The impact of natural transformation on adaptation in spatially structured bacterial populations

BMC Evolutionary Biology

Jan Engelstädter¹  Danesh Moradigaravand² 

[1] School of Biological Sciences, The University of Queensland, Brisbane, QLD 4072, Australia;Institute of Biogeochemistry and Pollutant Dynamics, ETH Zürich, 8092 Zürich, Switzerland

关键词: Spatially structured populations;    Biofilm;    Bacterial transformation;    Bacterial adaptation;   

Others  :  855171
DOI  :  10.1186/1471-2148-14-141

 received in 2014-02-20, accepted in 2014-06-08,  发布年份 2014

【 摘 要 】

Background

Recent studies have demonstrated that natural transformation and the formation of highly structured populations in bacteria are interconnected. In spite of growing evidence about this connection, little is known about the dynamics of natural transformation in spatially structured bacterial populations.

Results

In this work, we model the interdependency between the dynamics of the bacterial gene pool and those of environmental DNA in space to dissect the effect of transformation on adaptation. Our model reveals that even with only a single locus under consideration, transformation with a free DNA fragment pool results in complex adaptation dynamics that do not emerge in previous models focusing only on the gene shuffling effect of transformation at multiple loci. We demonstrate how spatial restriction on population growth and DNA diffusion in the environment affect the impact of transformation on adaptation. We found that in structured bacterial populations intermediate DNA diffusion rates predominantly cause transformation to impede adaptation by spreading deleterious alleles in the population.

Conclusion

Overall, our model highlights distinctive evolutionary consequences of bacterial transformation in spatially restricted compared to planktonic bacterial populations.

