Effects of Spatial Structure and Reduced Growth Rates on Evolution in Bacterial Populations

  • Michael T. France
  • Ben J. Ridenhour
  • Larry J. ForneyEmail author
Part of the Grand Challenges in Biology and Biotechnology book series (GCBB)


The evolutionary forces that create and maintain the awesome diversity observed in microbial communities and populations are not well understood. For the most part, previous studies on microbial evolution have been done using model species that are grown in well-mixed homogenous environments in which cells experience continuous or episodic periods of exponential growth. The relevance of these experimental systems to the evolution of naturally occurring populations is limited because bacterial populations in most environments reside in spatially structured heterogeneous habitats in which cell growth is slowed by nutrient limitation and cells often experience prolonged periods of stasis. Here we review and discuss how spatial structure and slow growth influence the evolution of microbial populations. We focus our discussion on microbial populations contained within biofilms, which are complex assemblages of microbial cells enclosed in self-made extracellular matrices. Biofilm-bound populations have spatial structure and contain subpopulations that are growing slowly. Studies have shown that spatial structure limits competition to a local scale thereby protracting selective sweeps. Additionally, reduced growth rates directly impact the rate at which selection can alter genotype frequencies in populations. Combined, these characteristics lead to the emergence and maintenance of genetic diversity within biofilms. We contend that the findings of studies on evolutionary processes in bacterial biofilms can readily be extrapolated to other spatially structured microbial habitats, such as soils and sediments, in which nutrient limitation causes slow growth.


  1. Adams J, Rosenzweig F (2014) Experimental microbial evolution: history and conceptual underpinnings. Genomics 104:393–398PubMedCrossRefGoogle Scholar
  2. Amato SM, Fazen CH, Henry TC et al (2014) The role of metabolism in bacterial persistence. Front Microbiol 5:1–9CrossRefGoogle Scholar
  3. Anderson P, Roth J (1981) Spontaneous tandem genetic duplications in Salmonella typhimurium arise by unequal recombination between rRNA (rrn) cistrons. Proc Natl Acad Sci USA 78:3113–3117PubMedCrossRefGoogle Scholar
  4. Anderson JT, Lee C, Rushworth CA et al (2013) Genetic trade-offs and conditional neutrality contribute to local adaptation. Mol Ecol 22:699–708PubMedCrossRefGoogle Scholar
  5. Barton NH, Briggs DEG, Eisen JA et al (2007) Evolution, 1st edn. Cold Spring Harbor Laboratory Press, New YorkGoogle Scholar
  6. Battin TJ, Kaplan LA, Denis Newbold J, Hansen CME (2003) Contributions of microbial biofilms to ecosystem processes in stream mesocosms. Nature 426:439–442PubMedCrossRefGoogle Scholar
  7. Besemer K, Singer G, Hödl I, Battin TJ (2009) Bacterial community composition of stream biofilms in spatially variable-flow environments. Appl Environ Microbiol 75:7189–7195PubMedPubMedCentralCrossRefGoogle Scholar
  8. Bjelland S (2003) Mutagenicity, toxicity and repair of DNA base damage induced by oxidation. Mutat Res 531:37–80PubMedCrossRefGoogle Scholar
  9. Boles BR, Singh PK (2008) Endogenous oxidative stress produces diversity and adaptability in biofilm communities. Proc Natl Acad Sci USA 105:12503–12508PubMedCrossRefGoogle Scholar
  10. Boles BR, Thoendel M, Singh PK (2004) Self-generated diversity produces “insurance effects” in biofilm communities. Proc Natl Acad Sci USA 101:16630–16635PubMedCrossRefGoogle Scholar
  11. Brauner A, Fridman O, Gefen O, Balaban NQ (2016) Distinguishing between resistance, tolerance and persistence to antibiotic treatment. Nat Rev Microbiol 14:320–330PubMedCrossRefGoogle Scholar
