Development of antibiotic resistance genes in microbial communities during long-term operation of anaerobic reactors in the treatment of pharmaceutical wastewater

Water Research

Volumn 83, Issue , 2015, Pages 337-344

  Aydin, Sevcan ^a   Ince, Bahar ^b   Ince, Orhan ^a  

^a ISTANBUL TECHNICAL UNIVERSITY   (Turkey)

^b BOGAZICI UNIVERSITY   (Turkey)

Author keywords

Anaerobic treatment; Antibiotic resistance; Antibiotics; Illumina sequencing; Real time PCR; Wastewater treatment

Indexed keywords

ANTIBIOTICS; BATCH REACTORS; BIOLOGICAL WATER TREATMENT; EFFLUENTS; GENE EXPRESSION; MICROORGANISMS; POLYMERASE CHAIN REACTION;

ANAEROBIC REACTOR; ANEROBIC TREATMENT; ANTIBIOTIC RESISTANCE GENES; ANTIBIOTICS RESISTANCE; ILLUMEN SEQUENCING; ILLUMINA; MICROBIAL COMMUNITIES; PHARMACEUTICAL WASTEWATER; REAL-TIME PCR; SULFAMETHOXAZOLE;

WASTEWATER TREATMENT;

ERYTHROMYCIN; SULFAMETHOXAZOLE; TETRACYCLINE; ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; WASTE WATER;

ANOXIC CONDITIONS; ANTIBIOTIC RESISTANCE; BIOREACTOR; CHEMICAL OXYGEN DEMAND; DRUG; ENZYME ACTIVITY; GENE EXPRESSION; LONG-TERM CHANGE; MICROBIAL COMMUNITY; POLLUTANT REMOVAL; POLYMERASE CHAIN REACTION; PROTEIN; SEWAGE TREATMENT; WASTEWATER; WATER TREATMENT;

ANAEROBIC REACTOR; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; CONTROLLED STUDY; GENE INACTIVATION; HORIZONTAL GENE TRANSFER; INTEGRON; MICROBIAL COMMUNITY; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SEQUENCING BATCH REACTOR; SLUDGE; WASTE COMPONENT REMOVAL; WASTE WATER MANAGEMENT; BIOREACTOR; ENVIRONMENTAL MONITORING; MICROBIOLOGY; SEWAGE; WASTE WATER;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; BIOREACTORS; DRUG RESISTANCE, MICROBIAL; ENVIRONMENTAL MONITORING; ERYTHROMYCIN; REAL-TIME POLYMERASE CHAIN REACTION; SULFAMETHOXAZOLE; TETRACYCLINE; TETRACYCLINE RESISTANCE; WASTE DISPOSAL, FLUID; WASTE WATER;

EID: 84936989510     PISSN: 00431354     EISSN: 18792448     Source Type: Journal    
DOI: 10.1016/j.watres.2015.07.007     Document Type: Article

References (37)

