No metrics data to plot.
The attempt to load metrics for this article has failed.
The attempt to plot a graph for these metrics has failed.

Mechanisms of Competition in Biofilm Communities

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.
  • PDF
    442.19 Kb
  • HTML
    177.41 Kb
  • XML
    178.48 Kb
  • Authors: Olaya Rendueles1, Jean-Marc Ghigo2
  • Editors: Mahmoud Ghannoum3, Matthew Parsek4, Marvin Whiteley5, Pranab Mukherjee6
    Affiliations: 1: Institute for Integrative Biology, ETH Zürich, 8092 Zürich, Switzerland; 2: Institut Pasteur, Unité de Génétique des Biofilms, Département de Microbiologie, F-75015 Paris, France; 3: Case Western Reserve University, Cleveland, OH; 4: University of Washington, Seattle, WA; 5: University of Texas at Austin, Austin, TX; 6: Case Western Reserve University, Cleveland, OH
  • Source: microbiolspec June 2015 vol. 3 no. 3 doi:10.1128/microbiolspec.MB-0009-2014
  • Received 13 August 2014 Accepted 17 February 2015 Published 26 June 2015
  • Jean-Marc Ghigo, [email protected]
image of Mechanisms of Competition in Biofilm Communities
    Preview this microbiology spectrum article:
    Zoom in

    Mechanisms of Competition in Biofilm Communities, Page 1 of 2

    | /docserver/preview/fulltext/microbiolspec/3/3/MB-0009-2014-1.gif /docserver/preview/fulltext/microbiolspec/3/3/MB-0009-2014-2.gif
  • Abstract:

    Bacterial biofilms are dense and often mixed-species surface-attached communities in which bacteria coexist and compete for limited space and nutrients. Here we present the different antagonistic interactions described in biofilm environments and their underlying molecular mechanisms, along with ecological and evolutionary insights as to how competitive interactions arise and are maintained within biofilms.

  • Citation: Rendueles O, Ghigo J. 2015. Mechanisms of Competition in Biofilm Communities. Microbiol Spectrum 3(3):MB-0009-2014. doi:10.1128/microbiolspec.MB-0009-2014.