  12. Bridges B (1992) Mutagenesis after exposure of bacteria to ultraviolet-light and delayed photoreversal. Mol Gen Genet 233:331–336PubMedCrossRefGoogle Scholar
  13. Brooks JD, Flint SH (2008) Biofilms in the food industry: problems and potential solutions. Int J Food Sci Technol 43:2163–2176CrossRefGoogle Scholar
  14. Bull HJ, Lombardo MJ, Rosenberg SM (2001) Stationary-phase mutation in the bacterial chromosome: recombination protein and DNA polymerase IV dependence. Proc Natl Acad Sci USA 98:8334–8341PubMedCrossRefGoogle Scholar
  15. Burch CL, Chao L (2000) Evolvability of an RNA virus is determined by its mutational neighbourhood. Nature 406:625–628PubMedCrossRefGoogle Scholar
  16. Burmolle M, Kjoller A, Sorensen SJ (2012) An invisible workforce: biofilms in the soil. In: Lear G, Lewis GD (eds) Microbial biofilm: current research and applications. Caister Academic Press, Norfolk, pp 61–71Google Scholar
  17. Carlucci AF, Williams PM (1978) Simulated in situ growth rates of pelagic marine bacteria. Naturwissenschaften 65:541–542CrossRefGoogle Scholar
  18. Cherry JL, Wakeley J (2003) A diffusion approximation for selection and drift in a subdivided population. Genetics 163:421–428PubMedPubMedCentralGoogle Scholar
  19. Chiang W, Tolker-Nielsen T (2010) Extracellular DNA as a matrix component in microbial biofilms. In: Kikuchi Y, Rykova E (eds) Extracellular nucleic acids. Springer, Berlin, pp 1–14Google Scholar
  20. Christensen BB, Sternberg C, Molin S (1996) Bacterial plasmid conjugation on semi-solid surfaces monitored with the green fluorescent protein (GFP) from Aequorea victoria as a marker. Gene 173:59–65PubMedCrossRefGoogle Scholar
  21. Christensen BB, Sternberg C, Andersen JB et al (1998) Establishment of new genetic trait in a microbial biofilm community. Appl Environ Microbiol 64:2247–2255PubMedPubMedCentralGoogle Scholar
  22. Cohan FM (2016) Bacterial speciation: genetic sweeps in bacterial species. Curr Biol 26:R112–R115PubMedCrossRefGoogle Scholar
  23. Costerton JW, Geesey GG, Cheng K-J (1978) How bacteria stick. Sci Am 238:86–95CrossRefGoogle Scholar
  24. Davies J, Davies D (2010) Origins and evolution of antibiotic resistance. Microbiol Mol Biol Rev 74:417–433PubMedPubMedCentralCrossRefGoogle Scholar
  25. de Beer D, Stoodley P, Roe F, Lewandowski Z (1994) Effects of biofilm structures on oxygen distribution and mass-transport. Biotechnol Bioeng 43:1131–1138PubMedCrossRefGoogle Scholar
  26. Debellis T, Kernaghan G, Bradley R, Widden P (1998) Growth rate of bacterial communities in soils at varying pH: a comparison of the thymidine and leucine incorporation techniques. Microb Ecol 36:316–327CrossRefGoogle Scholar
  27. Devictor V, Clavel J, Julliard R et al (2010) Defining and measuring ecological specialization. J Appl Ecol 47:15–25CrossRefGoogle Scholar
  28. Dixon JL, Turley CM (2001) Measuring bacterial production in deep-sea sediments using 3H-thymidine incorporation: ecological significance. Microb Ecol 42:549–561PubMedCrossRefGoogle Scholar
  29. Domenech M, Ramos-Sevillano E, García E et al (2013) Biofilm formation avoids complement immunity and phagocytosis of Streptococcus pneumoniae. Infect Immun 81:2606–2615PubMedPubMedCentralCrossRefGoogle Scholar
  30. Driffield K, Miller K, Bostock JM et al (2008) Increased mutability of Pseudomonas aeruginosa in biofilms. J Antimicrob Chemother 61(5):1053–1056PubMedCrossRefPubMedCentralGoogle Scholar
  31. Duncan B (1980) Mutagenic deamination of cytosine residues in DNA. Nature 287:560–561PubMedCrossRefPubMedCentralGoogle Scholar
  32. Dykhuizen DE (1998) Santa Rosalia revisited: why are there so many species of bacteria? Antonie van Leeuwenhoek 73:25–33PubMedCrossRefPubMedCentralGoogle Scholar
