Experimental evolution in biofilm populations

FEMS Microbiology Reviews

Volumn 40, Issue 3, 2016, Pages 373-397

  Steenackers, Hans P ^a   Parijs, Ilse ^a   Foster, Kevin R ^b   Vanderleyden, Jozef ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Adaptive diversification; Biofilm; Cooperation; Experimental evoultion

Indexed keywords

BACTERIAL STRAIN; BACTERIAL SURVIVAL; BIOFILM; BURKHOLDERIA CENOCEPACIA; COMPARATIVE STUDY; DIAGNOSTIC PROCEDURE; ENVIRONMENTAL FACTOR; GENETIC VARIABILITY; GENOTYPE; HORIZONTAL GENE TRANSFER; HUMAN; IN VITRO STUDY; METAGENOMICS; MICROBIAL COMMUNITY; MOLECULAR EVOLUTION; MUTATION RATE; NONHUMAN; PHENOTYPE; PLEIOTROPY; POPULATION STRUCTURE; PSEUDOMONAS FLUORESCENS; REVIEW; BACTERIAL PHENOMENA AND FUNCTIONS; BIODIVERSITY; BIOLOGICAL MODEL; EVOLUTION; MICROBIAL VIABILITY;

BACTERIAL PHYSIOLOGICAL PHENOMENA; BIODIVERSITY; BIOFILMS; BIOLOGICAL EVOLUTION; MICROBIAL VIABILITY; MODELS, BIOLOGICAL; PHENOTYPE;

EID: 84975709166     PISSN: 01686445     EISSN: 15746976     Source Type: Journal    
DOI: 10.1093/femsre/fuw002     Document Type: Review

References (188)

1. Ackermann M, Schauerte A, Stearns SC et al. Experimental evolution of aging in a bacterium. BMC Evol Biol 2007;7:126.
2. Akers KS, Cardile AP,Wenke JC et al. Biofilm formation by clinical isolates and its relevance to clinical infections. Adv Exp Med Biol 2015;830:1-28.
3. Allegrucci M, Sauer K. Characterization of colony morphology variants isolated from Streptococcus pneumoniae biofilms. J Bacteriol 2007;189:2030-8.
4. Allegrucci M, Sauer K. Formation of Streptococcus pneumoniae non-phase-variable colony variants is due to increased mutation frequency present under biofilm growth conditions. J Bacteriol 2008;190:6330-9.
5. Andersson DI. The biological cost of mutational antibiotic resistance: any practical conclusions? Curr Opin Microbiol 2006;9:461-5.
6. Antonova ES, Hammer BK. Quorum-sensing autoinducer molecules produced by members of a multispecies biofilm promote horizontal gene transfer to Vibrio cholerae. FEMS Microbiol Lett 2011;322:68-76.
7. Bantinaki E, Kassen R, Knight CG et al. Adaptive divergence in experimental populations of Pseudomonas fluorescens. III. Mutational origins of wrinkly spreader diversity. Genetics 2007;176:441-53.
8. Baquero F, Coque TM. Widening the spaces of selection:evolution along sublethal antimicrobial gradients. mBio 2014;5:e02270.
9. Baquero F, Negri MC, Morosini MI et al. Antibiotic-selective environments. Clin Infect Dis 1998;27(Suppl 1):S5-11.
10. Barrett RD, MacLean RC, Bell G. Experimental evolution of Pseudomonas fluorescens in simple and complex environments.Am Nat 2005;166:470-80.
11. Barrick JE, Lenski RE. Genome dynamics during experimental evolution. Nat Rev Genet 2013;14:827-39.
12. Behe MJ. Experimental evolution, loss-of-function mutations, and 'the first rule of adaptive evolution'. Q Rev Biol 2010;85:419-45.
13. Bell T, Newman JA, Silverman BW et al. The contribution of species richness and composition to bacterial services. Nature 2005;436:1157-60.
14. Bjarnsholt T, Alhede M, Eickhardt-Sorensen SR et al. The in vivo biofilm. Trends Microbiol 2013;21:466-74.
15. Bjedov I, Tenaillon O, Souza V et al. Stress-induced mutagenesis in bacteria. Science 2003;300:1404-9.
16. Boles BR, Singh PK. Endogenous oxidative stress produces diversity and adaptability in biofilm communities. P Natl Acad Sci USA 2008;105:12503-8.