1. Darwin C. 1859. On the Origin of Species by Means of Natural Selection, or the Preservation of Favored Races in the Struggle for Life. John Murray, London.
2. Davey ME, O’Toole GA. 2000. Microbial biofilms: from ecology to molecular genetics. Microbiol Mol Biol Rev 64:847–867. [PubMed][CrossRef]
3. Zengler K, Palsson BO. 2012. A road map for the development of community systems (CoSy) biology. Nat Rev Microbiol 10:366–372. [PubMed][CrossRef]
4. Burmølle M, Ren D, Bjarnsholt T, Sørensen SJ. 2014. Interactions in multispecies biofilms: do they actually matter? Trends Microbiol 22:84–91. [PubMed][CrossRef]
5. Elias S, Banin E. 2012. Multi-species biofilms: living with friendly neighbors. FEMS Microbiol Rev 36:990–1004. [PubMed][CrossRef]
6. Foster KR, Bell T. 2012. Competition, not cooperation, dominates interactions among culturable microbial species. Curr Biol 22:1845–1850. [PubMed][CrossRef]
7. Lawrence D, Fiegna F, Behrends V, Bundy JG, Phillimore AB, Bell T, Barraclough TG. 2012. Species interactions alter evolutionary responses to a novel environment. PLoS Biol 10:e1001330. doi:10.1371/journal.pbio.1001330. [PubMed][CrossRef]
8. Allee WC, Bowen E. 1932. Studies in animal aggregations: mass protection against colloidal silver among goldfishes. J Exp Zool 61:185–207. [CrossRef]
9. Ruxton GD, Sherratt TN. 2006. Aggregation, defence and warning signals: the evolutionary relationship. Proc Biol Sci 273:2417–2424. [PubMed][CrossRef]
10. Gascoigne J, Berec L, Gregory S, Courchamp F. 2009. Dangerously few liaisons: a review of mate-finding Allee effects. Popul Ecol 51:355–372. [CrossRef]
11. Potts M. 1994. Desiccation tolerance of prokaryotes. Microbiol Rev 58:755–805. [PubMed]
12. Li YH, Hanna MN, Svensater G, Ellen RP, Cvitkovitch DG. 2001. Cell density modulates acid adaptation in Streptococcus mutans: implications for survival in biofilms. J Bacteriol 183:6875–6884. [PubMed][CrossRef]
13. Smith R, Tan CM, Srimani JK, Pai A, Riccione KA, Song H, You LC. 2014. Programmed Allee effect in bacteria causes a tradeoff between population spread and survival. Proc Natl Acad Sci USA 111:1969–1974. [PubMed][CrossRef]
14. Butler MT, Wang Q, Harshey RM. 2010. Cell density and mobility protect swarming bacteria against antibiotics. Proc Natl Acad Sci USA 107:3776–3781. [PubMed][CrossRef]
15. Julou T, Mora T, Guillon L, Croquette V, Schalk IJ, Bensimon D, Desprat N. 2013. Cell-cell contacts confine public goods diffusion inside Pseudomonas aeruginosa clonal microcolonies. Proc Natl Acad Sci USA 110:12577–12582. [PubMed][CrossRef]
16. Darch SE, West SA, Winzer K, Diggle SP. 2012. Density-dependent fitness benefits in quorum-sensing bacterial populations. Proc Natl Acad Sci USA 109:8259–8263. [PubMed][CrossRef]
17. Taylor PD. 1992. Altruism in viscous populations: an inclusive fitness model. Evol Ecol 6:352–356. [CrossRef]
18. Whittaker CJ, Klier CM, Kolenbrander PE. 1996. Mechanisms of adhesion by oral bacteria. Annu Rev Microbiol 50:513–552. [PubMed][CrossRef]
19. Poltak SR, Cooper VS. 2011. Ecological succession in long-term experimentally evolved biofilms produces synergistic communities. ISME J 5:369–378. [PubMed][CrossRef]
20. Ramsey MM, Rumbaugh KP, Whiteley M. 2011 Metabolite cross-feeding enhances virulence in a model polymicrobial infection. PLoS Pathog 7:e1002012. doi:10.1371/journal.ppat.1002012. [CrossRef]
21. Breugelmans P, Barken KB, Tolker-Nielsen T, Hofkens J, Dejonghe W, Springael D. 2008. Architecture and spatial organization in a triple-species bacterial biofilm synergistically degrading the phenylurea herbicide linuron. FEMS Microbiol Ecol 64:271–282. [PubMed][CrossRef]
22. Burmolle M, Webb JS, Rao D, Hansen LH, Sorensen SJ, Kjelleberg S. 2006. Enhanced biofilm formation and increased resistance to antimicrobial agents and bacterial invasion are caused by synergistic interactions in multispecies biofilms. Appl Environ Microbiol 72:3916–3923. [PubMed][CrossRef]
23. Whiteley M, Ott JR, Weaver EA, McLean RJ. 2001. Effects of community composition and growth rate on aquifer biofilm bacteria and their susceptibility to betadine disinfection. Environ Microbiol 3:43–52. [PubMed][CrossRef]
24. Sutherland I. 2001. Biofilm exopolysaccharides: a strong and sticky framework. Microbiology 147:3–9. [PubMed]
25. Hamilton WD. 1964. The genetical evolution of social behaviour. I & II. J Theor Biol 7:1–52. [CrossRef]
26. Foster K. 2005. Biomedicine. Hamiltonian medicine: why the social lives of pathogens matter. Science 308:1269–1270. [PubMed][CrossRef]
27. Nowak MA, May RM. 1992. Evolutionary games and spatial chaos. Nature 359:826–829. [CrossRef]
28. Doebeli M, Knowlton N. 1998. The evolution of interspecific mutualisms. Proc Natl Acad Sci USA 95:8676–8680. [PubMed][CrossRef]
29. Travisano M, Velicer GJ. 2004. Strategies of microbial cheater control. Trends Microbiol 12:72–78. [PubMed][CrossRef]
30. Manhes P, Velicer GJ. 2011. Experimental evolution of selfish policing in social bacteria. Proc Natl Acad Sci USA 108:8357–8362. [PubMed][CrossRef]
31. Strassmann JE, Gilbert OM, Queller DC. 2011. Kin discrimination and cooperation in microbes. Annu Rev Microbiol 65:349–367. [PubMed][CrossRef]
32. Nadell CD, Foster KR, Xavier JB. 2010. Emergence of spatial structure in cell groups and the evolution of cooperation. PLoS Comput Biol 6:e1000716. doi:10.1371/journal.pcbi.1000716. [PubMed][CrossRef]