  33. Eastman JM, Harmon LJ, La HJ et al (2011) The onion model, a simple neutral model for the evolution of diversity in bacterial biofilms. J Evol Biol 24:2496–2504PubMedCrossRefPubMedCentralGoogle Scholar
  34. Elena SF, Cooper VS, Lenski RE (1996) Punctuated evolution caused by selection of rare beneficial mutations. Science 272:1802–1804PubMedCrossRefPubMedCentralGoogle Scholar
  35. Elias S, Banin E (2012) Multi-species biofilms: living with friendly neighbors. FEMS Microbiol Rev 36(5):990–1004. CrossRefPubMedPubMedCentralGoogle Scholar
  36. Ellis CN, Traverse CC, Mayo-smith L et al (2015) Character displacement and the evolution of niche complementarity in a model biofilm community. Evolution (NY) 69:283–293CrossRefGoogle Scholar
  37. Erban R, Chapman SJ (2007) Reactive boundary conditions for stochastic simulations of reaction-diffusion processes. Phys Biol 4:16–28PubMedCrossRefPubMedCentralGoogle Scholar
  38. Ferenci T (2016) Trade-off mechanisms shaping the diversity of bacteria. Trends Microbiol 24:209–223PubMedCrossRefPubMedCentralGoogle Scholar
  39. Fisher RRA (1928) The possible modification of the response of the wild type to recurrent mutations. Am Nat 62:115–116CrossRefGoogle Scholar
  40. Flemming H-C (2011) Microbial biofouling: unsolved problems, insufficient approaches, and possible solutions. In: Flemming H-C, Wingender J, Szewzyk U (eds) Biofilm highlights. Springer, Berlin, pp 81–109CrossRefGoogle Scholar
  41. Flemming HC, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8:623–633PubMedCrossRefGoogle Scholar
  42. Flemming H-C, Wingender J, Szewzyk U et al (2016) Biofilms: an emergent form of bacterial life. Nat Rev Microbiol 14:563–575PubMedCrossRefGoogle Scholar
  43. Foster PL (2006) Methods for determining spontaneous mutation rates. Methods Enzymol 409:195–213PubMedPubMedCentralCrossRefGoogle Scholar
  44. Foster PL (2007) Stress-induced mutagenesis in bacteria. Crit Rev Biochem Mol Biol 42:373–397PubMedPubMedCentralCrossRefGoogle Scholar
  45. Fox RE, Zhong X, Krone SM, Top EM (2008) Spatial structure and nutrients promote invasion of IncP-1 plasmids in bacterial populations. ISME J 2:1024–1039PubMedPubMedCentralCrossRefGoogle Scholar
  46. Frederico LA, Kunkel TA, Shaw BR (1993) Cytosine deamination in mismatched base pairs. Biochemistry 32:6523–6530PubMedCrossRefPubMedCentralGoogle Scholar
  47. Frost LS, Leplae R, Summers AO, Toussaint A (2005) Mobile genetic elements: the agents of open source evolution. Nat Rev Microbiol 3:722–732PubMedPubMedCentralCrossRefGoogle Scholar
  48. Futuyma DJ, Moreno G (1988) The evolution of ecological specialization. Annu Rev Ecol Syst 19:207–233CrossRefGoogle Scholar
  49. Gause GF (1934) The struggle for existence. Williams & Wilkins, Baltimore, MDCrossRefGoogle Scholar
  50. Gillespie JH (1983) Some properties of finite populations experiencing strong selection and weak mutation. Am Nat 121:691–708CrossRefGoogle Scholar
  51. Goodman MF (2002) Error-prone repair DNA polymerases in prokaryotes and eukaryotes. Annu Rev Biochem 71:17–50PubMedCrossRefGoogle Scholar
  52. Habets MGJL, Czárán T, Hoekstra RF, de Visser JAGM (2007) Spatial structure inhibits the rate of invasion of beneficial mutations in asexual populations. Proc R Soc B Biol Sci 274:2139–2143CrossRefGoogle Scholar
  53. Hall-Stoodley L, Stoodley P (2009) Evolving concepts in biofilm infections. Cell Microbiol 11:1034–1043PubMedCrossRefGoogle Scholar
  54. Hannan S, Ready D, Jasni AS et al (2010) Transfer of antibiotic resistance by transformation with eDNA within oral biofilms. FEMS Immunol Med Microbiol 59:345–349PubMedCrossRefGoogle Scholar
  55. Harris D, Paul EA (1994) Measurement of bacterial growth rates in soil. Appl Soil Ecol 1:277–290CrossRefGoogle Scholar
  56. Hausner M, Wuertz S (1999) High rates of conjugation in bacterial biofilms as determined by quantitative in situ analysis. Appl Environ Microbiol 65:3710–3713PubMedPubMedCentralGoogle Scholar
