Metagenomic insights into ultraviolet disinfection effects on antibiotic resistome in biologically treated wastewater

Water Research

Volumn 101, Issue , 2016, Pages 309-317

  Hu, Qing ^a   Zhang, Xu Xiang ^a   Jia, Shuyu ^a   Huang, Kailong ^a   Tang, Junying ^a   Shi, Peng ^a   Ye, Lin ^a   Ren, Hongqiang ^a  

^a NANJING UNIVERSITY   (China)

Author keywords

Antibiotic resistance; High throughput sequencing; Metagenomics; Microbial community; Mobile genetic elements; Ultraviolet disinfection

Indexed keywords

BACTERIA; BACTERIOLOGY; DISINFECTION; GENES; IRRADIATION; POLYMERASE CHAIN REACTION; RADIATION EFFECTS; THROUGHPUT; ULTRAVIOLET RADIATION; WASTEWATER TREATMENT;

ANTIBIOTIC RESISTANCE GENES; ANTIBIOTICS RESISTANCE; GENETIC ELEMENTS; HIGH-THROUGHPUT SEQUENCING; METAGENOMICS; MICROBIAL COMMUNITIES; MOBILE GENETIC ELEMENT; RELATIVE ABUNDANCE; TREATED WASTEWATER; ULTRAVIOLET DISINFECTIONS;

ANTIBIOTICS;

AMINOGLYCOSIDE ANTIBIOTIC AGENT; BACITRACIN; BETA LACTAM ANTIBIOTIC; CHLORAMPHENICOL; FOSFOMYCIN; FOSMIDOMYCIN; LINCOSAMIDE; MACROLIDE; POLYMYXIN; QUINOLONE; STREPTOGRAMIN DERIVATIVE; SULFONAMIDE; TETRACYCLINE; TRIMETHOPRIM; ANTIINFECTIVE AGENT;

ABUNDANCE ESTIMATION; ANTIBIOTIC RESISTANCE; COMMUNITY STRUCTURE; DISINFECTION; GENE; GENETIC ANALYSIS; MICROBIAL COMMUNITY; RELATIVE ABUNDANCE; SPECIES DIVERSITY; ULTRAVIOLET RADIATION; WASTEWATER;

AEROMONAS; ANTIBIOTIC RESISTANCE; ANTIBIOTIC RESISTANCE GENE; ARTICLE; BACILLUS; BACTERIAL GENE; BACTERIAL VIABILITY; BACTEROIDES; BACTEROIDETES; COMMUNITY STRUCTURE; CYANOBACTERIUM; ESCHERICHIA COLI; GAMMAPROTEOBACTERIA; HALOMONAS; HIGH THROUGHPUT SEQUENCING; KLEBSIELLA; METAGENOMICS; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; MOBILE GENETIC ELEMENT; MULTIDRUG RESISTANCE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOTOREACTIVATION; POPULATION ABUNDANCE; PRIORITY JOURNAL; PROTEOBACTERIA; PSEUDOMONAS AERUGINOSA; QUANTITATIVE ANALYSIS; RADIATION DOSE; REAL TIME POLYMERASE CHAIN REACTION; SALMONELLA; SPHAEROTILUS; ULTRAVIOLET RADIATION; WASTE WATER MANAGEMENT; DISINFECTION; GENETICS; MICROBIOLOGY; WASTE WATER;

AEROMONAS; BACILLUS (BACTERIUM); BACTERIA (MICROORGANISMS); HALOMONAS; PSEUDOMONAS;

ANTI-BACTERIAL AGENTS; DISINFECTION; DRUG RESISTANCE, MICROBIAL; METAGENOMICS; ULTRAVIOLET RAYS; WASTE WATER;

EID: 84971634532     PISSN: 00431354     EISSN: 18792448     Source Type: Journal    
DOI: 10.1016/j.watres.2016.05.092     Document Type: Article

References (59)

