The onion model, a simple neutral model for the evolution of diversity in bacterial biofilms

Journal of Evolutionary Biology

Volumn 24, Issue 11, 2011, Pages 2496-2504

  Eastman, J M ^a   Harmon, L J ^a   La, H J ^a   Joyce, P ^a   Forney, L J ^a  

^a UNIVERSITY OF IDAHO   (United States)

Author keywords

Antibiotic resistance; Escherichia coli; Insurance effect; Moran model; Neutral evolution

Indexed keywords

ANTIBIOTIC RESISTANCE; BACTERIUM; BIOFILM; EVOLUTIONARY BIOLOGY; GENETIC DRIFT; MUTATION;

ANTIBIOTIC RESISTANCE; ARTICLE; BIOFILM; BIOLOGICAL MODEL; COMPUTER SIMULATION; ESCHERICHIA COLI; GENETIC DRIFT; GENETICS; PHENOTYPE;

BIOFILMS; COMPUTER SIMULATION; DRUG RESISTANCE, MICROBIAL; ESCHERICHIA COLI; GENETIC DRIFT; MODELS, BIOLOGICAL; PHENOTYPE;

ALLIUM CEPA; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 80053935821     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2011.02377.x     Document Type: Article

References (49)

1. Balaban, N.O., Merrin, J., Chait, R., Kowalik, L. & Leibler, S. 2004. Bacterial persistence as a phenotypic switch. Science 305: 1622-1625.
2. Bantinaki, E., Kassen, R., Knight, C., Robinson, Z., Spiers, A.J. & Rainey, P.B. 2007. Adaptive divergence in experimental populations of Pseudomonas fluorescens III. Mutational origins of wrinkly spreader diversity. Genetics 176: 441-453.
3. Battin, T.J., Sloan, W.T., Kjelleberg, S., Daims, H., Head, I.M., Curtis, T.P. et al. 2007. Microbial landscapes: new paths to biofilm research. Nat. Rev. Microbiol. 5: 76-81.
4. Bjedov, I., Tenaillon, O., Gerard, B., Souza, V., Denamur, E., Radman, M. et al. 2003. Stress-induced mutagenesis in bacteria. Science 300: 1404-1409.
5. Boles, B.R. & Singh, P.K. 2008. Endogenous oxidative stress produces diversity and adaptability in biofilm communities. Proc. Natl Acad. Sci. USA 105: 12503-12508.
6. Boles, B.R., Thoendel, M. & Singh, P.K. 2004. Self-generated diversity produces ''insurance effects'' in biofilm communities. PNAS 101: 16630-16635.
7. Chang, I., Gilbert, E.S., Eliashberg, N. & Keasling, J.D. 2003. A three-dimensional, stochastic simulation of biofilm growth and transport-related factors that affect structure. Microbiology 149: 2859-2871.
8. Charlesworth, B. 2009. Fundamental concepts in genetics: effective population size and patterns of molecular evolution and variation. Nat. Rev. Gen. 10: 195-205.
9. Chen, X. & Stewart, P.S. 1996. Chlorine penetration into artificial biofilm is limited by a reaction-diffusion interaction. Environ. Sci. Technol. 30: 2078-2083.
10. Cochran, W.L., McFeters, G.A. & Stewart, P.S. 2000. Reduced susceptibility of thin Pseudomonas aeruginosa biofilms to hydrogen peroxide and monochloramine. J. Appl. Microbiol. 88: 22-30.
11. Conibear, T.C., Collins, S.L. & Webb, J.S. 2009. Role of mutation in Pseudomonas aeruginosa biofilm development. PLoS ONE 14: e6289.
12. Costerton, J.W., Cheng, K.-J., Geesey, G.G., Ladd, T.I., Nickel, J.C., Dasgupta, M. et al. 1987. Bacterial biofilms in nature and disease. Annu. Rev. Microbiol. 41: 435-464.
13. Drenkard, E. & Ausubel, F.M. 2002. Pseudomonas biofilm formation and antibiotic resistance are linked to phenotypic variation. Nature 416: 740-743.
14. Excoffier, L. & Nicolas, R. 2008. Surfing during population expansions promotes genetic revolutions and structuration. Trends Ecol. Evol. 23: 347-351.
15. Felsenstein, J. 1973. Maximum-likelihood estimation of evolutionary trees from continuous characters. Am. J. Hum. Genet. 25: 471-492.
16. Galhardo, R.S., Hastings, P.J. & Rosenberg, S.M. 2007. Mutation as a stress response and the regulation of evolvability. Crit. Rev. Biochem. Mol. Biol. 42: 399-435.
17. Gause, G.F. 1932. Experimental studies on the struggle for existence: 1. Mixed population of two species of yeast. J. Exp. Biol. 9: 389-402.
18. Gini, C. 1912. Variabilità e Mutabilità (Variability and Mutability). C. Cuppini, Bologna.
19. Hallatschek, O. & Nelson, D.R. 2010. Life at the front of an expanding population. Evolution 64: 193-206.