17. Boles BR, Thoendel M, Singh PK. Self-generated diversity produces insurance effects in biofilm communities. P Natl Acad Sci USA 2004;101:16630-5.
18. Boyle KE, Heilmann S, van Ditmarsch D et al. Exploiting social evolution in biofilms. Curr Opin Microbiol 2013;16:207-12.
19. Brockhurst MA, Colegrave N, Hodgson DJ et al. Niche occupation limits adaptive radiation in experimental microcosms. PLoS One 2007;2:1-4.
20. Brockhurst MA, Colegrave N, Rozen DE. Next-generation sequencing as a tool to study microbial evolution. Mol Ecol 2011;20:972-80.
21. Brockhurst MA, Hochberg ME, Bell T et al. Character displacement promotes cooperation in bacterial biofilms. Curr Biol 2006;16:2030-4.
22. Buckling A, Kassen R, Bell G et al. Disturbance and diversity in experimental microcosms. Nature 2000;408:961-4.
23. Burmolle M, Ren D, Bjarnsholt T et al. Interactions in multispecies biofilms: do they actually matter? Trends Microbiol 2014;22:84-91.
24. Chase JM, Leibold MA. Ecological Niches: Linking Classical and Contemporary Approaches. Chicago: Univ Chicago Press, 2003.
25. Ciofu O, Tolker-Nielsen T, Jensen PO et al. Antimicrobial resistance, respiratory tract infections and role of biofilms in lung infections in cystic fibrosis patients. Adv Drug Deliv Rev 2015;85:7-23.
26. Coenye T, Nelis HJ. In vitro and in vivo model systems to study microbial biofilm formation. J Microbiol Methods 2010;83:89-105.
27. Conibear TCR, Collins SL, Webb JS. Role of mutation in Pseudomonas aeruginosa biofilm development. PLoS One 2009;4:e6289.
28. Cooper TF, Beaumont HJE, Rainey PB. Biofilm diversity as a test of the insurance hypothesis. Microbiology 2005;151:2815-6.
29. Cooper TF, Lenski RE. Experimental evolution with E. coli in diverse resource environments. I. Fluctuating environments promote divergence of replicate populations. BMC Evol Biol 2010;10:11.
30. Cooper VS, Staples RK, Traverse CC et al. Parallel evolution of small colony variants in Burkholderia cenocepacia biofilms. Genomics 2014;104:447-52.
31. Costerton JW, Lewandowski Z, Caldwell DE et al. Microbial biofilms. Annu Rev Microbiol 1995;49:711-45.
32. Cramer N, Klockgether J, Wrasman K et al. Microevolution of the major common Pseudomonas aeruginosa clones C and PA14 in cystic fibrosis lungs. Environ Microbiol 2011;13:1690-704.
33. Davies D. Understanding biofilm resistance to antibacterial agents. Nat Rev Drug Discov 2003;2:114-22.
34. Davis MR, Muszynski A, Lollett IV et al. Identification of the mutation responsible for the temperature-sensitive lipopolysaccharide O-antigen defect in the Pseudomonas aeruginosa cystic fibrosis isolate 2192. J Bacteriol 2013;195:1504-14.
35. Day RL, Laland KN, Odling-Smee FJ. Rethinking adaptation: the niche-construction perspective. Perspect Biol Med 2003;46:80-95.
36. Day T, Young KA. Competitive and facilitative evolutionary diversification. Bioscience 2004;54:101-9.
37. Denamur E, Matic I. Evolution of mutation rates in bacteria. Mol Microbiol 2006;60:820-7.
38. Dettman JR, Rodrigue N, Melnyk AH et al. Evolutionary insight from whole-genome sequencing of experimentally evolved microbes. Mol Ecol 2012;21:2058-77.
39. Deziel E, Comeau Y, Villemur R. Initiation of biofilm formation by Pseudomonas aeruginosa 57RP correlates with emergence of hyperpiliated and highly adherent phenotypic variants deficient in swimming, swarming, and twitching motilities. J Bacteriol 2001;183:1195-204.
