Multi-species biofilms: How to avoid unfriendly neighbors

FEMS Microbiology Reviews

Volumn 36, Issue 5, 2012, Pages 972-989

  Rendueles, Olaya ^a   Ghigo, Jean Marc ^a  

^a INSTITUT PASTEUR   (France)

Author keywords

Adhesion; Bacterial interferences; Biofilm dispersion; Biofilm formation; Biosurfactants; Mixed communities

Indexed keywords

AMIDASE; BETA DEFENSIN 2; BETA MANNOSIDASE; BIOSURFACTANT; DEOXYRIBONUCLEASE; GLUCONOLACTONASE; IMMUNOGLOBULIN A; LACTOFERRIN; MUCIN; N ACETYLGLUCOSAMINE; N ACYLHOMOSERINE LACTONE; POLYSACCHARIDE; RIBONUCLEASE; SURFACTIN;

BACILLUS SUBTILIS; BACTERIAL COLONIZATION; BACTERIAL VIABILITY; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; BIOFILM; CANDIDA ALBICANS; CELL COMMUNICATION; CELL INTERACTION; CELL SURFACE; CHEMOTAXIS; DISPERSION; ENZYMATIC DEGRADATION; ESCHERICHIA COLI; EXTRACELLULAR MATRIX; GENE EXPRESSION; HUMAN; HYDROPHILICITY; HYDROPHOBICITY; LACTOBACILLUS ACIDOPHILUS; MOLECULAR MIMICRY; NONHUMAN; ORGANISMAL INTERACTION; PROTEIN DEGRADATION; PROTEUS MIRABILIS; PSEUDOMONAS AERUGINOSA; QUORUM SENSING; REVIEW; RHIZOBIUM RADIOBACTER; SALMONELLA ENTERICA; SIGNAL TRANSDUCTION; STREPTOCOCCUS SALIVARIUS; WETTABILITY; XANTHOMONAS CAMPESTRIS;

ADHESION; BACTERIAL INTERFERENCES; BIOFILM DISPERSION; BIOFILM FORMATION; BIOSURFACTANTS; MIXED COMMUNITIES;

ANTIBIOSIS; BACTERIAL ADHESION; BACTERIAL PHYSIOLOGICAL PHENOMENA; BIOFILMS; HOST-PATHOGEN INTERACTIONS; SURFACE-ACTIVE AGENTS;

BACTERIA (MICROORGANISMS);

EID: 84864410913     PISSN: 01686445     EISSN: 15746976     Source Type: Journal    
DOI: 10.1111/j.1574-6976.2012.00328.x     Document Type: Review

References (162)