33. Drescher K, Nadell CD, Stone HA, Wingreen NS, Bassler BL. 2014. Solutions to the public goods dilemma in bacterial biofilms. Curr Biol 24:50–55. [PubMed][CrossRef]
34. Griffin AS, West SA, Buckling A. 2004. Cooperation and competition in pathogenic bacteria. Nature 430:1024–1027. [PubMed][CrossRef]
35. West SA, Pen I, Griffin AS. 2002. Conflict and cooperation: cooperation and competition between relatives. Science 296:72–75. [PubMed][CrossRef]
36. Leigh EG. 2010. The evolution of mutualism. J Evol Biol 23:2507–2528. [PubMed][CrossRef]
37. Platt TG, Bever JD. 2009. Kin competition and the evolution of cooperation. Trends Ecol Evol 24:370–377. [PubMed][CrossRef]
38. Inglis RF, Brown SP, Buckling A. 2012. Spite versus cheats: competition among social strategies shapes virulence in Pseudomonas aeruginosa. Evolution 66:3472–3484. [PubMed][CrossRef]
39. Harrison F, Paul J, Massey RC, Buckling A. 2008. Interspecific competition and siderophore-mediated cooperation in Pseudomonas aeruginosa. ISME J 2:49–55. [PubMed][CrossRef]
40. Mitri S, Xavier JB, Foster KR. 2011. Social evolution in multispecies biofilms. Proc Natl Acad Sci USA 108(Suppl 2) :10839–10846. [PubMed][CrossRef]
41. Stewart PS. 2003. Diffusion in biofilms. J Bacteriol 185:1485–1491. [PubMed][CrossRef]
42. Korona R, Nakatsu CH, Forney LJ, Lenski RE. 1994. Evidence for multiple adaptive peaks from populations of bacteria evolving in a structured habitat. Proc Natl Acad Sci USA 91:9037–9041. [PubMed][CrossRef]
43. Boles BR, Thoendel M, Singh PK. 2004. Self-generated diversity produces “insurance effects” in biofilm communities. Proc Natl Acad Sci USA 101:16630–16635. [PubMed][CrossRef]
44. Rainey PB, Travisano M. Adaptive radiation in a heterogeneous environment. Nature 394:69–72. [PubMed][CrossRef]
45. Kerr B, Riley MA, Feldman MW, Bohannan BJ. 2002. Local dispersal promotes biodiversity in a real-life game of rock-paper-scissors. Nature 418:171–174. [PubMed][CrossRef]
46. Li K, Bihan M, Yooseph S, Methe BA. 2012. Analyses of the microbial diversity across the human microbiome. PLoS One 7:e32118. doi:10.1371/journal.pone.0032118. [PubMed][CrossRef]
47. 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. [PubMed][CrossRef]
48. Whiteley M, Bangera MG, Bumgarner RE, Parsek MR, Teitzel GM, Lory S, Greenberg EP. 2001. Gene expression in Pseudomonas aeruginosa biofilms. Nature 413:860–864. [PubMed][CrossRef]
49. Lazazzera BA. 2005. Lessons from DNA microarray analysis: the gene expression profile of biofilms. Curr Opin Microbiol 8:222–227. [PubMed][CrossRef]
50. Schembri MA, Kjaergaard K, Klemm P. 2003. Global gene expression in Escherichia coli biofilms. Mol Microbiol 48:253–267. [PubMed][CrossRef]
51. Marks, LR, Davidson BA, Knight PR, Hakansson AP. 2013. Interkingdom signaling induces Streptococcus pneumoniae biofilm dispersion and transition from asymptomatic colonization to disease. MBio 4:e00438-13. doi:10.1128/mBio.00438-13. [CrossRef]
52. Campisano A, Overhage J, Rehm BH. 2008. The polyhydroxyalkanoate biosynthesis genes are differentially regulated in planktonic- and biofilm-grown Pseudomonas aeruginosa. J Biotechnol 133:442–452. [PubMed][CrossRef]
53. Lequette Y, Greenberg EP. 2005. Timing and localization of rhamnolipid synthesis gene expression in Pseudomonas aeruginosa biofilms. J Bacteriol 187:37–44. [PubMed][CrossRef]
54. Ghigo J-M. 2003. Are there biofilm-specific physiological pathways beyond a reasonable doubt? Res Microbiol 154:1–8. [PubMed][CrossRef]
55. Case TJ, Gilpin ME. 1974. Interference competition and niche theory. Proc Natl Acad Sci USA 71:3073–3077. [PubMed][CrossRef]
56. Vance RR. 1984. Interference competition and the coexistence of two competitors on a single limiting resource. Ecology 65:1349–1357. [CrossRef]
57. Cornforth DM, Foster KR. 2013. Competition sensing: the social side of bacterial stress responses. Nat Rev Microbiol 11:285–293. [PubMed][CrossRef]
58. Rendueles O, Ghigo JM. 2012. Multi-species biofilms: how to avoid unfriendly neighbors. FEMS Microbiol Rev 36:972–989. [PubMed][CrossRef]
59. Amarasekare P. 2002. Interference competition and species coexistence. Proc Biol Sci 269:2541–2550. [PubMed][CrossRef]
60. Yamamoto K, Haruta S, Kato S, Ishii M, Igarashi Y. 2010. Determinative factors of competitive advantage between aerobic bacteria for niches at the air-liquid interface. Microbes Environ 25:317–320. [PubMed][CrossRef]
61. Bradshawa DJ, Marsha PD, Hodgson RJ, Visser JM. 2002. Effects of glucose and fluoride on competition and metabolism within in vitro dental bacterial communities and biofilms. Caries Res 36:81–86. [PubMed][CrossRef]
62. Oehmen A, Lemos PC, Carvalho G, Yuan Z, Keller J, Blackall LL, Reis MA. 2007. Advances in enhanced biological phosphorus removal: from micro to macro scale. Water Res 41:2271–2300. [PubMed][CrossRef]
63. Weaver VB, Kolter R. 2004. Burkholderia spp. alter Pseudomonas aeruginosa physiology through iron sequestration. J Bacteriol 186:2376–2384. [PubMed][CrossRef]
64. Eberl HJ, Collinson S. 2009. A modeling and simulation study of siderophore mediated antagonism in dual-species biofilms. Theor Biol Med Model 6:30. [PubMed][CrossRef]