20. Hallatschek, O., Hersen, P., Ramanathan, S. & Nelson, D.R. 2007. Genetic drift at expanding frontiers promotes gene segregation. Proc. Natl Acad. Sci. USA 104: 19926-19930.
21. Hall-Stoodley, L., Costerton, J.W. & Stoodley, P. 2004. Bacterial biofilms: from the natural environment to infectious diseases. Nat. Rev. Microbiol. 2: 95-108.
22. Holt, J.G. 1994. Bergey's Manual of Determinative Bacteriology, 9th edn. Williams and Wilkins, Baltimore, MD.
23. Jothi, R., Balaji, S., Wuster, A., Grochow, J.A., Gsponer, J., Przytycka, T.M. et al. 2009. Genomic analysis shows a tight link between transcription factor dynamics and regulatory network architecture. Mol. Syst. Biol. 5: 294.
24. Kassen, R. & Rainey, P.B. 2004. The ecology and genetics of microbial diversity. Annu. Rev. Microbiol. 58: 207-231.
25. Keightley, P.D. & Bataillon, T.M. 2000. Multigeneration maximum-likelihood analysis applied to mutation-accumulation experiments in Caenorhabditis elegans. Genetics 154: 1193-1201.
26. Kimura, M. 1983. The Neutral Theory of Molecular Evolution. Cambridge University Press, Cambridge, MA.
27. Kimura, M. & Crow, J. 1964. The number of alleles that can be maintained in a finite population. Genetics 49: 725-738.
28. Kingman, J.F.C. 1982. On the genealogy of large populations. J. Appl. Prob. 19A: 27-43.
29. Kreft, J.-U., Booth, G. & Wimpenny, J.W.T. 1998. Bacsim, a simulator for individual-based modelling of bacterial colony growth. Microbiology 144: 3275-3287.
30. Lewis, K. 2001. Riddle of biofilm resistance, Antimicrob. Agents Chemother. 45: 999-1007.
31. Luria, S.E. & Delbrück, M. 1943. Mutations of bacteria from virus sensitivity to virus resistance. Genetics 28: 491-511.
32. Mah, T.F. & O'Toole, G.A. 2001. Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol. 9: 34-39.
33. Matic, I., Radman, M., Taddei, F., Picard, B., Dolt, C., Bingen, E. et al. 1997. Highly variable mutation rates in commensal and pathogenic Escherichia coli. Science 277: 1833-1834.
34. Moran, P.A.P. 1962. The Statistical Processes of Evolutionary Theory. Clarendon Press, Oxford.
35. Ponciano, J.M., La, H.-J., Joyce, P. & Forney, L.J. 2009. Evolution of diversity in spatially structured Escherichia coli populations. Appl. Environ. Microbiol. 75: 6047-6054.
36. Prado, F. & Kerr, B. 2009. The evolution of restraint in bacterial biofilms under nontransitive competition. Evolution 62: 538-548.
37. R Development Core Team 2011. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria, ISBN 3-900051-07-0, Available from.
38. Rosindell, J., Wong, Y. & Etienne, R.S. 2008. A coalescent approach in spatial neutral ecology. Ecol. Inform. 2008: 259-271.
39. Simpson, E.H. 1949. Measurement of diversity. Nature 163: 688.
40. Stewart, P.S. 1996. Theoretical aspects of antibiotic diffusion into microbial biofilms. Antimicrob. Agents Chemother. 40: 2517-2522.
41. Stewart, P.S. & Costerton, J.W. 2001. Antibiotic resistance of bacteria in biofilms. Lancet 358: 135-138.
42. ® 320N. J. Hosp. Infect. 62: 487-493.
43. Waite, R.D., Struthers, J.K. & Dowson, C.G. 2001. Spontaneous sequence duplication within an open reading frame of the pneumococcal type 3 capsule locus causes high frequency phase variation. Mol. Microbiol. 42: 1223-1232.
44. Wiuff, C., Zappala, R.M., Regoes, R.R., Garner, K.N., Baquero, F. & Levin, B.R. 2005. Phenotypic tolerance: antibiotic enrichment of noninherited resistance in bacterial populations. Antimicrob. Agents Chemother. 49: 1483-1494.
45. Wrande, M., Roth, J.R. & Hughes, D. 2008. Accumulation of mutants in "aging" bacterial colonies is due to growth under selection, not stress-induced mutagenesis. Proc. Natl Acad. Sci. USA 105: 11863-11868.
46. Wright, S. 1931. Evolution in Mendelian populations. Genetics 16: 97-159.
47. Wright, S. 1943. Isolation by distance. Genetics 28: 114-138.
48. Yachi, S. & Loreau, M. 1999. Biodiversity and ecosystem productivity in a fluctuating environment: the insurance hypothesis. Proc. Natl Acad. Sci. U S A 96: 1463-1468.
49. Yarwood, J.M., Paquette, K.M, Tikh, I.B., Volper, E.M. & Greenberg, E.P. 2007. Generation of virulence factor variants in Staphylococcus aureus biofilms. J. Bacteriol. 189: 7961-7967.