1. Aberg V & Almqvist F (2007) Pilicides-small molecules targeting bacterial virulence. Org Biomol Chem 5: 1827-1834.
2. Allaker RP (2010) The use of nanoparticles to control oral biofilm formation. J Dent Res 89: 1175-1186.
3. An D, Danhorn T, Fuqua C & Parsek MR (2006) Quorum sensing and motility mediate interactions between Pseudomonas aeruginosa and Agrobacterium tumefaciens in biofilm cocultures. P Natl Acad Sci USA 103: 3828-3833.
4. Antoniani D, Bocci P, Maciag A, Raffaelli N & Landini P (2010) Monitoring of diguanylate cyclase activity and of cyclic-di-GMP biosynthesis by whole-cell assays suitable for high-throughput screening of biofilm inhibitors. Appl Microbiol Biotechnol 85: 1095-1104.
5. Ardehali R, Shi L, Janatova J, Mohammad SF & Burns GL (2002) The effect of apo-transferrin on bacterial adhesion to biomaterials. Artif Organs 26: 512-520.
6. Ardehali R, Shi L, Janatova J, Mohammad SF & Burns GL (2003) The inhibitory activity of serum to prevent bacterial adhesion is mainly due to apo-transferrin. J Biomed Mater Res A 66: 21-28.
7. Augustine N, Kumar P & Thomas S (2010) Inhibition of Vibrio cholerae biofilm by AiiA enzyme produced from Bacillus spp. Arch Microbiol 192: 1019-1022.
8. Banat IM, Franzetti A, Gandolfi I, Bestetti G, Martinotti MG, Fracchia L, Smyth TJ & Marchant R (2010) Microbial biosurfactants production, applications and future potential. Appl Microbiol Biotechnol 87: 427-444.
9. Bandara HM, Yau JY, Watt RM, Jin LJ & Samaranayake LP (2010) Pseudomonas aeruginosa inhibits in-vitro Candida biofilm development. BMC Microbiol 10: 125.
10. Barraud N, Hassett DJ, Hwang SH, Rice SA, Kjelleberg S & Webb JS (2006) Involvement of nitric oxide in biofilm dispersal of Pseudomonas aeruginosa. J Bacteriol 188: 7344-7353.
11. Barraud N, Schleheck D, Klebensberger J, Webb JS, Hassett DJ, Rice SA & Kjelleberg S (2009) Nitric oxide signaling in Pseudomonas aeruginosa biofilms mediates phosphodiesterase activity, decreased cyclic di-GMP levels, and enhanced dispersal. J Bacteriol 191: 7333-7342.
12. Bassler B & Losick R (2006) Bacterially speaking. Cell 125: 237-246.
13. Beloin C, Valle J, Latour-Lambert P, Faure P, Kzreminski M, Balestrino D, Haagensen JA, Molin S, Prensier G, Arbeille B & Ghigo JM (2004) Global impact of mature biofilm lifestyle on Escherichia coli K-12 gene expression. Mol Microbiol 51: 659-674.
14. Bendaoud M, Vinogradov E, Balashova NV, Kadouri DE, Kachlany SC & Kaplan JB (2011) Broad spectrum biofilm inhibition by Kingella kingae exopolysaccharide. J Bacteriol 193: 3879-3886.
15. Berggren A, Lazou Ahrén I, Larsson N & Önning G (2011) Randomised, double-blind and placebo-controlled study using new probiotic lactobacilli for strengthening the body immune defence against viral infections. Eur J Nutr 50: 203-210.
16. Bergstrom JD, Kurtz MM, Rew DJ, Amend AM, Karkas JD, Bostedor RG, Bansal VS, Dufresne C, VanMiddlesworth FL, Hensens OD et al. (1993) Zaragozic acids: a family of fungal metabolites that are picomolar competitive inhibitors of squalene synthase. P Natl Acad Sci USA 90: 80-84.
17. Bjarnsholt T, Tolker-Nielsen T & Givskov M (2011) Interfering with "Bacterial Gossip". Biofilm Highlights (Flemming H-C, ed), pp. 163-188. Springer-Verlag, Berlin.
18. Boles BR, Thoendel M & Singh PK (2005) Rhamnolipids mediate detachment of Pseudomonas aeruginosa from biofilms. Mol Microbiol 57: 1210-1223.
19. Boyd A & Chakrabarty AM (1994) Role of alginate lyase in cell detachment of Pseudomonas aeruginosa. Appl Environ Microbiol 60: 2355-2359.
20. Cegelski L, Pinkner JS, Hammer ND et al. (2009) Small-molecule inhibitors target Escherichia coli amyloid biogenesis and biofilm formation. Nat Chem Biol 5: 913-919.
21. Choi CH, Jo SY, Park HJ, Chang SK, Byeon JS & Myung SJ (2011) A randomized, double-blind, placebo-controlled multicenter trial of Saccharomyces boulardii in irritablebowel syndrome: effect on quality of life. J Clin Gastroenterol 45: 679-683.
22. Christopher AB, Arndt A, Cugini C & Davey ME (2010) A streptococcal effector protein that inhibits Porphyromonas gingivalis biofilm development. Microbiology (Reading, Engl) 156: 3469-3477.