65. Rendueles O, Beloin C, Latour-Lambert P, Ghigo JM. 2014. A new biofilm-associated colicin with increased efficiency against biofilm bacteria. ISME J 8:1275–1288. [PubMed][CrossRef]
66. 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. [PubMed][CrossRef]
67. Valle J, Da Re S, Schmid S, Skurnik D, D’Ari R, Ghigo JM. 2008. The amino acid valine is secreted in continuous-flow bacterial biofilms. J Bacteriol 190:264–274. [PubMed][CrossRef]
68. Graver MA, Wade JJ. 2011. The role of acidification in the inhibition of Neisseria gonorrhoeae by vaginal lactobacilli during anaerobic growth. Ann Clin Microbiol Antimicrob 10:8. [PubMed][CrossRef]
69. Létoffé S, Audrain B, Bernier SP, Delepierre M, Ghigo JM. 2014. Aerial exposure to the bacterial volatile compound trimethylamine modifies antibiotic resistance of physically separated bacteria by raising culture medium pH. MBio 5:e00944-13. doi:10.1128/mBio.00944-13. [CrossRef]
70. Pericone CD, Overweg K, Hermans PW, Weiser JN. 2000. Inhibitory and bactericidal effects of hydrogen peroxide production by Streptococcus pneumoniae on other inhabitants of the upper respiratory tract. Infect Immun 68:3990–3997. [PubMed][CrossRef]
71. Kreth J, Zhang Y, Herzberg MC. 2008. Streptococcal antagonism in oral biofilms: Streptococcus sanguinis and Streptococcus gordonii interference with Streptococcus mutans. J Bacteriol 190:4632–4640. [PubMed][CrossRef]
72. Gillor O, Kirkup BC, Riley MA. 2004. Colicins and microcins: the next generation antimicrobials. Adv Appl Microbiol 54:129–146. [PubMed][CrossRef]
73. Cascales E, Buchanan SK, Duche D, Kleanthous C, Lloubes R, Postle K, Riley M, Slatin S, Cavard D. 2007. Colicin biology. Microbiol Mol Biol Rev 71:158–229. [PubMed][CrossRef]
74. Gordon DM, Riley MA. 1999. A theoretical and empirical investigation of the invasion dynamics of colicinogeny. Microbiology 145:655–661. [PubMed][CrossRef]
75. Riley MA, Gordon DM. 1999. The ecological role of bacteriocins in bacterial competition. Trends Microbiol 7:129–133. [PubMed][CrossRef]
76. Gillor O, Vriezen JA, Riley MA. 2008. The role of SOS boxes in enteric bacteriocin regulation. Microbiology 154:1783–1792. [PubMed][CrossRef]
77. Bernier SP, Lebeaux D, DeFrancesco AS, Valomon A, Soubigou G, Coppee JY, Ghigo JM, Beloin C. 2013. Starvation, together with the SOS response, mediates high biofilm-specific tolerance to the fluoroquinolone ofloxacin. PLoS Genet 9:e1003144. doi:10.1371/journal.pgen.1003144. [PubMed][CrossRef]
78. Majeed H, Gillor O, Kerr B, Riley MA. 2011. Competitive interactions in Escherichia coli populations: the role of bacteriocins. ISME J 5:71–81. [PubMed][CrossRef]
79. Gillor O, Etzion A, Riley MA. 2008. The dual role of bacteriocins as anti- and probiotics. Appl Microbiol Biotechnol 81:591–606. [PubMed][CrossRef]
80. Qi F, Chen P, Caufield PW. 2000. Purification and biochemical characterization of mutacin I from the group I strain of Streptococcus mutans, CH43, and genetic analysis of mutacin I biosynthesis genes. Appl Environ Microbiol 66:3221–3229. [PubMed][CrossRef]
81. Aoki SK, Pamma R, Hernday AD, Bickham JE, Braaten BA, Low DA. 2005. Contact-dependent inhibition of growth in Escherichia coli. Science 309:1245–1248. [PubMed][CrossRef]
82. Aoki SK, Diner EJ, de Roodenbeke CT, Burgess BR, Poole SJ, Braaten BA, Jones AM, Webb JS, Hayes CS, Cotter PA, Low DA. 2010. A widespread family of polymorphic contact-dependent toxin delivery systems in bacteria. Nature 468:439–442. [PubMed][CrossRef]
83. Aoki SK, Malinverni JC, Jacoby K, Thomas B, Pamma R, Trinh BN, Remers S, Webb J, Braaten BA, Silhavy TJ, Low DA. 2008. Contact-dependent growth inhibition requires the essential outer membrane protein BamA (YaeT) as the receptor and the inner membrane transport protein AcrB. Mol Microbiol 70:323–340. [PubMed][CrossRef]
84. Anderson MS, Garcia EC, Cotter PA. 2014. Kind discrimination and competitive exclusion mediated by contact-dependent growth inhibition systems shape biofilm community structure. PLoS Pathog 10:e1004076. doi:10.1371/journal.ppat.1004076. [CrossRef]
85. Lemonnier M, Levin BR, Romeo T, Garner K, Baquero MR, Mercante J, Lemichez E, Baquero F, Blazquez J. 2008. The evolution of contact-dependent inhibition in non-growing populations of Escherichia coli. Proc Biol Sci 275:3–10. [PubMed][CrossRef]
86. Waite RD, Papakonstantinopoulou A, Littler E, Curtis MA. 2005. Transcriptome analysis of Pseudomonas aeruginosa growth: comparison of gene expression in planktonic cultures and developing and mature biofilms. J Bacteriol 187:6571–6576. [PubMed][CrossRef]
87. Kapitein N, Mogk A. 2013. Deadly syringes: type VI secretion system activities in pathogenicity and interbacterial competition. Curr Opin Microbiol 16:52–58. [PubMed][CrossRef]
88. Pukatzki S, Ma AT, Sturtevant D, Krastins B, Sarracino D, Nelson WC, Heidelberg JF, Mekalanos JJ. 2006. Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system. Proc Natl Acad Sci USA 103:1528–1533. [PubMed][CrossRef]
89. Ho BT, Dong TG, Mekalanos JJ. 2014. A view to a kill: the bacterial type VI secretion system. Cell Host Microbe 15:9–21. [PubMed][CrossRef]
90. Schwarz S, West TE, Boyer F, Chiang WC, Carl MA, Hood RD, Rohmer L, Tolker-Nielsen T, Skerrett SJ, Mougous JD. 2010. Burkholderia type VI secretion systems have distinct roles in eukaryotic and bacterial cell interactions. PLoS Pathog 6:e1001068. doi:10.1371/journal.ppat.1001068. [PubMed][CrossRef]