  57. Hendrickx L, Hausner M, Wuertz S (2003) Natural genetic transformation in monoculture Acinetobacter sp. Appl Environ Microbiol 69:1721–1727PubMedPubMedCentralCrossRefGoogle Scholar
  58. Hobley L, Harkins C, MacPhee CE, Stanley-Wall NR (2015) Giving structure to the biofilm matrix: an overview of individual strategies and emerging common themes. FEMS Microbiol Rev 39:649–669PubMedPubMedCentralCrossRefGoogle Scholar
  59. Høiby N, Bjarnsholt T, Givskov M et al (2010) Antibiotic resistance of bacterial biofilms. Int J Antimicrob Agents 35:322–332PubMedCrossRefGoogle Scholar
  60. Høiby N, Ciofu O, Johansen HK et al (2011) The clinical impact of bacterial biofilms. Int J Oral Sci 3:55–65PubMedPubMedCentralCrossRefGoogle Scholar
  61. Hoyle BD, Alcantara J, Costerton JW (1992) Pseudomonas aeruginosa biofilm as a diffusion barrier to piperacillin. Antimicrob Agents Chemother 36:2054–2056PubMedPubMedCentralCrossRefGoogle Scholar
  62. Imlay JA (2003) Pathways of oxidative damage. Annu Rev Microbiol 57:395–418PubMedCrossRefGoogle Scholar
  63. James GA, Swogger E, Wolcott R et al (2007) Biofilms in chronic wounds. Wound Repair Regen 16:37–44PubMedCrossRefGoogle Scholar
  64. Jannasch HW (1969) Estimations of bacterial growth rates in natural waters. J Bacteriol 99:156–160PubMedPubMedCentralGoogle Scholar
  65. Jensen PØ, Givskov M, Bjarnsholt T, Moser C (2010) The immune system vs. Pseudomonas aeruginosa biofilms. FEMS Immunol Med Microbiol 59:292–305PubMedCrossRefGoogle Scholar
  66. Joyce P, Rokyta DR, Beisel CJ, Orr HA (2008) A general extreme value theory model for the adaptation of DNA sequences under strong selection and weak mutation. Genetics 180:1627–1643PubMedPubMedCentralCrossRefGoogle Scholar
  67. Kajiura T, Wada H, Ito K et al (2006) Conjugative plasmid transfer in the biofilm formed by Enterococcus faecalis. J Heal Sci 52:358–367CrossRefGoogle Scholar
  68. Kassen R (2014) Experimental evolution and the nature of biodiversity. Roberts, Greenwood Village, COGoogle Scholar
  69. Kawecki TJ, Lenski RE, Ebert D et al (2012) Experimental evolution. Trends Ecol Evol 27:547–560PubMedCrossRefGoogle Scholar
  70. Kerr B, Riley MA, Feldman MW, Bohannan BJM (2002) Local dispersal promotes biodiversity in a real-life game of rock-paper-scissors. Nature 418:171–174PubMedCrossRefGoogle Scholar
  71. Kidwell M, Lisch D (2001) Perspective: transposable elements parasitic DNA and genome evolution. Int J Org Evol 55:1–24CrossRefGoogle Scholar
  72. Kim W, Racimo F, Schluter J et al (2014) Importance of positioning for microbial evolution. Proc Natl Acad Sci USA 111:E1639–E1647PubMedCrossRefGoogle Scholar
  73. Kirchman DL (2016) Growth rates of microbes in the oceans. Annu Rev Mar Sci 8:285–309CrossRefGoogle Scholar
  74. Kivisaar M (2003) Minireview: Stationary phase mutagenesis: mechanisms that accelerate adaptation of microbial populations under environmental stress. Environ Microbiol 5:814–827PubMedCrossRefGoogle Scholar
  75. Kivisaar M (2010) Mechanisms of stationary-phase mutagenesis in bacteria: mutational processes in pseudomonads. FEMS Microbiol Lett 312:1–14PubMedCrossRefGoogle Scholar
  76. Klevens RM, Edwards JR, Richards CL Jr et al (2007) Estimating health care-associated infections and deaths in U.S. hospitals, 2002. Public Heal Rep 122:160–166CrossRefGoogle Scholar
  77. Kopac S, Wang Z, Wiedenbeck J et al (2014) Genomic heterogeneity and ecological speciation within one subspecies of Bacillus subtilis. Appl Environ Microbiol 80:4842–4853PubMedPubMedCentralCrossRefGoogle Scholar
  78. Kouzel N, Oldewurtel ER, Maier B (2015) Gene transfer efficiency in Gonococcal biofilms: role of biofilm age, architecture, and pilin antigenic variation. J Bacteriol 197:2422–2431PubMedPubMedCentralCrossRefGoogle Scholar