40. Drake JW, Charlesworth B, Charlesworth D et al. Rates of Spontaneous Mutation. Genetics 1998;146:1667-86.
41. Drescher K, Nadell CD, Stone HA et al. Solutions to the public goods dilemma in bacterial biofilms. Curr Biol 2014;24:50-5.
42. Driffield K, Miller K, Bostock JM et al. Increased mutability of Pseudomonas aeruginosa in biofilms. J Antimicrob Chemoth 2008;61:1053-6.
43. Dunham MJ, Badrane H, Ferea T et al. Characteristic genome rearrangements in experimental evolution of Saccharomyces cerevisiae. P Natl Acad Sci USA 2002;99:16144-9.
44. Elena SF, Lenski RE. Evolution experiments with microorganisms:the dynamics and genetic bases of adaptation. Nat Rev Genet 2003;4:457-69.
45. Ellis CN, Traverse CC, Mayo-Smith L et al. Character displacement and the evolution of niche complementarity in amodel biofilm community. Evolution 2015;69:283-93.
46. Ferguson GC, Bertels F, Rainey PB. Adaptive divergence in experimental populations of Pseudomonas fluorescens. V. insight into the niche specialist fuzzy spreader compels revision of the model Pseudomonas radiation. Genetics 2013;195:1319-35.
47. Folkesson A, Jelsbak L, Yang L et al. Adaptation of Pseudomonas aeruginosa to the cystic fibrosis airway: an evolutionary perspective. Nat Rev Microbiol 2012;10:841-51.
48. Fukami T, Beaumont HJ, Zhang XX et al. Immigration history controls diversification in experimental adaptive radiation. Nature 2007;446:436-9.
49. Galhardo RS, Hastings PJ, Rosenberg SM. Mutation as a stress response and the regulation of evolvability. Crit Rev Biochem Mol 2007;42:399-435.
50. Gerstein AC, Lo DS, Otto SP. Parallel genetic changes and nonparallel gene-environment interactions characterize the evolution of drug resistance in yeast. Genetics 2012;192:241-52.
51. Golding I, Cohen I, Ben-Jacob E. Studies of sector formation in expanding bacterial colonies. EPL-Europhys Lett 1999;48:587-93.
52. Goller CC, Romeo T. Environmental influences on biofilm development. Curr Top Microbiol 2008;322:37-66.
53. Gomez P, Buckling A. Real-time microbial adaptive diversification in soil. Ecol Lett 2013;16:650-5.
54. Goymer P, Kahn SG, Malone JG et al. Adaptive divergence in experimental populations of Pseudomonas fluorescens. II. Role of the GGDEF regulator WspR in evolution and development of the wrinkly spreader phenotype. Genetics 2006;173:515-26.
55. Greaves M, Maley CC. Clonal evolution in cancer. Nature 2012;481:306-13.
56. Guggenheim B, Giertsen E, Schupbach P et al. Validation of an in vitro biofilm model of supragingival plaque. J Dent Res 2001;80:363-70.
57. Habets MG, Rozen DE, Hoekstra RF et al. The effect of population structure on the adaptive radiation of microbial populations evolving in spatially structured environments. Ecol Lett 2006;9:1041-8.
58. Hall AR, Miller AD, Leggett HC et al. Diversity-disturbance relationships: frequency and intensity interact. Biol Lett 2012;8:768-71.
59. Hallatschek O, Hersen P, Ramanathan S et al. Genetic drift at expanding frontiers promotes gene segregation. P Natl Acad Sci USA 2007;104:19926-30.
60. Hallatschek O, Nelson DR. Gene surfing in expanding populations. Theor Popul Biol 2008;73:158-70.
61. Hall-Stoodley L, Costerton JW, Stoodley P. Bacterial biofilms:from the natural environment to infectious diseases. Nat Rev Microbiol 2004;2:95-108.
62. Hall-Stoodley L, Stoodley P. Evolving concepts in biofilm infections. Cell Microbiol 2009;11:1034-43.
63. Hamilton WD. The genetical evolution of social behaviour. I. J Theor Biol 1964;7:1-16.
64. Hansen SK, Rainey PB, Haagensen JA et al. Evolution of species interactions in a biofilm community. Nature 2007;445:533-6.