91. Berleman JE, Kirby JR. 2009. Deciphering the hunting strategy of a bacterial wolfpack. FEMS Microbiol Rev 33:942–957. [PubMed][CrossRef]
92. Krug D, Zurek G, Revermann O, Vos M, Velicer GJ, Muller R. 2008. Discovering the hidden secondary metabolome of Myxococcus xanthus: a study of intraspecific diversity. Appl Environ Microbiol 74:3058–3068. [PubMed][CrossRef]
93. Xiao Y, Wei X, Ebright R, Wall D. 2011. Antibiotic production by myxobacteria plays a role in predation. J Bacteriol 193:4626–4633. [PubMed][CrossRef]
94. Morgan AD, MacLean RC, Hillesland KL, Velicer GJ. 2010. Comparative analysis of myxococcus predation on soil bacteria. Appl Environ Microbiol 76:6920–6927. [PubMed][CrossRef]
95. Cusumano CK, Hultgren SJ. 2009. Bacterial adhesion: a source of alternate antibiotic targets. IDrugs 12:699–705. [PubMed]
96. LaSarre B, Federle MJ. 2013. Exploiting quorum sensing to confuse bacterial pathogens. Microbiol Mol Biol Rev 77:73–111. [PubMed][CrossRef]
97. Rasko DA, Sperandio V. 2010. Anti-virulence strategies to combat bacteria-mediated disease. Nat Rev Drug Discov 9:117–128. [PubMed][CrossRef]
98. Bassler BL, Losick R. 2006. Bacterially speaking. Cell 125:237–246. [PubMed][CrossRef]
99. Fuqua C, Greenberg EP. 2002. Listening in on bacteria: acyl-homoserine lactone signalling. Nat Rev Mol Cell Biol 3:685–695. [PubMed][CrossRef]
100. Davies DG, Parsek MR, Pearson JP, Iglewski BH, Costerton JW, Greenberg EP. 1998. The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280:295–298. [PubMed][CrossRef]
101. Bijtenhoorn P, Schipper C, Hornung C, Quitschau M, Grond S, Weiland N, Streit W. 2011. BpiB05, a novel metagenome-derived hydrolase acting on N-acylhomoserine lactones. J Biotechnol 155:86–94. [PubMed][CrossRef]
102. Dong YH, Wang LY, Zhang LH. 2007. Quorum-quenching microbial infections: mechanisms and implications. Philos Trans R Soc Lond B Biol Sci 362:1201–1211. [PubMed][CrossRef]
103. Shepherd RW, Lindow SE. 2009. Two dissimilar N-acyl-homoserine lactone acylases of Pseudomonas syringae influence colony and biofilm morphology. Appl Environ Microbiol 75:45–53. [PubMed][CrossRef]
104. 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. [PubMed][CrossRef]
105. Augustine N, Kumar P, Thomas S. 2010. Inhibition of Vibrio cholerae biofilm by AiiA enzyme produced from Bacillus spp. Arch Microbiol 192:1019–1022. [PubMed][CrossRef]
106. Chu W, Zere TR, Weber MM, Wood TK, Whiteley M, Hidalgo-Romano B, Valenzuela E, Jr, McLean RJ. 2012. Indole production promotes Escherichia coli mixed-culture growth with Pseudomonas aeruginosa by inhibiting quorum signaling. Appl Environ Microbiol 78:411–419. [PubMed][CrossRef]
107. Senadheera D, Cvitkovitch DG. 2008. Quorum sensing and biofilm formation by Streptococcus mutans. Adv Exp Med Biol 631:178–188. [PubMed][CrossRef]
108. 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. [PubMed][CrossRef]
109. Golberg K, Pavlov V, Marks RS, Kushmaro A. 2013. Coral-associated bacteria, quorum sensing disrupters, and the regulation of biofouling. Biofouling 29:669–682. [PubMed][CrossRef]
110. Wang YJ, Leadbetter JR. 2005. Rapid acyl-homoserine lactone quorum signal biodegradation in diverse soils. Appl Environ Microbiol 71:1291–1299. [PubMed][CrossRef]
111. Garcia-Contreras R, Maeda T, Wood TK. 2013. Resistance to quorum-quenching compounds. Appl Environ Microbiol 79:6840–6846. [PubMed][CrossRef]
112. Maeda T, Garcia-Contreras R, Pu M, Sheng L, Garcia LR, Tomas M, Wood TK. 2012. Quorum quenching quandary: resistance to antivirulence compounds. ISME J 6:493–501. [PubMed][CrossRef]
113. Kalia VC, Wood TK, Kumar P. 2013. Evolution of resistance to quorum-sensing inhibitors. Microb Ecol. [Epub ahead of print.] doi:10.1007/s00248-013-0316-y. [PubMed][CrossRef]
114. 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. [PubMed][CrossRef]
115. Desai JD, Banat IM. 1997. Microbial production of surfactants and their commercial potential. Microbiol Mol Biol Rev 61:47–64. [PubMed]
116. Rendueles O, Kaplan JB, Ghigo JM. 2013. Antibiofilm polysaccharides. Environ Microbiol 15:334–346. [PubMed][CrossRef]
117. 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. doi:10.1128/mBio.00043-11. [CrossRef]
118. Travier L, Rendueles O, Ferrieres L, Herry JM, Ghigo JM. 2013. Escherichia coli resistance to nonbiocidal antibiofilm polysaccharides is rare and mediated by multiple mutations leading to surface physicochemical modifications. Antimicrob Agents Chemother 57:3960–3968. [PubMed][CrossRef]
119. Valle J, Da Re S, Henry N, Fontaine T, Balestrino D, Latour-Lambert P, Ghigo JM. 2006. Broad-spectrum biofilm inhibition by a secreted bacterial polysaccharide. Proc Natl Acad Sci USA 103:12558–12563. [PubMed][CrossRef]
120. 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. [PubMed][CrossRef]
121. Christopher AB, Arndt A, Cugini C, Davey ME. 2010. A streptococcal effector protein that inhibits Porphyromonas gingivalis biofilm development. Microbiology 156:3469–3477. [PubMed][CrossRef]
122. Flemming HC, Wingender J. 2010. The biofilm matrix. Nat Rev Microbiol 8:623–633. [PubMed][CrossRef]
123. Lambert C, Sockett RE. 2013. Nucleases in Bdellovibrio bacteriovorus contribute towards efficient self-biofilm formation and eradication of preformed prey biofilms. FEMS Microbiol Lett 340:109–116. [PubMed][CrossRef]