【 授权许可】

   
2014 Moradigaravand and Engelstädter; licensee BioMed Central Ltd.

【 图 表 】

【 参考文献 】

• [1]Costerton W, Veeh R, Shirtliff M, Pasmore M, Post C, Ehrlich G: The application of biofilm science to the study and control of chronic bacterial infections. J Clin Invest 2003, 112(10):1466-1477.
• [2]Hall-Stoodley L, Costerton JW, Stoodley P: Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2004, 2(2):95-108.
• [3]Rendueles O, Ghigo JM: Multi-species biofilms: how to avoid unfriendly neighbors. FEMS Microbiol Rev 2012, 36(5):972-989.
• [4]Fux CA, Costerton JW, Stewart PS, Stoodley P: Survival strategies of infectious biofilms. Trends Microbiol 2005, 13(1):34-40.
• [5]Vos M: Why do bacteria engage in homologous recombination? Trends Microbiol 2009, 17(6):226-232.
• [6]Madsen JS, Burmolle M, Hansen LH, Sorensen SJ: The interconnection between biofilm formation and horizontal gene transfer. Fems Immunol Med Mic 2012, 65(2):183-195.
• [7]Marks LR, Reddinger RM, Hakansson AP: High levels of genetic recombination during nasopharyngeal carriage and biofilm formation in streptococcus pneumoniae. Mbio 2012, 3(5):e00200-12.
• [8]Grande R, Di Campli E, Di Bartolomeo S, Verginelli F, Di Giulio M, Baffoni M, Bessa LJ, Cellini L: Helicobacter pylori biofilm: a protective environment for bacterial recombination. J Appl Microbiol 2012, 113(3):669-676.
• [9]Molin S, Tolker-Nielsen T: Gene transfer occurs with enhanced efficiency in biofilms and induces enhanced stabilisation of the biofilm structure. Curr Opin Biotechnol 2003, 14(3):255-261.
• [10]Li YH, Lau PC, Lee JH, Ellen RP, Cvitkovitch DG: Natural genetic transformation of Streptococcus mutans growing in biofilms. J Bacteriol 2001, 183(3):897-908.
• [11]Petersen FC, Tao L, Scheie AA: DNA binding-uptake system: a link between cell-to-cell communication and biofilm formation. J Bacteriol 2005, 187(13):4392-4400.
• [12]Matsukawa M, Greenberg EP: Putative exopolysaccharide synthesis genes influence Pseudomonas aeruginosa biofilm development. J Bacteriol 2004, 186(14):4449-4456.
• [13]Whitchurch CB, Tolker-Nielsen T, Ragas PC, Mattick JS: Extracellular DNA required for bacterial biofilm formation. Science 2002, 295(5559):1487.
• [14]Cohen E, Kessler DA, Levine H: Recombination dramatically speeds up evolution of finite populations. Phys Rev Lett 2005, 94(9):098102.
• [15]Moradigaravand D, Engelstädter J: The evolution of natural competence: disentangling costs and benefits of sex in bacteria. Am Nat 2013, 182(4):E112-126.
• [16]Moradigaravand D, Engelstädter J: The effect of bacterial recombination on adaptation on fitness landscapes with limited peak accessibility. Plos Comput Biol 2012, 8(10):e1002735.
• [17]Levin BR, Cornejo OE: The population and evolutionary dynamics of homologous gene recombination in bacteria. Plos Genet 2009, 5(8):e1000601.
• [18]Wylie CS, Trout AD, Kessler DA, Levine H: Optimal strategy for competence differentiation in bacteria. Plos Genet 2010, 6(9):e1001108.
• [19]Michod RE, Bernstein H, Nedelcu AM: Adaptive value of sex in microbial pathogens. Infect Genet Evol 2008, 8(3):267-285.
• [20]Redfield RJ: Do bacteria have sex? Nat Rev Genet 2001, 2(8):634-639.
• [21]Redfield RJ: Evolution of bacterial transformation - is sex with dead cells ever better than no sex at all. Genetics 1988, 119(1):213-221.
• [22]Redfield RJ, Schrag MR, Dean AM: The evolution of bacterial transformation: sex with poor relations. Genetics 1997, 146(1):27-38.
• [23]Nielsen KM, Johnsen PJ, Bensasson D, Daffonchio D: Release and persistence of extracellular DNA in the environment. Environ Biosafety Res 2007, 6(1–2):37-53.
• [24]Lewis K: Programmed death in bacteria. Microbiology and molecular biology reviews : MMBR 2000, 64(3):503-514.
• [25]Mortier-Barriere I, de Saizieu A, Claverys JP, Martin B: Competence-specific induction of recA is required for full recombination proficiency during transformation in Streptococcus pneumoniae. Mol Microbiol 1998, 27(1):159-170.
• [26]Finkel SE, Kolter R: DNA as a nutrient novel role for bacterial competence gene homologs. J Bacteriol 2001, 183(21):6288-6293.
• [27]Anderl JN, Franklin MJ, Stewart PS: Role of antibiotic penetration limitation in Klebsiella pneumoniae biofilm resistance to ampicillin and ciprofloxacin. Antimicrob Agents Chemother 2000, 44(7):1818-1824.
• [28]Anderl JN, Zahller J, Roe F, Stewart PS: Role of nutrient limitation and stationary-phase existence in Klebsiella pneumoniae biofilm resistance to ampicillin and ciprofloxacin. Antimicrob Agents Chemother 2003, 47(4):1251-1256.
• [29]Gilbert P, Collier PJ, Brown MR: Influence of growth rate on susceptibility to antimicrobial agents: biofilms, cell cycle, dormancy, and stringent response. Antimicrob Agents Chemother 1990, 34(10):1865-1868.
• [30]Donkor ES, Bishop CJ, Antonio M, Wren B, Hanage WP: High levels of recombination among Streptococcus pneumoniae Isolates from the Gambia. Mbio 2011, 2(3):e00040-11.
• [31]Leung MHY, Oriyo NM, Gillespie SH, Charalambous BM: The adaptive potential during nasopharyngeal colonisation of Streptococcus pneumoniae. Infect Genet Evol 2011, 11(8):1989-1995.
• [32]Engelstädter J, Moradigaravand D: Adaptation through genetic time travel? Fluctuating selection can drive the evolution of bacterial transformation. Proc R Soc Lond B 2014, 281(1775):20132609.
• [33]Szollosi GJ, Derenyi I, Vellai T: The maintenance of sex in bacteria is ensured by its potential to reload genes. Genetics 2006, 174(4):2173-2180.
• [34]Muller HJ: Some genetic aspects of sex. Am Nat 1932, 66:118-138.
• [35]Fisher RA: The Genetical Theory Of Natural Selection. USA: Oxford University Press; 1930.
• [36]Erik A: Interfering waves of adaptation promote spatial mixing. Martens and Oskar Hallatschek Genet 2011, 189(3):1045-1060. doi: 10.1534/genetics.111.130112. http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3213383/ webcite
• [37]Redfield RJ: Genes for breakfast: the have-your-cake-and-eat-it-too of bacterial transformation. J Hered 1993, 84(5):400-404.
• [38]Kreft JU, Picioreanu C, Wimpenny JWT, van Loosdrecht MCM: Individual-based modelling of biofilms. Microbiol-Sgm 2001, 147:2897-2912.
• [39]Wang Y, Roos KP, Taylor DE: Transformation of Helicobacter pylori by chromosomal metronidazole resistance and by a plasmid with a selectable chloramphenicol resistance marker. J Gen Microbiol 1993, 139(10):2485-2493.
• [40]Evans BA, Rozen DE: Significant variation in transformation frequency in Streptococcus pneumoniae. Isme J 2013, 7(4):791-799.
• [41]Wolfram Research, Inc: Mathematica, Version 8.0. Champaign, IL; 2010.