65. Hardin G. The competitive exclusion principle. Science 1960;131:1292-7.
66. Harrison F, Paul J, Massey RC et al. Interspecific competition and siderophore-mediated cooperation in Pseudomonas aeruginosa. Isme J 2008;2:49-55.
67. Haussler S, Lehmann C, Breselge C et al. Fatal outcome of lung transplantation in cystic fibrosis patients due to smallcolony variants of the Burkholderia cepacia complex. Eur J Clin Microbiol 2003;22:249-53.
68. Hector A, Schmid B, Beierkuhnlein C et al. Plant diversity and productivity experiments in european grasslands. Science 1999;286:1123-7.
69. Hegreness M, Shoresh N, Hartl D et al. An equivalence principle for the incorporation of favorable mutations in asexual populations. Science 2006;311:1615-7.
70. Hengge R. Principles of c-di-GMP signalling in bacteria. Nat Rev Microbiol 2009;7:263-73.
71. Hermsen R, Deris JB, Hwa T. On the rapidity of antibiotic resistance evolution facilitated by a concentration gradient. P Natl Acad Sci USA 2012;109:10775-80.
72. Herron MD, Doebeli M. Parallel evolutionary dynamics of adaptive diversification in Escherichia coli. PLoS Biol 2013;11:e1001490.
73. Hobley L, Harkins C, MacPhee CE et al. Giving structure to the biofilm matrix: an overview of individual strategies and emerging common themes. FEMS Microbiol Rev 2015;39:649-69.
74. Hoboth C, Hoffmann R, Eichner A et al. Dynamics of adaptive microevolution of hypermutable Pseudomonas aeruginosa during chronic pulmonary infection in patients with cystic fibrosis. J Infect Dis 2009;200:118-30.
75. Hogardt M, Heesemann J. Adaptation of Pseudomonas aeruginosa during persistence in the cystic fibrosis lung. Int J Med Microbiol 2010;300:557-62.
76. Huse HK, Kwon T, Zlosnik JE et al. Parallel evolution in Pseudomonas aeruginosa over 39 000 generations in vivo. mBio 2010;1:e00199-10.
77. Karlsson-Kanth A, Tegmark-Wisell K, Arvidson S et al. Natural human isolates of Staphylococcus aureus selected for high production of proteases and alpha-hemolysin are sigmaB deficient. Int J Med Microbiol 2006;296:229-36.
78. Kassen R. The evolution of specialists, generalists and the maintenance of diversity. J Evol Biol 2002;15:173-90.
79. Kassen R. Toward a general theory of adaptive radiation: insights from microbial experimental evolution. Ann NY Acad Sci 2009;1168:3-22.
80. Kassen R. Experimental Evolution and the Nature of Biodiversity. Greenwood Village, CO: Roberts and Company, Publishers, 2014.
81. Kassen R, Llewellyn M, Rainey PB. Ecological constraints on diversification in a model adaptive radiation. Nature 2004;431:984-8.
82. Kassen R, Rainey PB. The ecology and genetics of microbial diversity. Annu Rev Microbiol 2004;58:207-31.
83. Kawecki TJ, Lenski RE, Ebert D et al. Experimental evolution. Trends Ecol Evol 2012;27:547-60.
84. Kim W, Racimo F, Schluter J et al. Importance of positioning for microbial evolution. P Natl Acad Sci USA 2014;111:E1639-47.
85. Kirisits MJ, Prost L, Starkey M et al. Characterization of colony morphology variants isolated from Pseudomonas aeruginosa biofilms. Appl Environ Microb 2005;71:4809-21.
86. Klopfstein S, Currat M, Excoffier L. The fate of mutations surfing on the wave of a range expansion. Mol Biol Evol 2006;23:482-90.
87. Knight CG, Zitzmann N, Prabhakar S et al. Unraveling adaptive evolution: how a single point mutation affects the protein coregulation network. Nat Genet 2006;38:1015-22.
88. Koch G, Yepes A, Forstner KU et al. Evolution of resistance to a last-resort antibiotic in Staphylococcus aureus via bacterial competition. Cell 2014;158:1060-71.
89. Koh KS, Lam KW, Alhede M et al. Phenotypic diversification and adaptation of Serratia marcescens MG1 biofilm-derived morphotypes. J Bacteriol 2007;189:119-30.
