Water Disinfection Byproducts Induce Antibiotic Resistance-Role of Environmental Pollutants in Resistance Phenomena

Environmental Science and Technology

Volumn 50, Issue 6, 2016, Pages 3193-3201

  Li, Dan ^a,b,c   Zeng, Siyu ^b   He, Miao ^a   Gu, April Z ^b  

^a TSINGHUA UNIVERSITY   (China)

^b Northeastern University   (United States)

^c FUDAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTICS; BYPRODUCTS; DISINFECTION; ESCHERICHIA COLI; GENES; HEALTH RISKS; POLLUTION;

ANTIBIOTICS RESISTANCE; DISINFECTION BY-PRODUCT; ENVIRONMENTAL CONTAMINANT; ENVIRONMENTAL POLLUTANTS; EXPOSURE CONCENTRATION; MINIMAL INHIBITORY CONCENTRATION; WATER DISINFECTION BYPRODUCTS; WHOLE GENOME ANALYSIS;

WATER POLLUTION;

ANTIBIOTIC AGENT; IODOACETIC ACID; WATER; CHLORIDE; CHLORITE; DISINFECTANT AGENT; TRICHLOROACETIC ACID;

ANTIBIOTIC RESISTANCE; BACTERIUM; CHEMICAL POLLUTANT; CONCENTRATION (COMPOSITION); DISINFECTION; DRUG; EVOLUTION; INHIBITOR; MUTUALISM; PUBLIC HEALTH; SPECIATION (BIOLOGY);

ANTIBIOTIC RESISTANCE; ARTICLE; CONTROLLED STUDY; DISINFECTION; DNA REPAIR; ESCHERICHIA COLI; EVOLUTION; GENE MUTATION; GENOME ANALYSIS; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; OXIDATIVE STRESS; POLLUTANT; WATER DISINFECTION; CHEMISTRY; DRUG EFFECTS; GENETICS; MICROBIAL SENSITIVITY TEST; PHARMACOLOGY; PROCEDURES;

CHLORIDES; DISINFECTANTS; DISINFECTION; DRUG RESISTANCE, BACTERIAL; DRUG RESISTANCE, MICROBIAL; ENVIRONMENTAL POLLUTANTS; ESCHERICHIA COLI; IODOACETIC ACID; MICROBIAL SENSITIVITY TESTS; TRICHLOROACETIC ACID;

EID: 84961847708     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/acs.est.5b05113     Document Type: Article

References (49)

