1887

Abstract

DNA adenine methyltransferase () has been well documented for its role in regulation of replication, mismatch repair and transposition. Recent studies have also suggested a role for in protection against antibiotic stress, although this is not yet fully defined. We therefore evaluated the role of in the development of antibiotic resistance and triclosan-associated cross-resistance.

A significant impact on growth rate was seen in the knockout compared to the parental strain. Known triclosan resistance-associated mutations in were seen regardless of status, with an additional mutation in seen in the knockout. The expression of multiple antibiotic resistance-associated genes was significantly different between the parent and knockout post-resistance induction. Reversion rate assays showed that resistance mechanisms were stable.

knockout had a significant effect on growth, but its role in the development of antibiotic resistance is likely confined to those antibiotics using -containing efflux pumps.

Funding
This study was supported by the:
  • Not Applicable , Leeds Beckett University
Loading

Article metrics loading...

/content/journal/acmi/10.1099/acmi.0.000178
2020-11-18
2020-12-01
Loading full text...

Full text loading...

/deliver/fulltext/acmi/10.1099/acmi.0.000178/acmi000178.html?itemId=/content/journal/acmi/10.1099/acmi.0.000178&mimeType=html&fmt=ahah

References

  1. Ni M, Decrulle AL, Fontaine F, Demarez A, Taddei F et al. Pre-disposition and epigenetics govern variation in bacterial survival upon stress. PLoS Genet 2012; 8:e1003148
    [Google Scholar]
  2. Adam M, Murali B, Glenn NO, Potter SS. Epigenetic inheritance based evolution of antibiotic resistance in bacteria. BMC Evol Biol 2008; 8:52
    [Google Scholar]
  3. Robbins-Manke JL, Zdraveski ZZ, Marinus M, Essigmann JM. Analysis of global gene expression and double-strand-break formation in DNA adenine methyltransferase- and mismatch repair-deficient Escherichia coli. J Bacteriol 2005; 187:7027–7037
    [Google Scholar]
  4. Wyrzykowski J, Volkert MR. The Escherichia coli methyl-directed mismatch repair system repairs base pairs containing oxidative lesions. J Bacteriol 2003; 185:1701–1704
    [Google Scholar]
  5. Raghunathan N, Goswami S, Leela JK, Pandiyan A, Gowrishankar J. A new role for Escherichia coli dam DNA methylase in prevention of aberrant chromosomal replication. Nucleic Acids Res 2019; 47:5698–5711
    [Google Scholar]
  6. Messer W, Bellekes U, Lother H. Effect of dam methylation on the activity of the E. coli replication origin, oriC. Embo J 1985; 4:1327–1332
    [Google Scholar]
  7. Roberts D, Hoopes BC, McClure WR, Kleckner N. IS10 transposition is regulated by DNA adenine methylation. Cell 1985; 43:117–130
    [Google Scholar]
  8. Yin JC, Krebs MP, Reznikoff WS. Effect of dam methylation on Tn5 transposition. J Mol Biol 1988; 199:35–45
    [Google Scholar]
  9. Westphal LL, Sauvey P, Champion MM, Ehrenreich IM, Finkel SE. Genomewide dam methylation in Escherichia coli during long-term stationary phase. mSystems 2016; 1: [CrossRef]
    [Google Scholar]
  10. Cohen NR, Ross CA, Jain S, Shapiro RS, Gutierrez A et al. A role for the bacterial GATC methylome in antibiotic stress survival. Nat Genet 2016; 48:581–586
    [Google Scholar]
  11. X-Z L, Nikaido H. Antimicrobial drug efflux pumps in Escherichia coli. In X-Z Li, Elkins CA, Zgurskaya HI. (editors) Efflux-Mediated Antimicrobial Resistance in Bacteria: Mechanisms, Regulation and Clinical Implications Cham: Springer International Publishing; 2016 pp 219–259
    [Google Scholar]
  12. Casadesús J, Low D. Epigenetic gene regulation in the bacterial world. Microbiol Mol Biol Rev 2006; 70:830–856
    [Google Scholar]