  79. Kraemer S, Boynton P (2017) Evidence for microbial local adaptation in nature. Mol Ecol 26:1860–1876PubMedCrossRefGoogle Scholar
  80. Król JE, Nguyen HD, Rogers LM et al (2011) Increased transfer of a multidrug resistance plasmid in Escherichia coli biofilms at the air-liquid interface. Appl Environ Microbiol 77:5079–5088PubMedPubMedCentralCrossRefGoogle Scholar
  81. Kryazhimskiy S, Rice DP, Desai MM (2012) Population subdivision and adaptation in asexual populations of Saccharomyces cerevisiae. Evolution (NY) 66:1931–1941CrossRefGoogle Scholar
  82. Kumar CG, Anand SK (1998) Significance of microbial biofilms in food industry: a review. Int J Food Microbiol 42:9–27PubMedCrossRefGoogle Scholar
  83. Lang GI, Rice DP, Hickman MJ et al (2013) Pervasive genetic hitchhiking and clonal interference in forty evolving yeast populations. Nature 500:571–574PubMedPubMedCentralCrossRefGoogle Scholar
  84. Levin-Reisman I, Ronin I, Gefen O et al (2017) Antibiotic tolerance facilitates the evolution of resistance. Science 355:826–830PubMedCrossRefGoogle Scholar
  85. Levinson G, Gutman GA (1987) Slipped-strand mispairing: a major mechanism for DNA sequence evolution. Mol Biol Evol 4:203–221PubMedGoogle Scholar
  86. Lewis K (2007) Persister cells, dormancy and infectious disease. Nat Rev Microbiol 5:48–56PubMedCrossRefGoogle Scholar
  87. Lewis K (2010) Persister cells. Annu Rev Microbiol 64:357–372PubMedCrossRefGoogle Scholar
  88. Li Y, Lau PCY, Lee JH et al (2001) Natural genetic transformation of Streptococcus mutans growing in biofilms. J Bacteriol 183:897–908PubMedPubMedCentralCrossRefGoogle Scholar
  89. Lomstein B, Langerhuus A, D’Hondt S, Jorgensen B, Spivack A (2012) Endospore abundance, microbial growth, and necromass turnover in deep sub-seafloor sediment. Nature 484(7392):101–104PubMedCrossRefGoogle Scholar
  90. Lynch AS, Robertson GT (2008) Bacterial and fungal biofilm infections. Annu Rev Med 59:415–428PubMedCrossRefGoogle Scholar
  91. Macfarlane S, Dillon JF (2007) Microbial biofilms in the human gastrointestinal tract. J Appl Microbiol 102:1187–1196PubMedCrossRefGoogle Scholar
  92. Maisonneuve E, Gerdes K (2014) Molecular mechanisms underlying bacterial persisters. Cell 157:539–548PubMedCrossRefGoogle Scholar
  93. Mazin A, Gimadutdinov O, Turkin S et al (1985) Non-enzymatic DNA methylation by S-adenosylmethionine results in the formation of minor thymine residues and 5-methylcytosine from cytosine. Mol Biol 19:903–914Google Scholar
  94. Meckenstock RU, Elsner M, Griebler C et al (2015) Biodegradation: updating the concepts of control for microbial cleanup in contaminated aquifers. Environ Sci Technol 49:7073–7081PubMedCrossRefGoogle Scholar
  95. Merod RT, Wuertz S (2014) Extracellular polymeric substance architecture influences natural genetic transformation of Acinetobacter baylyi in biofilms. Appl Environ Microbiol 80:7752–7757PubMedPubMedCentralCrossRefGoogle Scholar
  96. Molin S, Tolker-Nielsen T (2003) Gene transfer occurs with enhanced efficiency in biofilms and induces enhanced stabilisation of the biofilm structure. Curr Opin Biotechnol 14:255–261PubMedCrossRefGoogle Scholar
  97. Mulcahy LR, Isabella VM, Lewis K (2014) Pseudomonas aeruginosa biofilms in disease. Microb Ecol 68:1–12PubMedCrossRefGoogle Scholar
  98. Muller CJ (1932) Some genetic aspects of sex. Am Nat 66:118–138CrossRefGoogle Scholar
  99. Nadell CD, Drescher K, Foster KR (2016) Spatial structure, cooperation and competition in biofilms. Nat Rev Microbiol 14:589–600PubMedCrossRefGoogle Scholar
  100. Nahum JR, Godfrey-Smith P, Harding BN et al (2015) A tortoise–hare pattern seen in adapting structured and unstructured populations suggests a rugged fitness landscape in bacteria. Proc Natl Acad Sci USA 112:201410631CrossRefGoogle Scholar
  101. Ochman H, Lawrence J, Groisman E (2000) Lateral gene transfer and the nature of bacterial innovation. Nature 405:299–304CrossRefGoogle Scholar
