Chapter 16 : Mechanisms of Competition in Biofilm Communities

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in

Mechanisms of Competition in Biofilm Communities, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555817466/9781555817459_Chap16-1.gif /docserver/preview/fulltext/10.1128/9781555817466/9781555817459_Chap16-2.gif


The rapid development of new sequencing technologies and the use of metagenomics revealed the great diversity of microbial life and enabled the emergence of a new perspective on population dynamics. Moreover, it has highlighted the central role of social interactions in ecological and evolutionary processes. Microbes living in multispecies communities are prevalent in nature and have been shown to extensively cooperate and compete. Both intra- and interspecies interactions are instrumental in major geochemical cycles and are important in human health and homeostasis (e.g., the human microbiome has been associated with several diseases) and in industrial and clinical settings ( ). Few studies have addressed the role of individual species within mixed communities ( ), and they generally focus on cooperative interactions and increased benefits of community life ( ). However, recent work pointed out that most interactions are competitive rather than cooperative, suggesting that adaptation is more likely achieved by competitive success ( ). A further degree of complexity in understanding multispecies interactions and dynamics is brought by increasing evidence suggesting that phenomena occurring in complex communities cannot be predicted by the observation of single-species communities ( ).

Citation: Rendueles O, Ghigo J. 2015. Mechanisms of Competition in Biofilm Communities, p 319-342. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0009-2014
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


Image of Figure 1
Figure 1

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.

Citation: Rendueles O, Ghigo J. 2015. Mechanisms of Competition in Biofilm Communities, p 319-342. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0009-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 2
Figure 2

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.)

Citation: Rendueles O, Ghigo J. 2015. Mechanisms of Competition in Biofilm Communities, p 319-342. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0009-2014
Permissions and Reprints Request Permissions
Download as Powerpoint


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]


Generic image for table

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

Citation: Rendueles O, Ghigo J. 2015. Mechanisms of Competition in Biofilm Communities, p 319-342. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0009-2014

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