23. Colvin KM, Gordon VD, Murakami K, Borlee BR, Wozniak DJ, Wong GC & Parsek MR (2011) The Pel polysaccharide can serve a structural and protective role in the biofilm matrix of Pseudomonas aeruginosa. PloS Pathog 7: e1001264.
24. Costerton JW, Cheng KJ, Geesey GG, Ladd TI, Nickel JC, Dasgupta M & Marrie TJ (1987) Bacterial biofilms in nature and disease. Annu Rev Microbiol 41: 435-464.
25. Costerton JW, Stewart PS & Greenberg EP (1999) Bacterial biofilms: a common cause of persistent infections. Science 284: 1318-1322.
26. Cugini C, Calfee MW, Farrow JM, Morales DK, Pesci EC & Hogan DA (2007) Farnesol, a common sesquiterpene, inhibits PQS production in Pseudomonas aeruginosa. Mol Microbiol 65: 896-906.
27. Czajkowski R & Jafra S (2009) Quenching of acyl-homoserine lactone-dependent quorum sensing by enzymatic disruption of signal molecules. Acta Biochim Pol 56: 1-16.
28. Davidson LE, Fiorino AM, Snydman DR & Hibberd PL (2011) Lactobacillus GG as an immune adjuvant for live-attenuated influenza vaccine in healthy adults: a randomized double-blind placebo-controlled trial. Eur J Clin Nutr 65: 501-507.
29. Davies DG & Marques CN (2009) A fatty acid messenger is responsible for inducing dispersion in microbial biofilms. J Bacteriol 191: 1393-1403.
30. Dong YH & Zhang L (2005) Quorum sensing and quorum-quenching enzymes. J Microbiol 43 Spec No: 101-109.
31. Dong YH, Wang LH, Xu JL, Zhang HB, Zhang XF & Zhang LH (2001) Quenching quorum-sensing-dependent bacterial infection by an N-acyl homoserine lactonase. Nature 411: 813-817.
32. Dong YH, Gusti AR, Zhang Q, Xu JL & Zhang LH (2002) Identification of quorum-quenching N-acyl homoserine lactonases from Bacillus species. Appl Environ Microbiol 68: 1754-1759.
33. Donlan RM (2009) Preventing biofilms of clinically relevant organisms using bacteriophage. Trends Microbiol 17: 66-72.
34. Donlan RM (2011) Biofilm elimination on intravascular catheters: important considerations for the infectious disease practitioner. Clin Infect Dis 52: 1038-1045.
35. Donlan RM & Costerton JW (2002) Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 15: 167-193.
36. Dubey GP & Ben-Yehuda S (2011) Intercellular nanotubes mediate bacterial communication. Cell 144: 590-600.
37. Dunne WM (2002) Bacterial adhesion: seen any good biofilms lately? Clin Microbiol Rev 15: 155-166.
38. Dusane DH, Pawar VS, Nancharaiah YV, Venugopalan VP, Kumar AR & Zinjarde SS (2011) Anti-biofilm potential of a glycolipid surfactant produced by a tropical marine strain of Serratia marcescens. Biofouling 27: 645-654.
39. Falagas ME & Makris GC (2009) Probiotic bacteria and biosurfactants for nosocomial infection control: a hypothesis. J Hosp Infect 71: 301-306.
40. Fernandez-Pinar R, Camara M, Dubern JF, Ramos JL & Espinosa-Urgel M (2011) The Pseudomonas aeruginosa quinolone quorum sensing signal alters the multicellular behaviour of Pseudomonas putida KT2440. Res Microbiol 162: 773-781.
41. Finlay BB & Falkow S (1989) Common themes in microbial pathogenesis. Microbiol Rev 53: 210-230.
42. Firoved AM, Wood SR, Ornatowski W, Deretic V & Timmins GS (2004) Microarray analysis and functional characterization of the nitrosative stress response in nonmucoid and mucoid Pseudomonas aeruginosa. J Bacteriol 186: 4046-4050.
43. Flemming H & Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8: 623-633.
44. Flemming HC, Neu TR & Wozniak DJ (2007) The EPS matrix: the "house of biofilm cells". J Bacteriol 189: 7945-7947.
45. Francolini I & Donelli G (2010) Prevention and control of biofilm-based medical-device-related infections. FEMS Immunol Med Microbiol 59: 227-238.
46. Fredheim EG, Klingenberg C, Rohde H, Frankenberger S, Gaustad P, Flaegstad T & Sollid JE (2009) Biofilm formation by Staphylococcus haemolyticus. J Clin Microbiol 47: 1172-1180.
47. Gakhar L, Bartlett JA, Penterman J, Mizrachi D, Singh PK, Mallampalli RK, Ramaswamy S & McCray PB (2010) PLUNC is a novel airway surfactant protein with anti-biofilm activity. PLoS ONE 5: e9098.
48. Ghigo J-M (2003) Are there biofilm-specific physiological pathways beyond a reasonable doubt? Res Microbiol 154: 1-8.
