期刊论文详细信息
BMC Evolutionary Biology
The evolution of antibiotic susceptibility and resistance during the formation of Escherichia coli biofilms in the absence of antibiotics
Luke J Harmon4  Larry J Forney4  Paul Joyce3  José M Ponciano1  Jabus G Tyerman2 
[1] Department of Biology, University of Florida, Gainesville, FL, USA;Current address: Genomatica, Inc., 10520 Wateridge Circle, San Diego, CA, 92121, USA;Departments of Statistics, University of Idaho, Moscow, ID, 83844, USA;Initiative for Bioinformatics and Evolutionary Studies (IBEST), University of Idaho, Moscow, ID, 83844, USA
关键词: Diversity;    Mutations;    Bacterial biofilms;    Antibiotic resistance;    Evolution;   
Others  :  1130095
DOI  :  10.1186/1471-2148-13-22
 received in 2012-06-18, accepted in 2013-01-11,  发布年份 2013
PDF
【 摘 要 】

Background

Explanations for bacterial biofilm persistence during antibiotic treatment typically depend on non-genetic mechanisms, and rarely consider the contribution of evolutionary processes.

Results

Using Escherichia coli biofilms, we demonstrate that heritable variation for broad-spectrum antibiotic resistance can arise and accumulate rapidly during biofilm development, even in the absence of antibiotic selection.

Conclusions

Our results demonstrate the rapid de novo evolution of heritable variation in antibiotic sensitivity and resistance during E. coli biofilm development. We suggest that evolutionary processes, whether genetic drift or natural selection, should be considered as a factor to explain the elevated tolerance to antibiotics typically observed in bacterial biofilms. This could be an under-appreciated mechanism that accounts why biofilm populations are, in general, highly resistant to antibiotic treatment.

【 授权许可】

   
2013 Tyerman et al.; licensee BioMed Central Ltd.

【 预 览 】
附件列表
Files Size Format View
20150226162947579.pdf 395KB PDF download
Figure 3. 65KB Image download
Figure 2. 58KB Image download
Figure 1. 64KB Image download
【 图 表 】

Figure 1.

Figure 2.

Figure 3.