90. Kohler T, Buckling A, van Delden C. Cooperation and virulence of clinical Pseudomonas aeruginosa populations. P Natl Acad Sci USA 2009;106:6339-44.
91. Korona R, Nakatsu CH, Forney LJ et al. Evidence for multiple adaptive peaks from populations of bacteria evolving in a structured habitat. P Natl Acad Sci USA 1994;91:9037-41.
92. Koza A, Moshynets O, Otten W et al. Environmental modification and niche construction: developing O2 gradients drive the evolution of the Wrinkly Spreader. Isme J 2011;5:665-73.
93. Kraigsley AM, Finkel SE. Adaptive evolution in single species bacterial biofilms. FEMS Microbiol Lett 2009;293:135-40.
94. Kreft JU, Picioreanu C, Wimpenny JW et al. Individual-based modelling of biofilms. Microbiology 2001;147:2897-912.
95. Lang GI, Rice DP, Hickman MJ et al. Pervasive genetic hitchhiking and clonal interference in forty evolving yeast populations. Nature 2013;500:571-4.
96. Lenski RE, Rose MR, Simpson SC et al. Long-term experimental evolution in Escherichia coli. 1. Adaptation and divergence during 2000 generations. Am Nat 1991;138:1315-41.
97. Lieberman TD, Michel JB, Aingaran M et al. Parallel bacterial evolution within multiple patients identifies candidate pathogenicity genes. Nat Genet 2011;43:1275-80.
98. Lind PA, Andersson DI. Whole-genomemutational biases in bacteria. PNatl Acad Sci USA 2008;105:17878-83.
99. Lind PA, Farr AD, Rainey PB. Experimental evolution reveals hidden diversity in evolutionary pathways. eLife 2015;4:e07074.
100. Lipsitch M. The rise and fall of antimicrobial resistance. Trends Microbiol 2001;9:438-44.
101. Loewe L, Textor V, Scherer S. High deleterious genomic mutation rate in stationary phase of Escherichia coli. Science 2003;302:1558-60.
102. Lujan AM, Macia MD, Yang L et al. Evolution and adaptation in Pseudomonas aeruginosa biofilms driven by mismatch repair system-deficient mutators. PLoS One 2011;6:e27842.
103. Macarthur R, Levins R. Competition, habitat selection, and character displacement in a patchy environment. P Natl Acad Sci USA 1964;51:1207-10.
104. McBain AJ. Chapter 4 In Vitro biofilm models. Adv Appl Microbiol 2009;69:99-132.
105. McCann KS. The diversity-stability debate. Nature 2000;405:228-33.
106. McDonald MJ, Gehrig SM, Meintjes PL et al. Adaptive divergence in experimental populations of Pseudomonas fluorescens. IV. Genetic constraints guide evolutionary trajectories in a parallel adaptive radiation. Genetics 2009;183:1041-53.
107. McElroy KE, Hui JG,Woo JK et al. Strain-specific parallel evolution drives short-term diversification during Pseudomonas aeruginosa biofilm formation. P Natl Acad Sci USA 2014;111:E1419-27.
108. MacLean RC, Bell G, Rainey PB. The evolution of a pleiotropic fitness tradeoff in Pseudomonas fluorescens. P Natl Acad Sci USA 2004;101:8072-7.
109. Maddamsetti R, Lenski RE, Barrick JE. Adaptation, clonal interference, and frequency dependent interactions in a long term evolution experiment with Escherichia coli. Genetics 2015;200:619-31.
110. Madsen JS, Burmolle M, Hansen LH et al. The interconnection between biofilm formation and horizontal gene transfer. FEMS Immunol Med Mic 2012;65:183-95.
111. Martens EA, Hallatschek O. Interfering waves of adaptation promote spatial mixing. Genetics 2011;189:1045-60.
112. Martens EA, Kostadinov R, Maley CC et al. Spatial structure increases the waiting time for cancer. New J Phys 2011;13:115014.
113. Martinez JL, Baquero F. Mutation frequencies and antibiotic resistance. Antimicrob Agents Ch 2000;44:1771-7.
114. Mena A, Smith EE, Burns JL et al. Genetic adaptation of Pseudomonas aeruginosa to the airways of cystic fibrosis patients is catalyzed by hypermutation. J Bacteriol 2008;190:7910-7.