49. Goldman CG, Barrado DA, Balcarce N et al. (2006) Effect of a probiotic food as an adjuvant to triple therapy for eradication of Helicobacter pylori infection in children. Nutrition 22: 984-988.
50. Golowczyc MA, Mobili P, Garrote GL, Abraham AG & De Antoni GL (2007) Protective action of Lactobacillus kefir carrying S-layer protein against Salmonella enterica serovar Enteritidis. Int J Food Microbiol 118: 264-273.
51. Grabosch C, Hartmann M, Schmidt-Lassen J & Lindhorst TK (2011) Squaric acid monoamide mannosides as ligands for the bacterial lectin FimH: covalent inhibition or not? Chembiochem 12: 1066-1074.
52. Grandy G, Medina M, Soria R, Terán CG & Araya M (2010) Probiotics in the treatment of acute rotavirus diarrhoea. A randomized, double-blind, controlled trial using two different probiotic preparations in Bolivian children. BMC Infect Dis 10: 253.
53. Hall-Stoodley L, Costerton JW & Stoodley P (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2: 95-108.
54. Hammond A, Dertien J, Colmer-Hamood JA, Griswold JA& Hamood AN (2008) Serum inhibits P. aeruginosa biofilm formation on plastic surfaces and intravenous catheters. J Surg Res 159: 735-746.
55. Hell E, Giske CG, Nelson A, Romling U & Marchini G (2009) Human cathelicidin peptide LL37 inhibits both attachment capability and biofilm formation of Staphylococcus epidermidis. Lett Appl Microbiol 50: 211-215.
56. Hengge R (2009) Principles of c-di-GMP signalling in bacteria. Nat Rev Microbiol 7: 263-273.
57. Hibbing ME, Fuqua C, Parsek MR & Peterson SB (2010) Bacterial competition: surviving and thriving in the microbial jungle. Nat Rev Microbiol 8: 15-25.
58. Hochbaum AI, Kolodkin-Gal I, Foulston L, Kolter R, Aizenberg J & Losick R (2011) Inhibitory effects of D-amino acids on Staphylococcus aureus biofilm development. J Bacteriol 193: 5616-5622.
59. Hogan DA & Kolter R (2002) Pseudomonas-Candida interactions: an ecological role for virulence factors. Science 296: 2229-2232.
60. Holcombe LJ, McAlester G, Munro CA, Enjalbert B, Brown AJ, Gow NA, Ding C, Butler G, O'Gara F & Morrissey JP (2010) Pseudomonas aeruginosa secreted factors impair biofilm development in Candida albicans. Microbiology 156: 1476-1486.
61. Hughes DT & Sperandio V (2008) Inter-kingdom signalling: communication between bacteria and their hosts. Nat Rev Microbiol 6: 111-120.
62. Iwase T, Uehara Y, Shinji H, Tajima A, Seo H, Takada K, Agata T & Mizunoe Y (2010) Staphylococcus epidermidis Esp inhibits Staphylococcus aureus biofilm formation and nasal colonization. Nature 465: 346-349.
63. Jabbouri S & Sadovskaya I (2010) Characteristics of the biofilm matrix and its role as a possible target for the detection and eradication of Staphylococcus epidermidis associated with medical implant infections. FEMS Immunol Med Microbiol 59: 280-291.
64. James G, Beaudette L & Costerton JW (1995) Interspecies bacterial interactions in biofilms. J Ind Microbiol Biotechnol 15: 257-262.
65. Ji G, Beavis R & Novick RP (1997) Bacterial interference caused by autoinducing peptide variants. Science 276: 2027-2030.
66. Jiang P, Li J, Han F, Duan G, Lu X, Gu Y & Yu W (2011) Antibiofilm activity of an exopolysaccharide from marine bacterium Vibrio sp. QY101. PLoS ONE 6: e18514.
67. Kanmani P, Satish kumar R, Yuvaraj N, Paari KA, Pattukumar V & Arul V (2011) Production and purification of a novel exopolysaccharide from lactic acid bacterium Streptococcus phocae PI80 and its functional characteristics activity in vitro. Bioresour Technol 102: 4827-4833.
68. Kaplan JB, Ragunath C, Ramasubbu N & Fine DH (2003) Detachment of Actinobacillus actinomycetemcomitans biofilm cells by an endogenous beta-hexosaminidase activity. J Bacteriol 185: 4693-4698.
69. Kaplan JB, Ragunath C, Velliyagounder K, Fine DH & Ramasubbu N (2004) Enzymatic detachment of Staphylococcus epidermidis biofilms. Antimicrob Agents Chemother 48: 2633-2636.
70. Karatan E & Watnick P (2009) Signals, regulatory networks, and materials that build and break bacterial biofilms. Microbiol Mol Biol Rev 73: 310-347.
71. Kim Y, Oh S & Kim SH (2009) Released exopolysaccharide (r-EPS) produced from probiotic bacteria reduce biofilm formation of enterohemorrhagic Escherichia coli O157:H7. Biochem Biophys Res Commun 379: 324-329.