  102. Olsen I (2015) Biofilm-specific antibiotic tolerance and resistance. Eur J Clin Microbiol Infect Dis 34:877–886PubMedCrossRefGoogle Scholar
  103. Orr HA (2002) The population genetics of adaptation: the adaptation of DNA sequences. Evolution 56:1317–1330PubMedCrossRefGoogle Scholar
  104. Otto M (2008) Staphylococcal biofilms. Curr Top Microbiol Immunol 322:207–228PubMedPubMedCentralGoogle Scholar
  105. Palestrant D, Holzknecht ZE, Collins BH et al (2004) Microbial biofilms in the gut: visualization by electron microscopy and by acridine orange staining. Ultrastruct Pathol 28:23–27PubMedCrossRefGoogle Scholar
  106. Pannell JR, Fields PD (2014) Evolution in subdivided plant populations: concepts, recent advances and future directions. New Phytol 201:417–432PubMedCrossRefGoogle Scholar
  107. Parsek MR, Singh PK (2003) Bacterial biofilms: an emerging link to disease pathogenesis. Annu Rev Microbiol 57:677–701PubMedCrossRefGoogle Scholar
  108. Paul BJ, Duthie HC, Taylor WD (1991) Nutrient cycling by biofilms in running waters of differing nutrient status. J North Am Benthol Soc 10:31–41CrossRefGoogle Scholar
  109. Percival SL, Hill KE, Williams DW et al (2012) A review of the scientific evidence for biofilms in wounds. Wound Repair Regen 20:647–657PubMedCrossRefGoogle Scholar
  110. Perfeito L, Pereira MI, Campos PRA, Gordo I (2008) The effect of spatial structure on adaptation in Escherichia coli. Biol Lett 4:57–59PubMedCrossRefGoogle Scholar
  111. Poltak SR, Cooper VS (2011) Ecological succession in long-term experimentally evolved biofilms produces synergistic communities. ISME J 5:369–378PubMedCrossRefGoogle Scholar
  112. Ponciano JM, La HJ, Joyce P, Forney LJ (2009) Evolution of diversity in spatially structured Escherichia coli populations. Appl Environ Microbiol 75:6047–6054PubMedPubMedCentralCrossRefGoogle Scholar
  113. Qi L, Li H, Zhang C et al (2016) Relationship between antibiotic resistance, biofilm formation, and biofilm-specific resistance in Acinetobacter baumannii. Front Microbiol 7:1–10Google Scholar
  114. Rainey PB, Travisano M (1998) Adaptive radiation in a heterogeneous environment. Nature 394:69–72PubMedCrossRefGoogle Scholar
  115. Rodgers K, Mcvey M (2016) Error-prone repair of DNA double-strand breaks. J Cell Physiol 231:15–24PubMedPubMedCentralCrossRefGoogle Scholar
  116. Roesch L, Fulthorpe R, Riva A et al (2007) Pyrosequencing enumerates and contrasts soil microbial diversity. ISME J 1:283–290PubMedPubMedCentralCrossRefGoogle Scholar
  117. Rogers J, Dowsett AB, Dennis PJ et al (1994) Influence of temperature and plumbing material selection on biofilm formation and growth of Legionella pneumophila in a model potable water system containing complex microbial flora. Appl Environ Microbiol 60:1585–1592PubMedPubMedCentralGoogle Scholar
  118. Rosche WA, Foster PL (2000) Determining mutation rates in bacterial populations. Methods 20:4–17PubMedPubMedCentralCrossRefGoogle Scholar
  119. Rousk J, Bååth E (2011) Growth of saprotrophic fungi and bacteria in soil. FEMS Microbiol Ecol 78:17–30PubMedCrossRefGoogle Scholar
  120. Rozen DE, Habets MGJL, Handel A, de Visser JAGM (2008) Heterogeneous adaptive trajectories of small populations on complex fitness landscapes. PLoS One 3:14–17CrossRefGoogle Scholar
  121. Rydberg B, Lindahl T (1982) Nonenzymatic methylation of DNA by the intracellular methyl group donor S-adenosyl-L-methionine is a potentially mutagenic reaction. EMBO J 1:211–216PubMedPubMedCentralCrossRefGoogle Scholar
  122. Saumaa S, Tover A, Kasak L, Kivisaar M (2002) Different spectra of stationary-phase mutations in early-arising versus late-arising mutants of Pseudomonas putida: involvement of the DNA repair enzyme MutY and the stationary-phase sigma factor RpoS. J Bacteriol 184:6957–6965PubMedPubMedCentralCrossRefGoogle Scholar