1. Taubes, G. The bacteria fight back Science 2008, 321, 356-361 10.1126/science.321.5887.356
2. Witte, W. Medical consequences of antibiotic use in agriculture Science 1998, 279, 996-997 10.1126/science.279.5353.996
3. Zhu, Y. G.; Johnson, T. A.; Su, J. Q.; Qiao, M.; Guo, G. X.; Stedtfeld, R. D.; Hashsham, S. A.; Tiedje, J. M. Diverse and abundant antibiotic resistance genes in Chinese swine farms Proc. Natl. Acad. Sci. U. S. A. 2013, 110, 3435-3440 10.1073/pnas.1222743110
4. Wright, G. D. Antibiotic resistance in the environment: a link to the clinic? Curr. Opin. Microbiol. 2010, 13, 589-594 10.1016/j.mib.2010.08.005
5. Andersson, D. I.; Hughes, D. Microbiological effects of sublethal levels of antibiotics Nat. Rev. Microbiol. 2014, 12, 465-478 10.1038/nrmicro3270
6. Kohanski, M. A.; DePristo, M. A.; Collins, J. J. Sublethal antibiotic treatment leads to multidrug resistance via radical-Induced mutagenesis Mol. Cell 2010, 37, 311-320 10.1016/j.molcel.2010.01.003
7. Gullberg, E.; Cao, S.; Berg, O. G.; Ilbäck, C.; Sandegren, L.; Hughes, D.; Andersson, D. I. Selection of resistant bacteria at very low antibiotic concentrations PLoS Pathog. 2011, 7 (7) e1002158 10.1371/journal.ppat.1002158
8. Gutierrez, A.; Laureti, L.; Crussard, S.; Abida, H.; Rodríguez-Rojas, A.; Blázquez, J.; Baharoglu, Z.; Mazel, D.; Darfeuille, F.; Vogel, J.; Matic, I. beta-lactam antibiotics promote bacterial mutagenesis via an RpoS-mediated reduction in replication fidelity Nat. Commun. 2013, 4, 1610 10.1038/ncomms2607
9. Kummerer, K. Antibiotics in the aquatic environment-A review-Part I Chemosphere 2009, 75, 417-434 10.1016/j.chemosphere.2008.11.086
10. Senta, I.; Terzic, S.; Ahel, M. Occurrence and fate of dissolved and particulate antimicrobials in municipal wastewater treatment Water Res. 2013, 47 (2) 705-714 10.1016/j.watres.2012.10.041
11. Miller, C.; Thomsen, L. E.; Gaggero, C.; Mosseri, R.; Ingmer, H.; Cohen, S. N. SOS response induction by beta-lactams and bacterial defense against antibiotic lethality Science 2004, 305 (5690) 1629-1631 10.1126/science.1101630
12. Baker-Austin, C.; Wright, M. S.; Stepanauskas, R.; McArthur, J. V. Co-selection of antibiotic and metal resistance Trends Microbiol. 2006, 14 (4) 176-182 10.1016/j.tim.2006.02.006
13. Berg, J.; Thorsen, M. K.; Holm, P. E.; Jensen, J.; Nybroe, O.; Brandt, K. K. Cu exposure under field conditions co-selects for antibiotic resistance as determined by a novel cultivation-independent bacterial community tolerance assay Environ. Sci. Technol. 2010, 44 (22) 8724-8728 10.1021/es101798r
14. Chapman, J. S. Disinfectant resistance mechanisms, cross-resistance, and co-resistance Int. Biodeterior. Biodegrad. 2003, 51, 271-276 10.1016/S0964-8305(03)00044-1
15. Bouzada, M. L.; Silva, V. L.; Moreira, F. A.; Silva, G. A.; Diniz, C. G. Antimicrobial resistance and disinfectants susceptibility of persistent bacteria in a tertiary care hospital J. Microbiol. Antimicrob. 2010, 2, 105-112
16. Richardson, S. D.; Plewa, M. J.; Wagner, E. D.; Schoeny, R.; Demarini, D. M. Occurrence, genotoxicity, and carcinogenicity of regulated and emerging disinfection by-products in drinking water: a review and roadmap for research Mutat. Res., Rev. Mutat. Res. 2007, 636 (1-3) 178-242 10.1016/j.mrrev.2007.09.001
17. Chowdhury, S.; Alhooshani, K.; Karanfil, T. Disinfection byproducts in swimming pool: occurrences, implications and future needs Water Res. 2014, 53, 68-109 10.1016/j.watres.2014.01.017