1. Amin M.M., Zilles J.L., Greiner J., Charbonneau S., Raskin L., Morgenroth E. Influence of the antibiotic erythromycin on anaerobic treatment of a pharmaceutical wastewater. Environ. Sci. Technol. 2006, 40(12):3971-3977.
2. Andersson D.I., Hughes D. Evolution of antibiotic resistance at non-lethal drug concentrations. Drug Resist. Updat. 2012, 15(3):162-172.
3. Antunes P., Machado J., Sousa J.C., Peixe L. Dissemination of sulfonamide resistance genes (sul1, sul2, and sul3) in portuguese salmonella enterica strains and relation with integrons. Antimicrob. Agents Chemother. 2005, 49(2):836-839.
4. Aydin S., Cetecioglu Z., Arikan O., Ince B., Ozbayram E.G., Ince O. Inhibitory effects of antibiotic combinations on syntrophic bacteria, homoacetogens and methanogens. Chemosphere 2015, 120:515-520.
5. Aydin S., Ince B., Cetecioglu Z., Ozbayram E.G., Shahi A., Ince O. Combined effect of erythromycin, tetracycline and sulfamethoxazole on performance of anaerobic sequencing batch reactors. Bioresour. Technol. 2015, 186:207-214.
6. Aydin S., Ince B., Cetecioglu Z., Ozbayram E.G., Shahi A., Okay O., Ince O. Performance of anaerobic sequencing batch reactor in the treatment of pharmaceutical wastewater containing erythromycin and sulfamethoxazole mixture. Water Sci. Technol. 2014, 70(10):1625-1632.
7. Aydin S., Ince B., Ince O. Application of real-time PCR to determination of combined effect of antibiotics on bacteria, methanogenic archaea, archaea in anaerobic sequencing batch reactors. Water Res. 2015, 76:88-98.
8. Baharoglu Z., Mazel D. Vibrio cholerae triggers SOS and mutagenesis in response to a wide range of antibiotics: a route towards multiresistance. Antimicrob. Agents Chemother. 2011, 55(5):2438-2441.
9. 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(4):e1003421.
10. Beaber J.W., Hochhut B., Waldor M.K. SOS response promotes horizontal dissemination of antibiotic resistance genes. Nature 2004, 427(6969):72-74.
11. Birošová L., Mackuľak T., Bodík I., Ryba J., Škubák J., Grabic R. Pilot study of seasonal occurrence and distribution of antibiotics and drug resistant bacteria in wastewater treatment plants in Slovakia. Sci. Total Environ. 2014, 490:440-444.
12. Blahna M.T., Zalewski C.A., Reuer J., Kahlmeter G., Foxman B., Marrs C.F. The role of horizontal gene transfer in the spread of trimethoprim-sulfamethoxazole resistance among uropathogenic Escherichia coli in Europe and Canada. J. Antimicrob. Chemother. 2006, 57(4):666-672.
13. Chelliapan S., Wilby T., Sallis P.J. Performance of an up-flow anaerobic stage reactor (UASR) in the treatment of pharmaceutical wastewater containing macrolide antibiotics. Water Res. 2006, 40:507-516.
14. Faria C., Vaz-Moreira I., Serapicos E., Nunes O.C., Manaia C.M. Antibiotic resistance in coagulase negative staphylococci isolated from wastewater and drinking water. Sci. Total Environ. 2009, 407(12):3876-3882.
15. Frank T., Gautier V., Talarmin A., Bercion R., Arlet G. Characterization of sulphonamide resistance genes and class 1 integron gene cassettes in Enterobacteriaceae, Central African Republic (CAR). J. Antimicrob. Chemother. 2007, 59(4):742-745.
16. Gao P., Mao D., Luo Y., Wang L., Xu B., Xu L. Occurrence of sulfonamide and tetracycline-resistant bacteria and resistance genes in aquaculture environment. Water Res. 2012, 46(7):2355-2364.
17. Henderson-Begg S.K., Livermore D.M., Hall L.M. Effect of subinhibitory concentrations of antibiotics on mutation frequency in Streptococcus pneumoniae. J. Antimicrob. Chemother. 2006, 57(5):849-854.
18. Kohanski M.A., DePristo M.A., Collins J.J. Sublethal antibiotic treatment leads to multidrug resistance via radical-induced mutagenesis. Mol. Cell. 2010, 37(3):311-320.