72. Kiran MD, Giacometti A, Cirioni O & Balaban N (2008) Suppression of biofilm related, device-associated infections by staphylococcal quorum sensing inhibitors. Int J Artif Organs 31: 761-770.
73. Kleerebezem M & Vaughan EE (2009) Probiotic and gut lactobacilli and bifidobacteria: molecular approaches to study diversity and activity. Annu Rev Microbiol 63: 269-290.
74. Klein T, Abgottspon D, Wittwer M et al. (2010) FimH antagonists for the oral treatment of urinary tract infections: from design and synthesis to in vitro and in vivo evaluation. J Med Chem 53: 8627-8641.
75. Klein GL, Soum-Soutera E, Guede Z, Bazire A, Compere C & Dufour A (2011) The anti-biofilm activity secreted by a marine Pseudoalteromonas strain. Biofouling 27: 931-940.
76. Kline KA, Falker S, Dahlberg S, Normark S & Henriques-Normark B (2009) Bacterial adhesins in host-microbe interactions. Cell Host Microbe 5: 580-592.
77. Kolodkin-Gal I, Romero D, Cao S, Clardy J, Kolter R & Losick R (2010) D-amino acids trigger biofilm disassembly. Science 328: 627-629.
78. Korea CG, Badouraly R, Prevost MC, Ghigo JM & Beloin C (2010) Escherichia coli K-12 possesses multiple cryptic but functional chaperone-usher fimbriae with distinct surface specificities. Environ Microbiol 12: 1957-1977.
79. Korea CG, Ghigo JM & Beloin C (2011) The sweet connection: solving the riddle of multiple sugar-binding fimbrial adhesins in Escherichia coli: multiple E. coli fimbriae form a versatile arsenal of sugar-binding lectins potentially involved in surface-colonisation and tissue tropism. Bioessays 33: 300-311.
80. Kuiper I, Lagendijk EL, Pickford R, Derrick JP, Lamers GE, Thomas-Oates JE, Lugtenberg BJ & Bloemberg GV (2004) Characterization of two Pseudomonas putida lipopeptide biosurfactants, putisolvin I and II, which inhibit biofilm formation and break down existing biofilms. Mol Microbiol 51: 97-113.
81. Kumada M, Motegi M, Nakao R, Yonezawa H, Yamamura H, Tagami J & Senpuku H (2009) Inhibiting effects of Enterococcus faecium non-biofilm strain on Streptococcus mutans biofilm formation. J Microbiol Immunol Infect 42: 188-196.
82. Lam H, Oh DC, Cava F, Takacs CN, Clardy J, de Pedro MA & Waldor MK (2009) D-amino acids govern stationary phase cell wall remodeling in bacteria. Science 325: 1552-1555.
83. Larsson PG, Stray-Pedersen B, Ryttig KR & Larsen S (2008) Human lactobacilli as supplementation of clindamycin to patients with bacterial vaginosis reduce the recurrence rate; a 6-month, double-blind, randomized, placebo-controlled study. BMC Womens Health 15: 3.
84. Lazazzera BA (2005) Lessons from DNA microarray analysis: the gene expression profile of biofilms. Curr Opin Microbiol 8: 222-227.
85. Leatham MP, Banerjee S, Autieri SM, Mercado-Lubo R, Conway T& Cohen PS (2009) Precolonized human commensal Escherichia coli strains serve as a barrier to E. coli O157:H7 growth in the streptomycin-treated mouse intestine. Infect Immun 77: 2876-2886.
86. Lopez D & Kolter R (2010) Functional microdomains in bacterial membranes. Genes Dev 24: 1893-1902.
87. Lowery CA, Dickerson TJ & Janda KD (2008) Interspecies and interkingdom communication mediated by bacterial quorum sensing. Chem Soc Rev 37: 1337-1346.
88. Mack DR & Sherman PM (1991) Mucin isolated from rabbit colon inhibits in vitro binding of Escherichia coli RDEC-1. Infect Immun 59: 1015-1023.
89. Mack DR, Ahrne S, Hyde L, Wei S & Hollingsworth MA (2003) Extracellular MUC3 mucin secretion follows adherence of Lactobacillus strains to intestinal epithelial cells in vitro. Gut 52: 827-833.
90. Manefield M, Rasmussen TB, Henzter M, Andersen JB, Steinberg P, Kjelleberg S & Givskov M (2002) Halogenated furanones inhibit quorum sensing through accelerated LuxR turnover. Microbiology 148: 1119-1127.
91. Mann EE, Rice KC, Boles BR, Endres JL, Ranjit D, Chandramohan L, Tsang LH, Smeltzer MS, Horswill AR & Bayles KW (2009) Modulation of eDNA release and degradation affects Staphylococcus aureus biofilm maturation. PLoS ONE 4: e5822.
92. Mathivanan N, Prabavathy VR & Vijayanandraj VR (2008) The effect of fungal secondary metabolites on bacterial and fungal pathogens. Secondary Metabolites in Soil Ecology, Soil Biology, Volume 14, III, (Karlovsky P, ed.), pp. 129-140.