18. Nieuwenhuijsen, M. J.; Martinez, D.; Grellier, J.; Bennett, J.; Best, N.; Iszatt, N.; Vrijheid, M.; Toledano, M. B. Chlorination disinfection by-products in drinking water and congenital anomalies: review and meta-analyses Environ. Health. Persp. 2009, 117 (10) 1486-1493 10.1289/ehp.0900677
19. Guilherme, S.; Rodriguez, M. J. Occurrence of regulated and non-regulated disinfection by-products in small drinking water systems Chemosphere 2014, 117, 425-432 10.1016/j.chemosphere.2014.08.002
20. Ye, Z.; Weinberg, H. S.; Meyer, M. T. Trace analysis of trimethoprim and sulfonamide, macrolide, quinolone, and tetracycline antibiotics in chlorinated drinking water using liquid chromatography electrospray tandem mass spectrometry Anal. Chem. 2007, 79 (3) 1135-1144 10.1021/ac060972a
21. Watkinson, A. J.; Murby, E. J.; Kolpin, D. W.; Costanzo, S. D. The occurrence of antibiotics in an urban watershed: from wastewater to drinking water Sci. Total Environ. 2009, 407 (8) 2711-2723 10.1016/j.scitotenv.2008.11.059
22. Lv, L.; Jiang, T.; Zhang, S. H.; Yu, X. Exposure to mutagenic disinfection byproducts leads to increase of antibiotic resistance in Pseudomonas aeruginosa Environ. Sci. Technol. 2014, 48 (14) 8188-8195 10.1021/es501646n
23. Toprak, E.; Veres, A.; Michel, J. B.; Chait, R.; Hartl, D. L.; Kishony, R. Evolutionary paths to antibiotic resistance under dynamically sustained drug selection Nat. Genet. 2011, 44 (1) 101-105 10.1038/ng.1034
24. Zhang, Q.; Lambert, G.; Liao, D.; Kim, H.; Robin, K.; Tung, C. K.; Pourmand, N.; Austin, R. H. Acceleration of emergence of bacterial antibiotic resistance in connected microenvironments Science 2011, 333 (6050) 1764-1767 10.1126/science.1208747
25. th ed.; World Health Organization: Geneva, 2011; ISBN 9789241548151.
26. Clinical and laboratory standards institute (CLSI). Performance standards for antimicrobial susceptibility testing; Institute antimicrobial susceptibility testing standards M02-A11 and M07-A9. Clinical and Laboratory Standards Institute: Wayne, PA, 2012.
27. Anfora, A. T.; Welch, R. A. DsdX is the second D-serine transporter in uropathogenic Escherichia coli clinical isolate CFT073 J. Bacteriol. 2006, 188 (18) 6622-6628 10.1128/JB.00634-06
28. Baker, K. R.; Postle, K. Mutations in Escherichia coli exbB transmembrane domains identify scaffolding and signal transduction functions and exclude participation in a proton pathway J. Bacteriol. 2013, 195 (12) 2898-2911 10.1128/JB.00017-13
29. Westenberg, D. J.; Gunsalus, R. P.; Ackrell, B. A. C.; Sices, H.; Cecchini, G. Escherichia coli fumarate reductase frdC and frdD mutants-Identification of amino-acid-residues involved in catalytic activity with quinones J. Biol. Chem. 1993, 268 (2) 815-822
30. Chen, L. Y. Glycerol modulates water permeation through Escherichia coli aquaglyceroporin GlpF Biochim. Biophys. Acta, Biomembr. 2013, 1828, 1786-1793 10.1016/j.bbamem.2013.03.008
31. Liu, Y.; Ho, K. K.; Su, J.; Gong, H.; Chang, A. C.; Lu, S. Potassium transport of Salmonella is important for type III secretion and pathogenesis Microbiology 2013, 159 (8) 1705-1719 10.1099/mic.0.068700-0
32. Justino, M. C.; Vicente, J. B.; Teixeira, M.; Saraiva, L. M. New genes implicated in the protection of anaerobically grown Escherichia coli against nitric oxide J. Biol. Chem. 2005, 280 (4) 2636-2643 10.1074/jbc.M411070200
33. Ruiz, J. Mechanisms of resistance to quinolones: target alterations, decreased accumulation and DNA gyrase protection J. Antimicrob. Chemoth. 2003, 51 (5) 1109-1117 10.1093/jac/dkg222
34. Lee, D. H.; Palsson, B. O. Adaptive evolution of Escherichia coli K-12 MG1655 during growth on a nonnative carbon source, L-1, 2-Propanediol Appl. Environ. Microb. 2010, 76 (13) 6327-6327 10.1128/AEM.01776-10