  13. Motta SS, Cluzel P, Aldana M. Adaptive resistance in bacteria requires epigenetic inheritance, genetic noise, and cost of efflux pumps. PLoS One 2015; 10:e0118464
    [Google Scholar]
  14. Low DA, Weyand NJ, Mahan MJ. Roles of DNA adenine methylation in regulating bacterial gene expression and virulence. Infect Immun 2001; 69:7197–7204
    [Google Scholar]
  15. Food and Drug Adminnistration, HHS Safety and effectiveness of consumer antiseptics; topical antimicrobial drug products for over-the-counter human use. FInal rule. Fed Regist 2016; 81:61106–61130[PubMed]
    [Google Scholar]
  16. Triclosan and Antibiotics resistance What is the biocide triclosan?. Internet. [cited 2019 Feb 6] http://ec.europa.eu/health/scientific_committees/opinions_layman/triclosan/en/l-3/1-biocides.htm
    [Google Scholar]
  17. Braoudaki M, Hilton AC. Adaptive resistance to biocides in Salmonella enterica and Escherichia coli O157 and cross-resistance to antimicrobial agents. J Clin Microbiol 2004; 42:73–78
    [Google Scholar]
  18. Carey DE, McNamara PJ. The impact of triclosan on the spread of antibiotic resistance in the environment. Front Microbiol 2014; 5:780
    [Google Scholar]
  19. Alfhili MA, Lee M-H. Triclosan: an update on biochemical and molecular mechanisms. Oxid Med Cell Longev 2019
    [Google Scholar]
  20. Karatzas KAG, Webber MA, Jorgensen F, Woodward MJ, Piddock LJV et al. Prolonged treatment of Salmonella enterica serovar Typhimurium with commercial disinfectants selects for multiple antibiotic resistance, increased efflux and reduced invasiveness. J Antimicrob Chemother 2007; 60:947–955
    [Google Scholar]
  21. Birošová L, Mikulášová M. Development of triclosan and antibiotic resistance in Salmonella enterica serovar Typhimurium. J Med Microbiol 2009; 58:436–441
    [Google Scholar]
  22. Hernández A, Ruiz FM, Romero A, Martínez JL. The binding of triclosan to SmeT, the repressor of the multidrug efflux pump SmeDEF, induces antibiotic resistance in Stenotrophomonas maltophilia. PLoS Pathog 2011; 7:e1002103
    [Google Scholar]
  23. Chuanchuen R, Beinlich K, Hoang TT, Becher A, Karkhoff-Schweizer RR et al. Cross-Resistance between triclosan and antibiotics in Pseudomonas aeruginosa is mediated by multidrug efflux pumps: exposure of a susceptible mutant strain to triclosan selects nfxB mutants overexpressing MexCD-OprJ. Antimicrob Agents Chemother 2001; 45:428–432
    [Google Scholar]
  24. Brown DFJ, Wootton M, Howe RA. Antimicrobial susceptibility testing breakpoints and methods from BSAC to EUCAST. J Antimicrob Chemother 2016; 71:3–5
    [Google Scholar]
  25. Andersen CL, Jensen JL, Ørntoft TF. Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res 2004; 64:5245–5250
    [Google Scholar]
  26. Wattam AR, Abraham D, Dalay O, Disz TL, Driscoll T et al. PATRIC, the bacterial bioinformatics database and analysis resource. Nucleic Acids Res 2014; 42:D581–591
    [Google Scholar]
  27. Kossykh VG, Lloyd RS. A DNA adenine methyltransferase of Escherichia coli that is cell cycle regulated and essential for viability. J Bacteriol 2004; 186:2061–2067
    [Google Scholar]
  28. Løbner-Olesen A, Skovgaard O, Marinus MG. Dam methylation: coordinating cellular processes. Curr Opin Microbiol 2005; 8:154–160
    [Google Scholar]
  29. Singh NJ, Shin D, Lee HM, Kim HT, Chang H-J et al. Structural basis of triclosan resistance. J Struct Biol 2011; 174:173–179
    [Google Scholar]
  30. Khan R, Roy N, Choi K, Lee S-W. Distribution of triclosan-resistant genes in major pathogenic microorganisms revealed by metagenome and genome-wide analysis. PLoS One 2018; 13:e0192277
    [Google Scholar]
  31. Rosenberg EY, Ma D, Nikaido H. Acrd of Escherichia coli is an aminoglycoside efflux pump. J Bacteriol 2000; 182:1754–1756
    [Google Scholar]