124. 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. [PubMed][CrossRef]
125. Nijland R, Hall MJ, Burgess JG. 2010. Dispersal of biofilms by secreted, matrix degrading, bacterial DNase. PLoS One 5:e15668. doi:10.1371/journal.pone.0015668. [PubMed][CrossRef]
126. Kaplan JB, Ragunath C, Velliyagounder K, Fine DH, Ramasubbu N. 2004. Enzymatic detachment of Staphylococcus epidermidis biofilms. Antimicrob Agents Chemother 48:2633–2636. [PubMed][CrossRef]
127. Ogawa A, Furukawa S, Fujita S, Mitobe J, Kawarai T, Narisawa N, Sekizuka T, Kuroda M, Ochiai K, Ogihara H, Kosono S, Yoneda S, Watanabe H, Morinaga Y, Uematsu H, Senpuku H. 2011. Inhibition of Streptococcus mutans biofilm formation by Streptococcus salivarius FruA. Appl Environ Microbiol 77:1572–1580. [PubMed][CrossRef]
128. Dusane DH, Damare SR, Nancharaiah YV, Ramaiah N, Venugopalan VP, Kumar AR, Zinjarde SS. 2013. Disruption of microbial biofilms by an extracellular protein isolated from epibiotic tropical marine strain of Bacillus licheniformis. PLoS One 8:e64501. doi:10.1371/journal.pone.0064501. [CrossRef]
129. 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. [PubMed][CrossRef]
130. Sugimoto S, Iwamoto T, Takada K, Okuda K, Tajima A, Iwase T, Mizunoe Y. 2013 Staphylococcus epidermidis Esp degrades specific proteins associated with Staphylococcus aureus biofilm formation and host-pathogen interaction. J Bacteriol 195:1645–1655. [PubMed][CrossRef]
131. McDougald D, Rice SA, Barraud N, Steinberg PD, Kjelleberg S. 2012. Should we stay or should we go: mechanisms and ecological consequences for biofilm dispersal. Nat Rev Microbiol 10:39–50. [PubMed]
132. Wang LH, He Y, Gao Y, Wu JE, Dong YH, He C, Wang SX, Weng LX, Xu JL, Tay L, Fang RX, Zhang L. 2004. A bacterial cell-cell communication signal with cross-kingdom structural analogues. Mol Microbiol 51:903–912. [PubMed][CrossRef]
133. Ryan RP, Dow JM. 2011. Communication with a growing family: diffusible signal factor (DSF) signaling in bacteria. Trends Microbiol 19:145–152. [PubMed][CrossRef]
134. Davies DG, Marques CN. 2009. A fatty acid messenger is responsible for inducing dispersion in microbial biofilms. J Bacteriol 191:1393–1403. [PubMed][CrossRef]
135. Boles BR, Thoendel M, Singh PK. 2005. Rhamnolipids mediate detachment of Pseudomonas aeruginosa from biofilms. Mol Microbiol 57:1210–1223. [PubMed][CrossRef]
136. Irie Y, O’Toole GA, Yuk MH. 2005. Pseudomonas aeruginosa rhamnolipids disperse Bordetella bronchiseptica biofilms. FEMS Microbiol Lett 250:237–243. [PubMed][CrossRef]
137. Barraud N, Schleheck D, Klebensberger J, Webb JS, Hassett DJ, Rice SA, Kjelleberg S. 2009. Nitric oxide signaling in Pseudomonas aeruginosa biofilms mediates phosphodiesterase activity, decreased cyclic di-GMP levels, and enhanced dispersal. J Bacteriol 191:7333–7342. [PubMed][CrossRef]
138. 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. [PubMed][CrossRef]
139. Kolodkin-Gal I, Cao S, Chai L, Bottcher T, Kolter R, Clardy J, Losick R. 2012. A self-produced trigger for biofilm disassembly that targets exopolysaccharide. Cell 149:684–692. [PubMed][CrossRef]
140. Kolodkin-Gal I, Romero D, Cao S, Clardy J, Kolter R, Losick R. 2010. D-amino acids trigger biofilm disassembly. Science 328:627–629. [PubMed][CrossRef]
141. 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. [PubMed][CrossRef]
142. Hobley L, Kim SH, Maezato Y, Wyllie S, Fairlamb AH, Stanley-Wall NR, Michael AJ. 2014. Norspermidine is not a self-produced trigger for biofilm disassembly. Cell 156:844–854. [PubMed][CrossRef]
143. Leiman SA, May JM, Lebar MD, Kahne D, Kolter R, Losick R. 2013. D-amino acids indirectly inhibit biofilm formation in Bacillus subtilis by interfering with protein synthesis. J Bacteriol 195:5391–5395. [PubMed][CrossRef]
144. Taylor TB, Buckling A. 2011. Selection experiments reveal trade-offs between swimming and twitching motilities in Pseudomonas aeruginosa. Evolution 65:3060–3069. [PubMed][CrossRef]
145. van Ditmarsch D, Boyle KE, Sakhtah H, Oyler JE, Nadell CD, Deziel E, Dietrich LE, Xavier JB. 2013. Convergent evolution of hyperswarming leads to impaired biofilm formation in pathogenic bacteria. Cell Rep 4:697–708. [PubMed][CrossRef]
146. Jin F, Conrad JC, Gibiansky ML, Wong GCL. 2011. Bacteria use type-IV pili to slingshot on surfaces. Proc Natl Acad Sci USA 108:12617–12622. [PubMed][CrossRef]
147. An D, Danhorn T, Fuqua C, Parsek MR. 2006. Quorum sensing and motility mediate interactions between Pseudomonas aeruginosa and Agrobacterium tumefaciens in biofilm cocultures. Proc Natl Acad Sci USA 103:3828–3833. [PubMed][CrossRef]
148. Hibbing ME, Fuqua C. 2012. Inhibition and dispersal of Agrobacterium tumefaciens biofilms by a small diffusible Pseudomonas aeruginosa exoproduct(s). Arch Microbiol 194:391–403. [PubMed][CrossRef]
149. Ma Q, Zhang G, Wood TK. 2011. Escherichia coli BdcA controls biofilm dispersal in Pseudomonas aeruginosa and Rhizobium meliloti. BMC Res Notes 4:447. [PubMed][CrossRef]
150. Houry A, Gohar M, Deschamps J, Tischenko E, Aymerich S, Gruss A, Briandet R. 2012. Bacterial swimmers that infiltrate and take over the biofilm matrix. Proc Natl Acad Sci USA 109:13088–13093. [PubMed][CrossRef]