115. Metzgar D,Wills C. Evidence for the adaptive evolution ofmutation rates. Cell 2000;101:581-4
116. Meyer JR, Dobias DT,Weitz JS et al. Repeatability and contingency in the evolution of a key innovation in phage lambda. Science 2012;335:428-32.
117. Meyer JR, Schoustra SE, Lachapelle J et al. Overshooting dynamics in a model adaptive radiation. P Roy Soc B-Biol Sci 2011;278:392-8.
118. Miralles R, Gerrish PJ, Moya A et al. Clonal interference and the evolution of RNA viruses. Science 1999;285:1745-7.
119. Mitri S, Clarke E, Foster KR. Resource limitation drives spatial organization in microbial groups. ISME J 2015;1-12.
120. Mitri S, Foster KR. The genotypic view of social interactions in microbial communities. Annu Rev Genet 2013;47:247-73.
121. Mitri S, Xavier JB, Foster KR. Social evolution in multispecies biofilms. P Natl Acad Sci USA 2011;108(Suppl 2):10839-46.
122. Nadell CD, Bassler BL. A fitness trade-off between local competition and dispersal in Vibrio cholerae biofilms. P Natl Acad Sci USA 2011;108:14181-5.
123. Nadell CD, Foster KR, Xavier JB. Emergence of spatial structure in cell groups and the evolution of cooperation. PLoS Comput Biol 2010;6:e1000716.
124. Nadell CD, Xavier JB, Foster KR. The sociobiology of biofilms. FEMS Microbiol Rev 2009;33:206-24.
125. Nadell CD, Xavier JB, Levin SA et al. The evolution of quorum sensing in bacterial biofilms. PLoS Biol 2008;6:e14.
126. Nahum JR, Godfrey-Smith P, Harding BN et al. A tortoise-hare pattern seen in adapting structured and unstructured populations suggests a rugged fitness landscape in bacteria. P Natl Acad Sci USA 2015;112:201410631.
127. Nilsson AI, Koskiniemi S, Eriksson S et al. Bacterial genome size reduction by experimental evolution. P Natl Acad Sci USA 2005;102:12112-6.
128. Odum EP. Ecology, 2nd edn. New York: Holt, Rinehart, and Winston, 1975.
129. Oliveira NM, Niehus R, Foster KR. Evolutionary limits to cooperation in microbial communities. P Natl Acad Sci USA 2014;111:17941-6.
130. O'Rourke D, FitzGerald CE, Traverse CC et al. There and back again: consequences of biofilm specialization under selection for dispersal. Front Genet 2015;6:18.
131. Park SC, Krug J. Clonal interference in large populations. P Natl Acad Sci USA 2007;104:18135-40.
132. Penterman J, Nguyen D, Anderson E et al. Rapid evolution of culture-impaired bacteria during adaptation to biofilm growth. Cell Rep 2014;6:293-300.
133. Perfeito L, PereiraMI, Campos PR et al. The effect of spatial structure on adaptation in Escherichia coli. Biol Lett 2008;4:57-59.
134. Perron GG, Gonzalez A, Buckling A. Source-sink dynamics shape the evolution of antibiotic resistance and its pleiotropic fitness cost. P Roy Soc B-Biol Sci 2007;274:2351-6.
135. Picioreanu C, Kreft JU, Van Loosdrecht MC. Particle-based multidimensional multispecies biofilm model. Appl Environ Microb 2004;70:3024-40.
136. Poltak SR, Cooper VS. Ecological succession in long-term experimentally evolved biofilms produces synergistic communities. ISME J 2011;5:369-78.
137. Ponciano JM, La HJ, Joyce P et al. Evolution of diversity in spatially structured Escherichia coli populations. Appl Environ Microb 2009;75:6047-54.
138. Popat R, Crusz SA, Messina M et al. Quorum-sensing and cheating in bacterial biofilms. P Roy Soc B-Biol Sci 2012;279:4765-71.
139. Pulido-Tamayo S, Sanchez-Rodriguez A, Swings T et al. Frequency-based haplotype reconstruction from deep sequencing data of bacterial populations. Nucleic Acids Res 2015;43:e105.
140. Rainey PB, Rainey K. Evolution of cooperation and conflict in experimental bacterial populations. Nature 2003;425:69-72.