93. Matz C, Webb JS, Schupp PJ, Phang SY, Penesyan A, Egan S, Steinberg P & Kjelleberg S (2008) Marine biofilm bacteria evade eukaryotic predation by targeted chemical defense. PLoS ONE 3: e2744.
94. McNab R, Ford SK, El-Sabaeny A, Barbieri B, Cook GS & Lamont RJ (2003) LuxS-based signaling in Streptococcus gordonii: autoinducer 2 controls carbohydrate metabolism and biofilm formation with Porphyromonas gingivalis. J Bacteriol 185: 274-284.
95. Mireles JR 2nd, Toguchi A & Harshey RM (2001) Salmonella enterica serovar typhimurium swarming mutants with altered biofilm-forming abilities: surfactin inhibits biofilm formation. J Bacteriol 183: 5848-5854.
96. Moons P, Michiels C & Aertsen A (2009) Bacterial interactions in biofilms. Crit Rev Microbiol 35: 157-168.
97. Mowat E, Rajendran R, Williams C, McCulloch E, Jones B, Lang S & Ramage G (2010) Pseudomonas aeruginosa and their small diffusible extracellular molecules inhibit Aspergillus fumigatus biofilm formation. FEMS Microbiol Lett 313: 96-102.
98. Murthy AK, Chaganty BK, Troutman T, Guentzel MN, Yu JJ, Ali SK, Lauriano CM, Chambers JP, Klose KE & Arulanandam BP (2011) Mannose-containing oligosaccharides of non-specific human secretory immunoglobulin A mediate inhibition of Vibrio cholerae biofilm formation. PLoS ONE 6: e16847.
99. Musthafa KS, Saroja V, Pandian SK & Ravi AV (2011) Antipathogenic potential of marine Bacillus sp. SS4 on N-acyl-homoserine-lactone-mediated virulence factors production in Pseudomonas aeruginosa (PAO1). J Biosci 36: 55-67.
100. Naves P, del Prado G, Huelves L, Rodriguez-Cerrato V, Ruiz V, Ponte MC & Soriano F (2010) Effects of human serum albumin, ibuprofen and N-acetyl-L-cysteine against biofilm formation by pathogenic Escherichia coli strains. J Hosp Infect 76: 165-170.
101. Neu TR (1996) Significance of bacterial surface-active compounds in interaction of bacteria with interfaces. Microbiol Rev 60: 151-166.
102. Nijland R, Hall MJ & Burgess JG (2010) Dispersal of biofilms by secreted, matrix degrading, bacterial DNase. PLoS ONE 5: e15668.
103. Nithya C, Aravindraja C & Pandian SK (2010a) Bacillus pumilus of Palk Bay origin inhibits quorum-sensing-mediated virulence factors in Gram-negative bacteria. Res Microbiol 161: 293-304.
104. Nithya C, Begum MF & Pandian SK (2010b) Marine bacterial isolates inhibit biofilm formation and disrupt mature biofilms of Pseudomonas aeruginosa PAO1. Appl Microbiol Biotechnol 88: 341-358.
105. Nithya C, Devi MG & Karutha Pandian S (2011) A novel compound from the marine bacterium Bacillus pumilus S6-15 inhibits biofilm formation in Gram-positive and Gram-negative species. Biofouling 27: 519-528.
106. Nithyanand P, Thenmozhi R, Rathna J & Pandian SK (2010) Inhibition of Streptococcus pyogenes biofilm formation by coral-associated actinomycetes. Current Microbiology 60: 454-460.
107. Ogawa A, Furukawa S, Fujita S et al. (2011) Inhibition of Streptococcus mutans biofilm formation by Streptococcus salivarius FruA. Appl Environ Microbiol 77: 1572-1580.
108. Orgaz B, Kives J, Pedregosa AM, Monistrol IF, Laborda F & SanJos CÉ (2006) Bacterial biofilm removal using fungal enzymes. Enzyme Microb Technol 40: 51-56.
109. Otto M (2008) Staphylococcal biofilms. Curr Top Microbiol Immunol 322: 207-228.
110. Parsek MR & Singh PK (2003) Bacterial biofilms: an emerging link to disease pathogenesis. Annu Rev Microbiol 57: 677-701.
111. 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.
112. Peters L, Konig GM, Wright AD, Pukall R, Stackebrandt E, Eberl L & Riedel K (2003) Secondary metabolites of Flustra foliacea and their influence on bacteria. Appl Environ Microbiol 69: 3469-3475.
113. Pinkner JS, Remaut H, Buelens F et al. (2006) Rationally designed small compounds inhibit pilus biogenesis in uropathogenic bacteria. P Natl Acad Sci USA 103: 17897-17902.
114. Qin Z, Yang L, Qu D, Molin S & Tolker-Nielsen T (2009) Pseudomonas aeruginosa extracellular products inhibit staphylococcal growth, and disrupt established biofilms produced by Staphylococcus epidermidis. Microbiology 155: 2148-2156.
115. Quigley EM (2010) Prebiotics and probiotics; modifying and mining the microbiota. Pharmacol Res 61: 213-218.