151. Da Re S, Valle J, Charbonnel N, Beloin C, Latour-Lambert P, Faure P, Turlin E, Le Bouguenec C, Renauld-Mongenie G, Forestier C, Ghigo JM. 2013. Identification of commensal Escherichia coli genes involved in biofilm resistance to pathogen colonization. PLoS One 8:e61628. doi:10.1371/journal.pone.0061628. [CrossRef]
152. He X, Tian Y, Guo L, Lux R, Zusman DR, Shi W. 2010. Oral-derived bacterial flora defends its domain by recognizing and killing intruders: a molecular analysis using Escherichia coli as a model intestinal bacterium. Microb Ecol 60:655–664. [PubMed][CrossRef]
153. He X, McLean JS, Guo L, Lux R, Shi W. 2014. The social structure of microbial community involved in colonization resistance. ISME J 8:564–574. [PubMed][CrossRef]
154. Mayr E. 1989. Speciational evolution or punctuated equilibria. J Soc Biol Struct 12:137–158. [CrossRef]
155. Rainey PB, Rainey K. 2003. Evolution of cooperation and conflict in experimental bacterial populations. Nature 425:72–74. [PubMed][CrossRef]
156. Diggle SP, Griffin AS, Campbell GS, West SA. 2007. Cooperation and conflict in quorum-sensing bacterial populations. Nature 450:411–414. [PubMed][CrossRef]
157. MacLean RC, Gudelj I. 2006. Resource competition and social conflict in experimental populations of yeast. Nature 441:498–501. [PubMed][CrossRef]
158. Fagerlind MG, Webb JS, Barraud N, McDougald D, Jansson A, Nilsson P, Harlen M, Kjelleberg S, Rice SA. 2012. Dynamic modelling of cell death during biofilm development. J Theor Biol 295:23–36. [PubMed][CrossRef]
159. Stolyar S, Van Dien S, Hillesland KL, Pinel N, Lie TJ, Leigh JA, Stahl DA. 2007. Metabolic modeling of a mutualistic microbial community. Mol Syst Biol 3:92. [PubMed][CrossRef]
160. Zhuang K, Izallalen M, Mouser P, Richter H, Risso C, Mahadevan R, Lovley DR. 2011. Genome-scale dynamic modeling of the competition between Rhodoferax and Geobacter in anoxic subsurface environments. ISME J 5:305–316. [PubMed][CrossRef]
161. Wanner O, Gujer W. 1986. A multispecies biofilm model. Biotechnol Bioeng 28:314–328. [PubMed][CrossRef]
162. Poplawski NJ, Shirinifard A, Swat M, Glazier JA. 2008. Simulation of single-species bacterial-biofilm growth using the Glazier-Graner-Hogeweg model and the CompuCell3D modeling environment. Math Biosci Eng 5:355–388. [PubMed][CrossRef]
163. Xavier JB, Foster KR. 2007. Cooperation and conflict in microbial biofilms. Proc Natl Acad Sci USA 104:876–881. [PubMed][CrossRef]
164. Nadell CD, Bassler BL. 2011. A fitness trade-off between local competition and dispersal in Vibrio cholerae biofilms. Proc Natl Acad Sci USA 108:14181–14185. [PubMed][CrossRef]
165. Kussell E. 2013. Evolution in microbes. Annu Rev Biophys 42:493–514. [PubMed][CrossRef]
166. Blount ZD, Borland CZ, Lenski RE. 2008. Historical contingency and the evolution of a key innovation in an experimental population of Escherichia coli. Proc Natl Acad Sci USA. 105:7899–7906. [PubMed][CrossRef]
167. Wiser MJ, Ribeck N, Lenski RE. 2013. Long-term dynamics of adaptation in asexual populations. Science 342:1364–1367. [PubMed][CrossRef]
168. Spiers AJ, Kahn SG, Bohannon J, Travisano M, Rainey PB. 2002. Adaptive divergence in experimental populations of Pseudomonas fluorescens. I. Genetic and phenotypic bases of wrinkly spreader fitness. Genetics 161:33–46. [PubMed]
169. Hansen SK, Rainey PB, Haagensen JA, Molin S. 2007. Evolution of species interactions in a biofilm community. Nature 445:533–536. [PubMed][CrossRef]
170. Traverse, CC, Mayo-Smith LM, Poltak SR, Cooper VS. 2013. Tangled bank of experimentally evolved Burkholderia biofilms reflects selection during chronic infections. Proc Natl Acad Sci USA 110:E250–E259. [PubMed][CrossRef]
171. Park SC, Krug J. 2007. Clonal interference in large populations. Proc Natl Acad Sci USA 104:18135–18140. [PubMed][CrossRef]
172. Lee KW, Periasamy S, Mukherjee M, Xie C, Kjelleberg S, Rice SA. 2013. Biofilm development and enhanced stress resistance of a model, mixed-species community biofilm. ISME J. [Epub ahead of print.] doi:10.1038/ismej.2013.194. [PubMed][CrossRef]
173. Turcotte MM, Corrin MSC, Johnson MTJ. 2012. Adaptive evolution in ecological communities. PLoS Biol 10:e1001332. doi:10.1371/journal.pbio.1001332. [PubMed][CrossRef]
174. Boyle KE, Heilmann S, van Ditmarsch D, Xavier JB. 2013. Exploiting social evolution in biofilms. Curr Opin Microbiol 16:207–212. [PubMed][CrossRef]
175. Reid G, Howard J, Gan BS. 2001. Can bacterial interference prevent infection? Trends Microbiol 9:424–428. [PubMed][CrossRef]
176. Buffie CG, Pamer EG. 2013. Microbiota-mediated colonization resistance against intestinal pathogens. Nat Rev Immunol 13:790–801. [PubMed][CrossRef]
177. Conrad D, Haynes M, Salamon P, Rainey PB, Youle M, Rohwer F. 2013. Cystic fibrosis therapy: a community ecology perspective. Am J Respir Cell Mol Biol 48:150–156. [PubMed][CrossRef]
178. Ren D, Madsen JS, de la Cruz-Perera CI, Bergmark L, Sorensen SJ, Burmolle M. 2013. High-throughput screening of multispecies biofilm formation and quantitative PCR-based assessment of individual species proportions, useful for exploring interspecific bacterial interactions. Microb Ecol [Epub ahead of print.] doi:10.1007/s00248-013-0315-z. [CrossRef]
179. Shank EA. 2013. Using coculture to detect chemically mediated interspecies interactions. J Vis Exp 80:e50863. doi:10.3791/50863. [PubMed][CrossRef]