【 参考文献 】
  • [1]Costerton JW, Stewart PS, Greenberg EP: Bacterial biofilms: a common cause of persistent infections. Science 1999, 284:1318-1322.
  • [2]Costerton JW: Microbial ecology comes of age and joins the general ecology community. Proc Natl Acad Sci U S A 2004, 49:16983-16984.
  • [3]Fux CA, Costerton JW, Stewart PS, Stoodley P: Survival strategies of infectious biofilms. Trends Microbiol 2005, 13:34-40.
  • [4]Thomassen MJ, Boxerbaum B, Demko CA, Kuchenbrod PJ, Dearborn DG, Wood RE: Inhibitory effect of cystic fibrosis serum on pseudomonas phagocytosis by rabbit and human alveolar macrophages. Pediatr Res 1979, 13:1085-1088.
  • [5]Lang BJ, Arron SD, Ferris SW, Hebert PC, MacDonald NE: Multiple combination bactericidal antibiotic testing for patients with cystic fibrosis infected with multiresistant strains of Pseudomonas aeruginosa. Am J Respir Crit Care Med 2000, 162:2241-2245.
  • [6]Smith EE, Buckley DG, Wu Z, Saenphimmachak C, Hoffman LR, D'Argenio DA, Miller SI, Ramsey BW, Speert DP, Moskowitz SM, Burns JL, Kaul R, Olson MV: Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc Natl Acad Sci U S A 2006, 103:8487-8492.
  • [7]Conibear TC, Collins SL, Webb JS: Role of mutation in Pseudomonas aeruginosa biofilm development. PLoS One 2009, 14:e6289.
  • [8]Cloete TE: Resistance mechanisms of bacteria to antimicrobial compounds. Int Biodeter & Biodegrad 2003, 51:277-282.
  • [9]Mah TC, O’Toole GA: Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol 2001, 9:34-39.
  • [10]Stewart PS, Costerton JW: Antibiotic resistance of bacteria in biofilms. Lancet 2001, 358:135-138.
  • [11]Cheema MS, Rassing JE, Marriot C: The diffusion characteristics of antibiotics in mucus glycoprotein gels. J Pharm Pharmacol 1986, 38:53.
  • [12]Gordon CA, Hodges NA, Marriott C: Antibiotic interaction and diffusion through alginate and exopolysaccharide of cystic fibrosis-derived Pseudomonas aeruginosa. J Antimicrob Chemother 1988, 22:667-674.
  • [13]Anderl JN, Franklin MJ, Stewart PS: Role of antibiotic penetration limitation in Klebsiella pneumoniae biofilm resistance to ampicillin and ciprofloxacin. Antimicrob Agents Chemother 2000, 44:1818-1824.
  • [14]Stewart PS, Rayner J, Roe F, Rees WM: Biofilm penetration and disinfection efficacy of alkaline hypochlorite and chlorosulfamates. J App Microbiol 2001, 91:525-532.
  • [15]Stewart PS: Mechanisms of antibiotic resistance in bacterial biofilms. Int J Med Microbiol 2002, 292:107-113.
  • [16]Lewis K: Persister cells, dormancy and infectious disease. Nature Rev Microbiol 2007, 5:48-56.
  • [17]Dhar N, McKinney D: Microbial phenotypic heterogeneity and antibiotic tolerance. Curr Opinion in Microbiol 2007, 10:30-38.
  • [18]Lewis K: Riddle of biofilm resistance. Antimicrob Agents Chemother 2001, 45:999-1007.
  • [19]Roberts ME, Stewart PS: Modeling protection from antimicrobial agents in biofilms through the formation of persister cells. Microbiol 2005, 151:75-80.
  • [20]Hairston NG Jr, Ellner SP, Geber MA, Yoshida T, Fox JA: Rapid evolution and the convergence of ecological and evolutionary time. Ecol Lett 2005, 8:1114-1127.
  • [21]Nesse RM, Stearns SC: The great opportunity: evolutionary applications to medicine and public health. Evolutionary Applications 2008, 1:28-48.
  • [22]Wrande M, Roth JR, Hughes D: Accumulation of mutants in “ageing” bacterial colonies is due to growth under selection, not stress-induced mutagenesis. Proc Natl Acad Sci U S A 2008, 105:11863-11868.
  • [23]Foweraker JE, Laughton CR, Brown DFJ, Bilton D: Phenotypic variability of Pseudomonas aeruginosa in sputa from patients with acute infective exacerbation of cystic fibrosis and its impact on the validity of antimicrobial susceptibility testing. J Antimicrobl Chemotherapy 2005, 55:921-927.
  • [24]Martínez-Solano L, Macia MD, Fajardo A, Oliver A, Martinez JL: Chronic Pseudomonas aeruginosa infection in chronic obstructive pulmonary disease. Clin Infect Dis 2008, 47:1526-1533.
  • [25]Mena A, Smith EE, Burns JL, Speert DP, Moskowitz SM, Perez JL, Oliver A: Genetic adaptation of Pseudomonas aeruginosa to the airways of cystic fibrosis patients is catalyzed by hypermutation. J Bacteriol 2008, 190:7910-7917.
  • [26]Ponciano JM, La H-J, Joyce P, Forney LJ: Evolution of Diversity in Spatially Structured E. coli populations. Appl Env Microbiol 2009, 75:6047-6054.
  • [27]Allegrucci M, Sauer K: Characterization of colony morphology variants isolated from Streptococcus pneumoniae biofilms. J Bac 2007, 189:2030-2038.
  • [28]Bantinaki E, Kassen R, Knight CG, Robinson Z, Spiers AJ, Rainey PB: Adaptive divergence in experimental populations of Pseudomonas fluorescens. III. Mutational origins of wrinkly spreader diversity. Genetics 2007, 176:441-453.
  • [29]Yarwood JM, Paquette KM, Tikh IB, Volper EM, Greenberg EP: Generation of virulence factor variants in Staphylococcus aureus biofilms. J Bac 2007, 189:7961-7967.
  • [30]Boles BR, Singh PK: Endogenous oxidative stress produces diversity and adaptability in biofilm communities. Proc Natl Acad Sci U S A 2008, 105:12503-12508.
  • [31]Boles BR, Thoendel M, Singh PK: Self-generated diversity produces “insurance effects” in biofilm communities. Proc Natl Acad Sci U S A 2004, 101:16630-16635.
  • [32]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, 42:1223-1232.
  • [33]Yachi S, Loreau M: Biodiversity and ecosystem productivity in a fluctuating environment: the insurance hypothesis. Proc Natl Acad Sci U S A 1999, 96:1463-1468.
  • [34]Ortez JH: Disk diffusion testing. In Manual of Antimicrobial Susceptibility Testing. Edited by Coyle MB. Washington, DC: American Society for Microbiology; 2005.
  • [35]Rosche WA, Foster PL: Determining Mutation Rates in Bacterial Populations. Methods 2000, 20:4-17.
  • [36]Martinez JL, Baquero F: Mutation Frequencies and Antibiotic Resistance. Antimicrob Agents Chemother 2000, 44:1771-1777.
  • [37]Stewart PS, Franklin MJ: Physiological heterogeneity in biofilms. Nat Rev Microbiol 2008, 6:199-210.
  • [38]Stewart PW: Diffusion in biofilms. J Bacteriol 2003, 185:1485-1491.
  • [39]Perez-Osorio AC, Williamson KS, Franklin MJ: Heterogeneous rpoS and rhlR mRNA Levels and 16S rRNA/rDNA (rRNA Gene) Ratios within Pseudomonas aeruginosa Biofilms Sampled by Laser Capture Microdissection. J Bacteriol 2010, 192:2991-3000.
  • [40]Eastman JM, Harmon LJ, La H-J, Joyce P, Forney LJ: The onion model, a simple neutral model for the evolution of diversity in bacterial biofilms. J Evol Biol 2011, 11:2496-2504.
  • [41]Tenaillon O, Toupance B, Le Nagard H, Taddei F, Godelle B: Mutators, population size, adaptive landscape and the adaptation of asexual populations of bacteria. Genetics 1999, 152:485-493.
  • [42]Chang I, Gilbert ES, Eliashberg E, Keasling JD: A three-dimensional, stochastic simulation of biofilm growth and transport-related factors that affect structure. Microbiology 2003, 149:2859-2871.
  • [43]Perfeito L, Fernandes L, Mota C, Gordo I: Adaptive Mutations in Bacteria: High Rate and Small Effects. Science 2007, 317:813-815.
  • [44]Barrick JE, Yu DS, Yoon SH, Jeong H, Oh TK, Schneider D, Lenski RE, Kim FJ: Genome evolution and adaptation in a long-term experiment with Escherichia coli. Nature 2009, 461:1243-1247.
  • [45]Johnson RA, Wichern DW: Applied Multivariate Analysis. New Jersey: Prentice Hall; 2002.
  • [46]Development Core Team R: R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2012. URL http://www.R-project.org webcite
  文献评价指标  
  下载次数:13次 浏览次数:14次