116. Rasko DA & Sperandio V (2010) Anti-virulence strategies to combat bacteria-mediated disease. Nat Rev Drug Discov 9: 117-128.
117. Reen FJ, Mooij MJ, Holcombe LJ, McSweeney CM, McGlacken GP, Morrissey JP & O'Gara F (2011) The Pseudomonas quinolone signal (PQS), and its precursor HHQ, modulate interspecies and interkingdom behaviour. FEMS Microbiol Ecol 77: 413-428.
118. Reid G, Howard J & Gan BS (2001) Can bacterial interference prevent infection? Trends Microbiol 9: 424-428.
119. Rendueles O, Travier L, Latour-Lambert P, Fontaine T, Magnus J, Denamur E & Ghigo JM (2011) Screening of Escherichia coli species biodiversity reveals new biofilm-associated antiadhesion polysaccharides. MBio 2: e00043-11.
120. Rice SA, Koh KS, Queck SY, Labbate M, Lam KW & Kjelleberg S (2005) Biofilm formation and sloughing in Serratia marcescens are controlled by quorum sensing and nutrient cues. J Bacteriol 187: 3477-3485.
121. Rivardo F, Turner RJ, Allegrone G, Ceri H & Martinotti MG (2009) Anti-adhesion activity of two biosurfactants produced by Bacillus spp. prevents biofilm formation of human bacterial pathogens. Appl Microbiol Biotechnol 83: 541-553.
122. Rodrigues L, Banat IM, Teixeira J & Oliveira R (2006a) Biosurfactants: potential applications in medicine. J Antimicrob Chemother 57: 609-618.
123. Rodrigues L, van der Mei H, Banat IM, Teixeira J & Oliveira R (2006b) Inhibition of microbial adhesion to silicone rubber treated with biosurfactant from Streptococcus thermophilus A. FEMS Immunol Med Microbiol 46: 107-112.
124. Rodrigues LR, Teixeira JA, van der Mei HC & Oliveira R (2006c) Isolation and partial characterization of a biosurfactant produced by Streptococcus thermophilus A. Colloids Surf B Biointerfaces 53: 105-112.
125. Romero D & Kolter R (2011) Will biofilm disassembly agents make it to market? Trends Microbiol 19: 304-306.
126. Romero D, Vlamakis H, Losick R & Kolter R (2011) An accessory protein required for anchoring and assembly of amyloid fibres in B. subtilis biofilms. Mol Microbiol 80: 1155-1168.
127. Rowland I, Capurso L, Collins K, Cummings J, Delzenne N, Goulet O, Guarner F, Marteau P & Meier R (2010) Current level of consensus on probiotic science-report of an expert meeting-London, 23 November 2009. Gut microbes 1: 436-439.
128. Ryan RP & Dow JM (2011) Communication with a growing family: diffusible signal factor (DSF) signaling in bacteria. Trends Microbiol 19: 145-152.
129. Ryan RP, Fouhy Y, Garcia BF, Watt SA, Niehaus K, Yang L, Tolker-Nielsen T & Dow JM (2008) Interspecies signalling via the Stenotrophomonas maltophilia diffusible signal factor influences biofilm formation and polymyxin tolerance in Pseudomonas aeruginosa. Mol Microbiol 68: 75-86.
130. Sanz Y, Nadal I & Sanchez E (2007) Probiotics as drugs against human gastrointestinal infections. Recent Pat Antiinfect Drug Discov 2: 148-156.
131. Sayem SM, Manzo E, Ciavatta L, Tramice A, Cordone A, Zanfardino A, De Felice M & Varcamonti M (2011) Anti-biofilm activity of an exopolysaccharide from a sponge-associated strain of Bacillus licheniformis. Microb Cell Fact 10: 74.
132. Schembri MA, Kjaergaard K & Klemm P (2003) Global gene expression in Escherichia coli biofilms. Mol Microbiol 48: 253-267.
133. Schillaci D (2011) Staphylococcal biofilms: challenges in the discovery of novel anti-infective agents. J Microbial Biochem Technol 3: iv-vi.
134. Senadheera D & Cvitkovitch DG (2008) Quorum sensing and biofilm formation by Streptococcus mutans. Adv Exp Med Biol 631: 178-188.
135. Singh PK (2004) Iron sequestration by human lactoferrin stimulates P. aeruginosa surface motility and blocks biofilm formation. Biometals 17: 267-270.
136. Singh PK, Parsek MR, Greenberg EP & Welsh MJ (2002) A component of innate immunity prevents bacterial biofilm development. Nature 417: 552-555.
137. Slater H, Alvarez-Morales A, Barber CE, Daniels MJ & Dow JM (2000) A two-component system involving an HD-GYP domain protein links cell-cell signalling to pathogenicity gene expression in Xanthomonas campestris. Mol Microbiol 38: 986-1003.
138. Sockett RE (2009) Predatory lifestyle of Bdellovibrio bacteriovorus. Annu Rev Microbiol 63: 523-539.