19. Kümmerer K. Antibiotics in the aquatic environment-a review-part I. Chemosphere 2009, 75(4):417-434.
20. Larsson D.J., de Pedro C., Paxeus N. Effluent from drug manufactures contains extremely high levels of pharmaceuticals. J. Hazard. Mater. 2007, 148(3):751-755.
21. Liu L., Liu Y.H., Wang Z., Liu C.X., Huang X., Zhu G.F. Behavior of tetracycline and sulfamethazine with corresponding resistance genes from swine wastewater in pilot-scale constructed wetlands. J. Hazard. Mater. 2014, 278:304-310.
22. Mao E.F., Lane L., Lee J., Miller J.H. Proliferation of mutators in a cell population. J. Bacteriol. 1997, 179(2):417-422.
23. Munir M., Wong K., Xagoraraki I. Release of antibiotic resistant bacteria and genes in the effluent and biosolids of five wastewater utilities in Michigan. Water Res. 2011, 45(2):681-693.
24. Nakajima Y. Mechanisms of bacterial resistance to macrolide antibiotics. J. Infect. Chemother. 1999, 5(2):61-74.
25. Oktem Y.A., Ince O., Sallis P., Donnelly T., Ince B.K. Anaerobic treatment of a chemical synthesis-based pharmaceutical wastewater in a hybrid upflow anaerobic sludge blanket reactor. Bioresour. Technol. 2008, 99:1089-1096.
26. Pei R., Kim S.C., Carlson K.H., Pruden A. Effect of river landscape on the sediment concentrations of antibiotics and corresponding antibiotic resistance genes (ARG). Water Res. 2006, 40(12):2427-2435.
27. Pruden A., Pei R., Storteboom H., Carlson K.H. Antibiotic resistance genes as emerging contaminants: studies in northern Colorado. Environ. Sci. Technol. 2006, 40(23):7445-7450.
28. Rizzo L., Manaia C., Merlin C., Schwartz T., Dagot C., Ploy M.C., Fatta-Kassinos D. Urban wastewater treatment plants as hotspots for antibiotic resistant bacteria and genes spread into the environment: a review. Sci. Total Environ. 2013, 447:345-360.
29. Szczepanowski R., Linke B., Krahn I., Gartemann K.H., Gützkow T., Eichler W., Schlüter A. Detection of 140 clinically relevant antibiotic-resistance genes in the plasmid metagenome of wastewater treatment plant bacteria showing reduced susceptibility to selected antibiotics. Microbiology 2009, 155(7):2306-2319.
30. Thi T.D., López E., Rodríguez-Rojas A., Rodríguez-Beltrán J., Couce A., Guelfo J.R., Blázquez J. Effect of recA inactivation on mutagenesis of Escherichia coli exposed to sublethal concentrations of antimicrobials. J. Antimicrob. Chemother. 2011, 66(3):531-538.
31. Úbeda C., Maiques E., Knecht E., Lasa Í., Novick R.P., Penadés J.R. Antibiotic-induced SOS response promotes horizontal dissemination of pathogenicity island-encoded virulence factors in staphylococci. Mol. Microbiol. 2005, 56(3):836-844.
32. 2O. Appl. Microbiol. Biotechnol. 2014, 98(6):2667-2673.
33. Wright G.D. Bacterial resistance to antibiotics: enzymatic degradation and modification. Adv. drug Deliv. Rev. 2005, 57(10):1451-1470.
34. Yang Y., Li B., Ju F., Zhang T. Exploring variation of antibiotic resistance genes in activated sludge over a four-year period through a metagenomic approach. Environ. Sci. Technol. 2013, 47(18):10197-10205.
35. Yu Z., Michel F.C., Hansen G., Wittum T., Morrison M. Development and application of real-time PCR assays for quantification of genes encoding tetracycline resistance. Appl. Environ. Microbiol. 2005, 71(11):6926-6933.
36. Zhang T., Zhang M., Zhang X., Fang H.H. Tetracycline resistance genes and tetracycline resistant lactose-fermenting Enterobacteriaceae in activated sludge of sewage treatment plants. Environ. Sci. Technol. 2009, 43(10):3455-3460.
37. Zhang W., Huang M.H., Qi F.F., Sun P.Z., Van Ginkel S.W. Effect of trace tetracycline concentrations on the structure of a microbial community and the development of tetracycline resistance genes in sequencing batch reactors. Bioresour. Technol. 2013, 150:9-14.