  123. Schaaper R, Loeb L (1980) Depurination causes mutations in SOS-induced cells. PNAS 78:1773–1777CrossRefGoogle Scholar
  124. Schenk MF, Witte S, Salverda MLM et al (2015) Role of pleiotropy during adaptation of TEM-1 β-lactamase to two novel antibiotics. Evol Appl 8:248–260PubMedCrossRefGoogle Scholar
  125. Schloss PD, Handelsman J (2006) Toward a census of bacteria in soil. PLoS Comput Biol 2:0786–0793CrossRefGoogle Scholar
  126. Schumacher MA, Balani P, Min J et al (2015) HipBA-promoter structures reveal the basis of heritable multidrug tolerance. Nature 524:59–64PubMedCrossRefGoogle Scholar
  127. Seoane J, Yankelevich T, Dechesne A et al (2011) An individual-based approach to explain plasmid invasion in bacterial populations. FEMS Microbiol Ecol 75:17–27PubMedCrossRefGoogle Scholar
  128. Shapiro BJ, Polz MF (2014) Ordering microbial diversity into ecologically and genetically cohesive units. Trends Microbiol 22:235–247PubMedPubMedCentralCrossRefGoogle Scholar
  129. Simões M, Pereira MO, Vieira MJ (2005) Effect of mechanical stress on biofilms challenged by different chemicals. Water Res 39:5142–5152PubMedCrossRefGoogle Scholar
  130. Sniegowski PD, Gerrish PJ (2010) Beneficial mutations and the dynamics of adaptation in asexual populations. Proc R Soc B Biol Sci 365:1255–1263Google Scholar
  131. Stalder T, Top EM (2016) Plasmid transfer in biofilms: a perspective on limitations and opportunities. NPJ Biofilms Microbiomes 2:16022PubMedPubMedCentralCrossRefGoogle Scholar
  132. Steenackers HP, Parijs I, Foster KR, Vanderleyden J (2016) Experimental evolution in biofilm populations. FEMS Microbiol Rev 40:373–397PubMedPubMedCentralCrossRefGoogle Scholar
  133. Sternberg C, Christensen BB, Johansen T et al (1999) Distribution of bacterial growth activity in flow-chamber biofilms. Appl Environ Microbiol 65:4108–4117PubMedPubMedCentralGoogle Scholar
  134. Stewart PS (1996) Theoretical aspects of antibiotic diffusion into microbial biofilms. Antimicrob Agents Chemother 40:2517–2522PubMedPubMedCentralCrossRefGoogle Scholar
  135. Stewart PS (1998) A review of experimental measurements of effective diffusive permeabilities and effective diffusion coefficients in biofilms. Biotechnol Bioeng 59:261–272PubMedCrossRefGoogle Scholar
  136. Stewart PS, Franklin MJ (2008) Physiological heterogeneity in biofilms. Nat Rev Microbiol 6:199–210PubMedCrossRefGoogle Scholar
  137. Stewart PS, Zhang T, Xu R et al (2016) Reaction–diffusion theory explains hypoxia and heterogeneous growth within microbial biofilms associated with chronic infections. NPJ Biofilms Microbiomes 2:16012PubMedPubMedCentralCrossRefGoogle Scholar
  138. Stoodley P, Sauer K, Davies DG, Costerton JW (2002) Biofilms as complex differentiated communities. Annu Rev Microbiol 56:187–209PubMedCrossRefGoogle Scholar
  139. Suzuki T, Ohsumi S, Makino K (1994) Mechanistic studies on depurination and apurinic site chain breakage in oligodeoxyribonucleotides. Nucleic Acids Res 22:4997–5003PubMedPubMedCentralCrossRefGoogle Scholar
  140. Thomas CM, Nielsen KM (2005) Mechanisms of, and barriers to, horizontal gene transfer between bacteria. Nat Rev Microbiol 3:711–721PubMedPubMedCentralCrossRefGoogle Scholar
  141. Tillman D (1994) Competition and biodiversity in spatially structured habitats. Ecology 75:2–16CrossRefGoogle Scholar
  142. Tolker-Nielsen T, Molin S (2000) Spatial organization of microbial biofilm communities. Microb Ecol 40:75–84PubMedGoogle Scholar
  143. Torres-cruz J, Van Der Woude MW (2003) Slipped-strand mispairing can function as a phase variation mechanism in Escherichia coli. J Bacteriol 185:6990–6994PubMedPubMedCentralCrossRefGoogle Scholar
  144. 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(3):E250–E259PubMedCrossRefGoogle Scholar