35. Blomfield, I. C.; Mcclain, M. S.; Princ, J. A.; Calie, P. J.; Eisenstein, B. I. Type-1 fimbriation and fime mutants of Escherichia coli K-12 J. Bacteriol. 1991, 173 (17) 5298-5307
36. Bryskier, A. Fluoroquinolones: mechanisms of action and resistance Int. J. Antimicrob. Agents 1993, 2, 151-83 10.1016/0924-8579(93)90052-7
37. Wong, F. C.; Beuning, P. J.; Nagan, M.; Shiba, K.; Musier-Forsyth, K. Functional role of the prokaryotic proline-tRNA synthetase insertion domain in amino acid editing Biochemistry 2002, 41 (22) 7108-7115 10.1021/bi012178j
38. Herman, J. D.; Rice, D. P.; Ribacke, U.; Silterra, J.; Deik, A. A.; Moss, E. L.; Broadbent, K. M.; Neafsey, D. E.; Desai, M. M.; Clish, C. B.; Mazitschek, R.; Wirth, D. F. A genomic and evolutionary approach reveals non-genetic drug resistance in malaria Genome Biol. 2014, 15 (11) 511 10.1186/s13059-014-0511-2
39. Montgomery, J. I.; Smith, J. F.; Tomaras, A. P.; Zaniewski, R.; McPherson, C. J.; McAllister, L. A.; Hartman-Neumann, S.; Arcari, J. T.; Lescoe, M.; Gutierrez, J.; Yuan, Y.; Limberakis, C.; Miller, A. A. Discovery and characterization of a novel class of pyrazolopyrimidinedione tRNA synthesis inhibitors J. Antibiot. 2015, 68, 361 10.1038/ja.2014.163
40. Nilsson, A. I.; Berg, O. G.; Aspevall, O.; Kahlmeter, G.; Andersson, D. I. Biological costs and mechanisms of fosfomycin resistance in Escherichia coli Antimicrob. Agents Chemother. 2003, 47 (9) 2850-2858 10.1128/AAC.47.9.2850-2858.2003
41. Alekshun, M. N.; Levy, S. B. The mar regulon: multiple resistance to antibiotics and other toxic chemicals Trends Microbiol. 1999, 7 (10) 410-413 10.1016/S0966-842X(99)01589-9
42. Pradel, N.; Delmas, J.; Wu, L. F.; Santini, C. L.; Bonnet, R. Sec- and Tat-dependent translocation of beta-Lactamases across the Escherichia coli inner membrane Antimicrob. Agents Chemother. 2009, 53 (1) 242-248 10.1128/AAC.00642-08
43. Degnan, P. H.; Ochman, H.; Moran, N. A. Sequence conservation and functional constraint on intergenic spacers in reduced genomes of the obligate symbiont buchnera PLoS Genet. 2011, 7 (9) e1002252 (2011). 10.1371/journal.pgen.1002252
44. Hughes, D.; Andersson, D. I. Selection of resistance at lethal and non-lethal antibiotic concentrations Curr. Opin. Microbiol. 2012, 15 (5) 555-560 10.1016/j.mib.2012.07.005
45. Onnis-Hayden, A.; Weng, H.; He, M.; Hansen, S.; Ilyin, V.; Lewis, K.; Gu, A. Z. Prokaryotic real-time gene expression profiling for toxicity assessment Environ. Sci. Technol. 2009, 43 (12) 4574-4581 10.1021/es803227z
46. Gou, N.; Gu, A. Z. A new transcriptional effect level index (TELI) for toxicogenomics-based toxicity assessment Environ. Sci. Technol. 2011, 45 (12) 5410-5417 10.1021/es200455p
47. Tang, H. L.; Ristau, R. J.; Xie, Y. F. Disinfection By-Products in Swimming Pool Water: Formation, Modeling, and Control ACS Symp. Ser. 2015, 1190, 381-403 10.1021/bk-2015-1190.ch020
48. Richardson, S. D.; Fasano, F.; Ellington, J. J.; Crumley, F. G.; Buettner, K. M.; Evans, J. J.; Blount, B. C.; Silva, L. K.; Waite, T. J.; Luther, G. W.; Mckague, A. B.; Miltner, R. J.; Wagner, E. D.; Plewa, M. J. Occurrence and mammalian cell toxicity of iodinated disinfection byproducts in drinking water Environ. Sci. Technol. 2008, 42 (22) 8330-8338 10.1021/es801169k
49. Lv, L.; Yu, X.; Xu, Q.; Ye, C. Induction of bacterial antibiotic resistance by mutagenic halogenated nitrogenous disinfection byproducts Environ. Pollut. 2015, 205, 291-298 10.1016/j.envpol.2015.06.026