141. Rainey PB, Travisano M. Adaptive radiation in a heterogeneous environment. Nature 1998;31:69-72.
142. Rani SA, Pitts B, Stewart PS. Rapid diffusion of fluorescent tracers into Staphylococcus epidermidis biofilms visualized by time lapse microscopy. Antimicrob Agents Ch 2005;49:728-32.
143. Roberfroid S, Vanderleyden J, Steenackers HP. Gene expression variability in clonal populations: causes and consequences. Crit Rev Microbiol 2016;5:1-16.
144. Romling U, Galperin MY, Gomelsky M. Cyclic di-GMP: the first 25 years of a universal bacterial second messenger. Microbiol Mol Biol Rev 2013;77:1-52.
145. Rosenberg SM. Evolving responsively adaptivemutation. Nat Rev Genet 2001;2:504-15.
146. Rosenberg SM, Queitsch C. Combating evolution to fight disease. Science 2014;343:1088-9.
147. Rozen DE, de Visser JA, Gerrish PJ. Fitness effects of fixed beneficial mutations in microbial populations. Curr Biol 2002;12:1040-5.
148. Rozen DE, Habets MGJL, Handel A et al. Heterogeneous adaptive trajectories of small populations on complex fitness landscapes. PLoS One 2008;3:e1715.
149. Rumbaugh KP, Carty NL. In vivo models of biofilm infection. In: Bjarnsholt T (ed.). Biofilm Infections. New York: Springer-Verlag, 2011, 267-29.
150. Ryder VJ, Chopra I, O'Neill AJ. Increased mutability of Staphylococci in biofilms as a consequence of oxidative stress. PLoS One 2012;7:e47695.
151. Saint-Ruf C, Garfa-Traore M, Collin V et al. Massive diversification in aging colonies of Escherichia coli. J Bacteriol 2014;196:3059-73.
152. Savage VJ, Chopra I, O'Neill AJ. Population diversification in Staphylococcus aureus biofilms may promote dissemination and persistence. PLoS One 2013;8:e62513.
153. Schluter D. The Ecology of Adaptive Radiation. New York: Oxford University Press, 2000.
154. Schluter J, Nadell CD, Bassler BL et al. Adhesion as a weapon in microbial competition. ISME J 2015;9:139-49.
155. Simpson G. The Major Features of Evolution. New York: Columbia University Press, 1953.
156. Smith EE, Buckley DG, Wu Z et al. Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. P Natl Acad Sci USA 2006;103:8487-92.
157. Sniegowski PD, Gerrish PJ. Beneficial mutations and the dynamics of adaptation in asexual populations. Philos T Roy Soc B 2010;365:1255-63.
158. Spencer P, Greenman J, McKenzie C et al. In vitro biofilm model for studying tongue flora and malodour. J Appl Microbiol 2007;103:985-92.
159. Spiers AJ. A mechanistic explanation linking adaptive mutation, niche change, and fitness advantage for the wrinkly spreader. Int J Evol Biology 2014;2014:675432.
160. Spiers AJ, Bohannon J, Gehrig SM et al. Biofilm formation at the air-liquid interface by the Pseudomonas fluorescens SBW25 wrinkly spreader requires an acetylated form of cellulose. Mol Microbiol 2003;50:15-27.
161. Spiers AJ, Kahn SG, Bohannon J et al. Adaptive divergence in experimental populations of Pseudomonas fluorescens. I. Genetic and phenotypic bases of wrinkly spreader fitness. Genetics 2002;161:33-46.
162. Starkey M, Hickman JH, Ma L et al. Pseudomonas aeruginosa rugose small-colony variants have adaptations that likely promote persistence in the cystic fibrosis lung. J Bacteriol 2009;191:3492-503.
163. Steenackers H, Hermans K, Vanderleyden J et al. Salmonella biofilms: an overview on occurrence, structure, regulation and eradication. Food Res Int 2012;45:502-31.
164. Stern DL. The genetic causes of convergent evolution. Nat Rev Genet 2013;14:751-64.
165. Stewart PS, Franklin MJ. Physiological heterogeneity in biofilms. Nat Rev Microbiol 2008;6:199-210.
166. Taddei F, Matic I, Radman M. cAMP-dependent SOS induction andmutagenesis in resting bacterial populations. P Natl Acad Sci USA 1995;92:11736-40.
