, Smeds E, Foster TJ, Hook M (2011) Fibrinogen is a ligand for the Staphylococcus aureus microbial surface components recognizing adhesive matrix molecules (MSCRAMM) bone sialoprotein-binding protein (Bbp). J Biol Chem 286:29797–29805. doi: 10.1074/jbc.M110.214981 PubMedCentralPubMedCrossRefGoogle Scholar
  134. Verma P, Brown JM, Nunez VH, Morey RE, Steigerwalt AG, Pellegrini GJ, Kessler HA (2006) Native valve endocarditis due to Gordonia polyisoprenivorans: case report and review of literature of bloodstream infections caused by Gordonia species. J Clin Microbiol 44:1905–1908. doi: 10.1128/JCM.44.5.1905-1908.2006 PubMedCentralPubMedCrossRefGoogle Scholar
  135. Vivant AL, Garmyn D, Gal L, Piveteau P (2014) The Agr communication system provides a benefit to the populations of Listeria monocytogenes in soil. Front Cell Infect Microbiol 4:160. doi: 10.3389/fcimb.2014.00160 PubMedCentralPubMedGoogle Scholar
  136. Wagner M, Loy A (2002) Bacterial community composition and function in sewage treatment systems. Curr Opin Biotechnol 13:218–227. doi: 10.1016/S0958-1669(02)00315-4 PubMedCrossRefGoogle Scholar
  137. Walters M, Sperandio V (2006a) Autoinducer-3 and epinephrine signaling in the kinetics of locus of enterocyte effacement gene expression in enterohemorrhagic Escherichia coli. Infect Immun 74:5445–5455. doi: 10.1128/IAI.00099-06 PubMedCentralPubMedCrossRefGoogle Scholar
  138. Walters M, Sperandio V (2006b) Quorum sensing in Escherichia coli and Salmonella typhimurium. Int J Med Microbiol 296:125–131. doi: 10.1016/j.ijmm.2006.01.041 PubMedCrossRefGoogle Scholar
  139. Wang X, Lünsdorf H, Ehrén I, Brauner A, Römling U (2010) Characteristics of biofilms from urinary tract catheters and presence of biofilm-related components in Escherichia coli. Curr Microbiol 60:446–453. doi: 10.1007/s00284-009-9563-z PubMedCrossRefGoogle Scholar
  140. Wang S, Liu X, Liu H, Zhang L, Guo Y, Yu S, Wozniak DJ, Ma LZ (2015) The exopolysaccharide Psl-eDNA interaction enables the formation of a biofilm skeleton in Pseudomonas aeruginosa. Environ Microbiol Rep 7:330–340. doi: 10.1111/1758-2229.12252 PubMedCentralPubMedCrossRefGoogle Scholar
  141. Waters CM, Bassler BL (2005) Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Biol 21:319–346. doi: 10.1146/annurev.cellbio.21.012704.131001 CrossRefGoogle Scholar
  142. Whitehead NA, Barnard AM, Slater H, Simpson NJ, Salmond GP (2001) Quorum-sensing in gram-negative bacteria. FEMS Microbiol Rev 25:365–404. doi: 10.1016/S0168-6445(01)00059-6 PubMedCrossRefGoogle Scholar
  143. Wiens JR, Vasil AI, Schurr MJ, Vasil ML (2014) Iron-regulated expression of alginate production, mucoid phenotype, and biofilm formation by Pseudomonas aeruginosa. mBio 5:e01010–e01013. doi: 10.1128/mBio.01010-13 PubMedCentralPubMedCrossRefGoogle Scholar
  144. Yakimov MM, Golyshin PN, Lang S (1998) Alcanivorax borkumensis gen. nov., sp. nov., a new, hydrocarbon-degrading and surfactant-producing marine bacterium. Int J Syst Bacteriol 48:339–348. doi: 10.1099/00207713-48-2-339 PubMedCrossRefGoogle Scholar
  145. Yang S, Yang F, Fu Z, Wang T, Lei R (2010) Simultaneous nitrogen and phosphorus removal by a novel sequencing batch moving bed membrane bioreactor for wastewater treatment. J Hazard Mater 175:551–557. doi: 10.1016/j.jhazmat.2009.10.040 PubMedCrossRefGoogle Scholar
  146. Yebra DM, Kiil S, Johansen KD (2004) Antifouling technology-past, present and future steps toward efficient and environmentally friendly antifouling coatings. Prog Org Coat 50:75–104. doi: 10.1016/j.porgcoat.2003.06.001 CrossRefGoogle Scholar
  147. Yeon KM, Lee C-H, Kim J (2009) Magnetic enzyme carrier for effective biofouling control in the membrane bioreactor based on enzymatic quorum quenching. Environ Sci Technol 43:7403–7409. doi: 10.1021/es9001323k PubMedCrossRefGoogle Scholar
  148. Zhong C, Gurry T, Cheng AA, Downey J, Deng SCM, Lu TK (2014) Strong underwater adhesives made by self-assembling multi-protein nanofibres. Nat Nanotechnol 9:858–866. doi: 10.1038/nnano.2014.199 PubMedCentralPubMedCrossRefGoogle Scholar
  149. Zobell CE (1943) The effect of solid surfaces on bacterial activity. J Bacteriol 46:39–56PubMedCentralPubMedGoogle Scholar

Copyright information

© Springer India 2015

Authors and Affiliations

  • Neha Dubey
    • 1
  • Raja Singh
    • 2
  • Aditya K. Sharma
    • 3
    • 4
  • Sharmila Basu-Modak
    • 1
  • Yogendra Singh
    • 5
  1. 1.Department of ZoologyUniversity of DelhiDelhiIndia
  2. 2.Special center for molecular Medicine (SCMM)Jawaharlal Nehru UniversityNew DelhiIndia
  3. 3.Lab 208, Allergy and Infectious DiseasesCSIR-Institute of Genomics and Integrative BiologyNew DelhiIndia
  4. 4.Academy of Scientific & Innovative Research (AcSIR)New DelhiIndia
  5. 5.Allergy and Infectious DiseasesCSIR-Institute of Genomics and Integrative BiologyDelhiIndia

Personalised recommendations