1. Alekshun M.N., Levy S.B. Molecular mechanisms of antibacterial multidrug resistance. Cell 2007, 128(6):1037-1050.
2. Aminov R.I. Horizontal gene exchange in environmental microbiota. Front. Microbiol. 2011, 2:19.
3. Biswal B.K., Khairallah R., Bibi K., Mazza A., Gehr R., Masson L., Frigon D. Impact of UV and peracetic acid disinfection on the prevalence of virulence and antimicrobial resistance genes in uropathogenic Escherichia coli in wastewater effluents. Appl. Environ. Microbiol. 2014, 80(12):3656-3666.
4. Chao Y.Q., Ma L.P., Yang Y., Ju F., Zhang X.X., Wu W.M., Zhang T. Metagenomic analysis reveals significant changes of microbial compositions and protective functions during drinking water treatment. Sci. Rep. 2013, 3:9.
5. Chen B.W., Yang Y., Liang X.M., Yu K., Zhang T., Li X.D. Metagenomic profiles of antibiotic resistance genes (ARGs) between human impacted estuary and deep ocean sediments. Environ. Sci. Technol. 2013, 47(22):12753-12760.
6. Cole J.R., Chai B., Farris R.J., Wang Q., Kulam S., McGarrell D.M., Garrity G.M., Tiedje J.M. The Ribosomal Database Project (RDP-II): sequences and tools for high-throughput rRNA analysis. Nucleic Acids Res. 2005, 33(Suppl. 1):D294-D296.
7. Craik S.A., Finch G.R., Bolton J.R., Belosevic M. Inactivation of Giardia muris cysts using medium-pressure ultraviolet radiation in filtered drinking water. Water Res. 2000, 34(18):4325-4332.
8. Da Costa P.M., Vaz-Pires P., Bernardo F. Antimicrobial resistance in Enterococcus spp. isolated in inflow, effluent and sludge from municipal sewage water treatment plants. Water Res. 2006, 40(8):1735-1740.
9. Damelin L., Vokes S., Whitcutt J., Damelin S., Alexander J. Hormesis: a stress response in cells exposed to low levels of heavy metals. Hum. Exp. Toxicol. 2000, 19(7):420-430.
10. Davies J., Spiegelman G.B., Yim G. The world of subinhibitory antibiotic concentrations. Curr. Opin. Microbiol. 2006, 9(5):445-453.
11. 2-fixing bacterial diversity in soil under Acacia tortilis ssp. raddiana and Balanites aegyptiaca in the dryland part of Senegal. Environ. Microbiol. 2004, 6(4):400-415.
12. DeVos D., Lim A., Pirnay J.P., Struelens M., Vandenvelde C., Duinslaeger L., Vanderkelen A., Cornelis P. Direct detection and identification of Pseudomonas aeruginosa in clinical samples such as skin biopsy specimens and expectorations by multiplex PCR based on two outer membrane lipoprotein genes, oprI and oprL. J. Clin. Microbiol. 1997, 35(6):1295-1299.
13. Dodd M.C. Potential impacts of disinfection processes on elimination and deactivation of antibiotic resistance genes during water and wastewater treatment. J. Environ. Monit. 2012, 14(7):1754-1771.
14. Guo M.T., Yuan Q.B., Yang J. Microbial selectivity of UV treatment on antibiotic-resistant heterotrophic bacteria in secondary effluents of a municipal wastewater treatment plant. Water Res. 2013, 47(16):6388-6394.
15. Hassen A., Mahrouk M., Ouzari H., Cherif M., Boudabous A., Damelincourt J.J. UV disinfection of treated wastewater in a large-scale pilot plant and inactivation of selected bacteria in a laboratory UV device. Bioresour. Technol. 2000, 74(2):141-150.
16. Hijnen W.A., Beerendonk E.F., Medema G.J. Inactivation credit of UV radiation for viruses, bacteria and protozoan (oo)cysts in water: a review. Water Res. 2006, 40(1):3-22.
17. Huson D.H., Auch A.F., Qi J., Schuster S.C. MEGAN analysis of metagenomic data. Genome Res. 2007, 17(3):377-386.
18. Jia S., Shi P., Hu Q., Li B., Zhang T., Zhang X.X. Bacterial community shift drives antibiotic resistance promotion during drinking water chlorination. Environ. Sci. Technol. 2015, 49(20):12271-12279.
19. Jungfer C., Schwartz T., Obst U. UV-induced dark repair mechanisms in bacteria associated with drinking water. Water Res. 2007, 41(1):188-196.
20. Kaur J., Karthikeyan R., Pillai S.D. Effectiveness of ultrasound, UV-C, and photocatalysis on inactivation kinetics of Aeromonas hydrophila. J. Environ. Sci. Health C 2015, 50(12):1223-1229.