167. Tilman D, Reich PB, Knops J et al. Diversity and productivity in a long-term grassland experiment. Science 2001;294:843-5.
168. Traber KE, Lee E, Benson S et al. agr function in clinical Staphylococcus aureus isolates. Microbiology 2008;154:2265-74.
169. Traverse CC, Mayo-Smith LM, Poltak SR et al. Tangled bank of experimentally evolved Burkholderia biofilms reflects selection during chronic infections. P Natl Acad Sci USA 2012;110:E250-9.
170. Travis E, Travis J. Mutators in space: the dynamics of high-mutability clones in a two-patch model. Genetics 2004;167:513-22.
171. Tyerman JG, Ponciano JM, Joyce P et al. The evolution of antibiotic susceptibility and resistance during the formation of Escherichia coli biofilms in the absence of antibiotics. BMC Evol Biol 2013;13:22.
172. Udall YC, Deeni Y, Hapca SM et al. The evolution of biofilmforming Wrinkly Spreaders in static microcosms and dripfed columns selects for subtle differences in wrinkleality and fitness. FEMS Microbiol Ecol 2015;91, DOI: 10.1093/femsec/ fiv057.
173. Van Dyken JD, Muller MJ, Mack KM et al. Spatial population expansion promotes the evolution of cooperation in an experimental Prisoner's Dilemma. Curr Biol 2013;23:919-23.
174. Waite RD, Struthers JK, Dowson CG. Spontaneous sequence duplication within an open reading frame of the pneumococcal type 3 capsule locus causes high-frequency phase variation. Mol Microbiol 2001;42:1223-32.
175. Warren AE, Boulianne-Larsen CM, Chandler CB et al. Genotypic and phenotypic variation in Pseudomonas aeruginosa reveals signatures of secondary infection andmutator activity in certain cystic fibrosis patients with chronic lung infections. Infect Immun 2011;79:4802-18.
176. Weber SD, Ludwig W, Schleifer KH et al. Microbial composition and structure of aerobic granular sewage biofilms. Appl Environ Microb 2007;73:6233-40.
177. West SA, Griffin AS, Gardner A et al. Social evolution theory for microorganisms. Nat Rev Microbiol 2006;4:597-607.
178. Wong A, Rodrigue N, Kassen R. Genomics of adaptation during experimental evolution of the opportunistic pathogen Pseudomonas aeruginosa. PLos Genet 2012;8:e1002928.
179. Wrande M, Roth JR, Hughes D. Accumulation of mutants in "aging" bacterial colonies is due to growth under selection, not stress-induced mutagenesis. P Natl Acad Sci USA 2008;105:11863-8.
180. Wright S. Evolution in Mendelian populations. Genetics 1931;16:97-159.
181. Xavier JB, Foster KR. Cooperation and conflict in microbial biofilms. P Natl Acad Sci USA 2007;104:876-81.
182. Xavier JB, Martinez-Garcia E, Foster KR. Social evolution of spatial patterns in bacterial biofilms: when conflict drives disorder. Am Nat 2009;174:1-12.
183. Xavier JB, Picioreanu C, van Loosdrecht MC. A framework for multidimensional modelling of activity and structure of multispecies biofilms. Environ Microbiol 2005;7:1085-103.
184. Yachi S, Loreau M. Biodiversity and ecosystem productivity in a fluctuating environment: the insurance hypothesis. P Natl Acad Sci USA 1999;96:1463-8.
185. Yang L, Jelsbak L, Marvig RL et al. Evolutionary dynamics of bacteria in a human host environment. P Natl Acad Sci USA 2011;108:7481-6.
186. Yarwood JM, Paquette KM, Tikh IB et al. Generation of virulence factor variants in Staphylococcus aureus biofilms. J Bacteriol 2007;189:7961-7.
187. Yoder JB, Clancey E, Des Roches S et al. Ecological opportunity and the origin of adaptive radiations. J Evol Biol 2010;23:1581-96.
188. Zhang Q, Lambert G, Liao D et al. Acceleration of emergence of bacterial antibiotic resistance in connected microenvironments. Science 2011;333:1764-7.