Article metrics loading...



Bacterial biofilms are dense and often mixed-species surface-attached communities in which bacteria coexist and compete for limited space and nutrients. Here we present the different antagonistic interactions described in biofilm environments and their underlying molecular mechanisms, along with ecological and evolutionary insights as to how competitive interactions arise and are maintained within biofilms.

Highlighted Text: Show | Hide
Loading full text...

Full text loading...



Image of FIGURE 1

Click to view


Ecological and evolutionary parameters operating within biofilm communities. Group effects: increase bacterial fitness compared to solitary life. Cooperation: biofilm bacteria can actively cooperate to increase their individual fitness. Kin competition: under high stress and low nutrient conditions, kin can become a source of competition and enhance spatial segregation. Genetic expression profiles: planktonic bacteria express different genes than those expressed by biofilm. Genotypic and phenotypic diversification: Due to competition, different variants can spontaneously appear within biofilm communities.

Source: microbiolspec June 2015 vol. 3 no. 3 doi:10.1128/microbiolspec.MB-0009-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 2

Click to view


Mechanisms of competition within biofilms. Microbial interference can affect biofilm formation or dispersion through different mechanisms and strategies at different biofilm stages. These strategies include the secretion of growth or adhesion inhibitory molecules, jamming quorum sensing, altering biofilm regulation, and enhancing biofilm dispersal. (See text.)

Source: microbiolspec June 2015 vol. 3 no. 3 doi:10.1128/microbiolspec.MB-0009-2014
Permissions and Reprints Request Permissions
Download as Powerpoint


Generic image for table

Click to view


Interference competition. Summary of the interference strategies described in this chapter

Source: microbiolspec June 2015 vol. 3 no. 3 doi:10.1128/microbiolspec.MB-0009-2014

Supplemental Material

No supplementary material available for this content.

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