  32. Marinus MG, Løbner-Olesen A. DNA methylation. EcoSal Plus 2014; 6: [CrossRef][PubMed]
    [Google Scholar]
  33. Reisenauer A, Kahng LS, McCollum S, Shapiro L. Bacterial DNA methylation: a cell cycle regulator?. J Bacteriol 1999; 181:5135–5139
    [Google Scholar]
  34. Stephenson SA-M, Brown PD. Epigenetic influence of dam methylation on gene expression and attachment in uropathogenic Escherichia coli. Front Public Health 2016; 4:131
    [Google Scholar]
  35. Huang Y-M, Kan B, Lu Y, Szeto S. The effect of osmotic shock on rpoS expression and antibiotic resistance in Escherichia coli. Journal of Experimental Microbiology and Immunology 2009; 13:13–17
    [Google Scholar]
  36. Dougherty TJ, Pucci MJ. Penicillin-Binding proteins are regulated by rpoS during transitions in growth states of Escherichia coli. Antimicrob Agents Chemother 1994; 38:205–210
    [Google Scholar]
  37. Gutierrez A, Laureti L, Crussard S, Abida H, Rodríguez-Rojas A et al. β-Lactam antibiotics promote bacterial mutagenesis via an RpoS-mediated reduction in replication fidelity. Nat Commun 2013; 4:1610
    [Google Scholar]
  38. Murakami K, Ono T, Viducic D, Kayama S, Mori M et al. Role for rpoS gene of Pseudomonas aeruginosa in antibiotic tolerance. FEMS Microbiol Lett 2005; 242:161–167
    [Google Scholar]
  39. Merrikh H, Ferrazzoli AE, Bougdour A, Olivier-Mason A, Lovett ST. A DNA damage response in Escherichia coli involving the alternative sigma factor, rpoS. Proc Natl Acad Sci U S A 2009; 106:611–616
    [Google Scholar]
  40. Baharoglu Z, Krin E, Mazel D. Rpos plays a central role in the SOS induction by sub-lethal aminoglycoside concentrations in Vibrio cholerae. PLoS Genet 2013; 9:e1003421
    [Google Scholar]
  41. Worthington RJ, Melander C. Combination approaches to combat multidrug-resistant bacteria. Trends Biotechnol 2013; 31:177–184
    [Google Scholar]
  42. Nishino K, Honda T, Yamaguchi A. Genome-wide analyses of Escherichia coli gene expression responsive to the BaeSR two-component regulatory system. J Bacteriol 2005; 187:1763–1772
    [Google Scholar]
  43. Sköld O. Sulfonamide resistance: mechanisms and trends. Drug Resist Updat 2000; 3:155–160
    [Google Scholar]
  44. Huovinen P. Resistance to trimethoprim-sulfamethoxazole. Clin Infect Dis 2001; 32:1608–1614
    [Google Scholar]
  45. Choi Y, Sims GE, Murphy S, Miller JR, Chan AP. Predicting the functional effect of amino acid substitutions and indels. PLoS One. 2012; 7:e46688
    [Google Scholar]
  46. Hart BR, Mishra PK, Lintner RE, Hinerman JM, Herr AB et al. Recognition of DNA by the helix-turn-helix global regulatory protein LRP is modulated by the amino terminus. J Bacteriol 2011; 193:3794–3803
    [Google Scholar]
  47. Escalada MG, Harwood JL, Maillard J-Y, Ochs D. Triclosan inhibition of fatty acid synthesis and its effect on growth of Escherichia coli and Pseudomonas aeruginosa. J Antimicrob Chemother 2005; 55:879–882
    [Google Scholar]
  48. Molshanski-Mor S, Yosef I, Kiro R, Edgar R, Manor M et al. Revealing bacterial targets of growth inhibitors encoded by bacteriophage T7. Proc Natl Acad Sci U S A 2014; 111:18715–18720
    [Google Scholar]
  49. RegulonDB fabI operon and associated TUs in Escherichia coli K-12 genome. [Internet]. [cited 2020 Jan 28] http://regulondb.ccg.unam.mx/operon?term=ECK120029041&organism=ECK12&format=jsp&type=operon
    [Google Scholar]
  50. My L, Ghandour Achkar N, Viala JP, Bouveret E. Reassessment of the genetic regulation of fatty acid synthesis in Escherichia coli: global positive control by the dual functional regulator FadR. J Bacteriol 2015; 197:1862–1872
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/acmi/10.1099/acmi.0.000178
Loading
/content/journal/acmi/10.1099/acmi.0.000178
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error