  145. Truglio JJ, Croteau DL, van Houten B, Kisker C (2006) Prokaryotic nucleotide excision repair: the UvrABC system. Chem Rev 106:233–252PubMedCrossRefGoogle Scholar
  146. Tyerman JG, Ponciano JM, Joyce P et al (2013) The evolution of antibiotic susceptibility and resistance during the formation of Escherichia coli biofilms in the absence of antibiotics. BMC Evol Biol 13:1–7CrossRefGoogle Scholar
  147. Van Meervenne E, De Weirdt R, Van Coillie E et al (2014) Biofilm models for the food industry: hot spots for plasmid transfer? Pathog Dis 70:332–338PubMedCrossRefGoogle Scholar
  148. Verstraelen H, Swidsinski A (2013) The biofilm in bacterial vaginosis: implications for epidemiology, diagnosis and treatment. Curr Opin Infect Dis 26:86–89PubMedCrossRefGoogle Scholar
  149. Wakeley J (1998) Segregating sites in Wright’s island model. Theor Popul Biol 53:166–174PubMedCrossRefGoogle Scholar
  150. Wang H, Ding S, Wang G et al (2013) In situ characterization and analysis of Salmonella biofilm formation under meat processing environments using a combined microscopic and spectroscopic approach. Int J Food Microbiol 167:293–302PubMedCrossRefPubMedCentralGoogle Scholar
  151. Webster NS, Negri AP, Base S (2006) Site-specific variation in Antarctic marine biofilms established on artificial surfaces. Environ Microbiol 8:1177–1190PubMedCrossRefPubMedCentralGoogle Scholar
  152. Wentland EJ, Stewart PS, Huang CT, McFeters GA (1996) Spatial variations in growth rate within Klebsiella pneumoniae colonies and biofilm. Biotechnol Prog 12:316–321PubMedCrossRefPubMedCentralGoogle Scholar
  153. Whitchurch CB, Tolker-nielsen T, Ragas PC et al (2002) Extracellular DNA required for bacterial biofilm formation. Science 295:59–60CrossRefGoogle Scholar
  154. Whitlock MC (2003) Fixation probability and time in subdivided populations. Genetics 164:767–779PubMedPubMedCentralGoogle Scholar
  155. Whitman WB, Coleman DC, Wiebe WJ et al (1998) Prokaryotes: the unseen majority. Proc Natl Acad Sci USA 95:6578–6583PubMedCrossRefPubMedCentralGoogle Scholar
  156. Wierzchos J, Vincent WF, Quesada A (2015) Microstructure and cyanobacterial composition of microbial mats from the High Arctic. Biodivers Conserv 24(4):841–863CrossRefGoogle Scholar
  157. Wijker CA, Wientjes NM, Lafleur MVM (1998) Mutation spectrum in the lacI gene, induced by gamma radiation in aqueous solution under oxic conditions. Mutat Res 403:137–147PubMedCrossRefPubMedCentralGoogle Scholar
  158. Williams I, Venables WA, Lloyd D et al (1997) The effects of adherence to silicone surfaces on antibiotic susceptibility in Staphylococcus aureus. Microbiology 143:2407–2413PubMedCrossRefPubMedCentralGoogle Scholar
  159. Wolcott RD, Rhoads DD, Bennett ME, et al (2010) Chronic wounds and the medical biofilm paradigm. J Wound Care 19:45–46, 48–50, 52–53PubMedCrossRefPubMedCentralGoogle Scholar
  160. Wright S (1932) The roles of mutation, inbreeding, crossbreeding and selection in evolution. In: Proceedings of the sixth international congress on genetics. Brooklyn Botanic Garden, Brooklyn, NY, pp 356–366Google Scholar
  161. Xu KD, Stewart PS, Xia F et al (1998) Spatial physiological heterogeneity in Pseudomonas aeruginosa biofilm is determined by oxygen availability. Appl Environ Microbiol 64:4035–4039PubMedPubMedCentralGoogle Scholar
  162. Yachi S, Loreau M (1999) Biodiversity and ecosystem productivity in a fluctuating environment: the insurance hypothesis. Proc Natl Acad Sci USA 96:1463–1468PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Michael T. France
    • 1
  • Ben J. Ridenhour
    • 1
    • 2
  • Larry J. Forney
    • 1
    • 2
    Email author
  1. 1.Institute for Bioinformatics and Evolutionary StudiesUniversity of IdahoMoscowUSA
  2. 2.Department of Biological SciencesUniversity of IdahoMoscowUSA

Personalised recommendations