139. Soderling EM, Marttinen AM & Haukioja AL (2011) Probiotic lactobacilli interfere with Streptococcus mutans biofilm formation in vitro. Current Microbiology 62: 618-622.
140. Sutherland I (2001) Biofilm exopolysaccharides: a strong and sticky framework. Microbiology 147: 3-9.
141. Tamura S, Yonezawa H, Motegi M, Nakao R, Yoneda S, Watanabe H, Yamazaki T & Senpuku H (2009) Inhibiting effects of Streptococcus salivarius on competence-stimulating peptide-dependent biofilm formation by Streptococcus mutans. Oral Microbiol Immunol 24: 152-161.
142. Tang J, Kang M, Chen H, Shi X, Zhou R, Chen J & Du Y (2011) The staphylococcal nuclease prevents biofilm formation in Staphylococcus aureus and other biofilm-forming bacteria. Sci China Life Sci 54: 863-869.
143. Thenmozhi R, Nithyanand P, Rathna J & Pandian SK (2009) Antibiofilm activity of coral-associated bacteria against different clinical M serotypes of Streptococcus pyogenes. FEMS Immunol Med Microbiol 57: 284-294.
144. Valle J, Da Re S, Henry N, Fontaine T, Balestrino D, Latour-Lambert P & Ghigo J (2006) Broad-spectrum biofilm inhibition by a secreted bacterial polysaccharide. P Natl Acad Sci USA 103: 12558-12563.
145. Valle J, Da Re S, Schmid S, Skurnik D, D'Ari R & Ghigo J (2008) The amino acid valine is secreted in continuous-flow bacterial biofilms. J Bacteriol 190: 264-274.
146. Velraeds MM, van der Mei HC, Reid G & Busscher HJ (1996) Inhibition of initial adhesion of uropathogenic Enterococcus faecalis by biosurfactants from Lactobacillus isolates. Appl Environ Microbiol 62: 1958-1963.
147. Walencka E, Rozalska S, Sadowska B & Rozalska B (2008a) The influence of Lactobacillus acidophilus-derived surfactants on staphylococcal adhesion and biofilm formation. Folia Microbiol (Praha) 53: 61-66.
148. Walencka E, Sadowska B, Wieckowska-Szakiel M & Rozalska B (2008b) [Activity of indolicidin, alone or together with oxacillin, against Staphylococcus aureus and S. epidermidis]. Med Dosw Mikrobiol 60: 191-196.
149. Wang LH, He Y, Gao Y et al. (2004) A bacterial cell-cell communication signal with cross-kingdom structural analogues. Mol Microbiol 51: 903-912.
150. Wang BY, Deutch A, Hong J & Kuramitsu HK (2011) Proteases of an early colonizer can hinder Streptococcus mutans colonization in vitro. J Dent Res 90: 501-505.
151. Whitchurch CB, Tolker-Nielsen T & Ragas PC (2002) Extracellular DNA required for bacterial biofilm formation. Science 295: 1487.
152. 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.
153. Whitfield C (2006) Biosynthesis and assembly of capsular polysaccharides in Escherichia coli. Annu Rev Biochem 75: 39-68.
154. Wu J & Xie H (2010) Role of arginine deiminase of Streptococcus cristatus in Porphyromonas gingivalis colonization. Antimicrob Agents Chemother 54: 4694-4698.
155. Xie H, Cook GS, Costerton JW, Bruce G, Rose TM & Lamont RJ (2000) Intergeneric communication in dental plaque biofilms. J Bacteriol 182: 7067-7069.
156. Xie H, Lin X, Wang BY, Wu J & Lamont RJ (2007) Identification of a signalling molecule involved in bacterial intergeneric communication. Microbiology 153: 3228-3234.
157. Xu H & Liu Y (2011) D-Amino acid mitigated membrane biofouling and promoted biofilm detachment. Anglais 376: 9.
158. Xun LY, Mah RA & Boone DR (1990) Isolation and characterization of disaggregatase from Methanosarcina mazei LYC. Appl Environ Microbiol 56: 3693-3698.
159. Yan L, Boyd KG, Adams DR & Burgess JG (2003) Biofilm-specific cross-species induction of antimicrobial compounds in bacilli. Appl Environ Microbiol 69: 3719-3727.
160. You J, Xue X, Cao L, Lu X, Wang J, Zhang L & Zhou S (2007) Inhibition of Vibrio biofilm formation by a marine actinomycete strain A66. Appl Microbiol Biotechnol 76: 1137-1144.
161. Zeraik AE & Nitschke M (2010) Biosurfactants as agents to reduce adhesion of pathogenic bacteria to polystyrene surfaces: effect of temperature and hydrophobicity. Curr Microbiol 61: 554-559.
162. Zinger-Yosovich KD, Iluz D, Sudakevitz D & Gilboa-Garber N (2010) Blocking of Pseudomonas aeruginosa and Chromobacterium violaceum lectins by diverse mammalian milks. J Dairy Sci 93: 473-482.