21. Kim S.C., Carlson K. Temporal and spatial trends in the occurrence of human and veterinary antibiotics in aqueous and river sediment matrices. Environ. Sci. Technol. 2007, 41(1):50-57.
22. Kirchman D.L. The ecology of Cytophaga-Flavobacteria in aquatic environments. FEMS Microbiol. Ecol. 2002, 39(2):91-100.
23. Kokjohn T.A., Miller R.V. IncN plasmids mediate UV resistance and error-prone repair in Pseudomonas aeruginosa PAO. Microbiology 1994, 140:43-48.
24. Kozich J.J., Westcott S.L., Baxter N.T., Highlander S.K., Schloss P.D. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl. Environ. Microbiol. 2013, 79(17):5112-5120.
25. Kummerer K. Antibiotics in the aquatic environment - a review - part I. Chemosphere 2009, 75(4):417-434.
26. Lai J., Mi X. Ordination analysis of ecological data using Vegan package in R. Adv. Biodivers. Conserv. Res. China 2005, 332-343.
27. Lambert P. Mechanisms of antibiotic resistance in Pseudomonas aeruginosa. J. R. Soc. Med. 2002, 95(Suppl. 41):22.
28. Legendre P., Legendre L.F. Numer. Ecol. 2012, Elsevier.
29. Levy M.S., Balbinder E., Nagel R. Effect of mutations in SOS genes on UV-induced precise excision of Tn10 in Escherichia coli. Mutat. Res. DNA Repair 1993, 293(3):241-247.
30. Li B., Zhang T. Different removal behaviours of multiple trace antibiotics in municipal wastewater chlorination. Water Res. 2013, 47(9):2970-2982.
31. Li X.-Z., Nikaido H. Efflux-mediated drug resistance in bacteria. Drugs 2004, 64(2):159-204.
32. Linden K.G., Shin G.A., Faubert G., Cairns W., Sobsey M.D. UV disinfection of Giardia lamblia cysts in water. Environ. Sci. Technol. 2002, 36(11):2519-2522.
33. Lopez-Gutierrez J.C., Henry S., Hallet S., Martin-Laurent F., Catroux G., Philippot L. Quantification of a novel group of nitrate-reducing bacteria in the environment by real-time PCR. J. Microbiol. Methods 2004, 57(3):399-407.
34. Luddeke F., Hess S., Gallert C., Winter J., Gude H., Loffler H. Removal of total and antibiotic resistant bacteria in advanced wastewater treatment by ozonation in combination with different filtering techniques. Water Res. 2015, 69:243-251.
35. Luo Y., Xu L., Rysz M., Wang Y.Q., Zhang H., Alvarez P.J.J. Occurrence and transport of tetracycline, sulfonamide, quinolone, and macrolide antibiotics in the Haihe River Basin, China. Environ. Sci. Technol. 2011, 45(5):1827-1833.
36. 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.
37. Martin E.L., Reinhardt R.L., Baum L.L., Becker M.R., Shaffer J.J., Kokjohn T.A. The effects of ultraviolet radiation on the moderate halophile Halomonas elongata and the extreme halophile Halobacterium salinarum. Can. J. Microbiol. 2000, 46(2):180-187.
38. McKinney C.W., Pruden A. Ultraviolet disinfection of antibiotic resistant bacteria and their antibiotic resistance genes in water and wastewater. Environ. Sci. Technol. 2012, 46(24):13393-13400.
39. 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.
40. Nebot Sanz E., Salcedo Davila I., Andrade Balao J.A., Quiroga Alonso J.M. Modelling of reactivation after UV disinfection: effect of UV-C dose on subsequent photoreactivation and dark repair. Water Res. 2007, 41(14):3141-3151.
41. Ordoñez O.F., Flores M.R., Dib J.R., Paz A., Farías M.E. Extremophile culture collection from Andean lakes: extreme pristine environments that host a wide diversity of microorganisms with tolerance to UV radiation. Microb. Ecol. 2009, 58(3):461-473.
42. 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.
43. Proteau P., Gerwick W., Garcia-Pichel F., Castenholz R. The structure of scytonemin, an ultraviolet sunscreen pigment from the sheaths of cyanobacteria. Experientia 1993, 49(9):825-829.
44. Pruden A. Balancing water sustainability and public health goals in the face of growing concerns about antibiotic resistance. Environ. Sci. Technol. 2013, 48(1):5-14.
45. Pruden A., Pei R.T., Storteboom H., Carlson K.H. Antibiotic resistance genes as emerging contaminants: studies in northern Colorado. Environ. Sci. Technol. 2006, 40(23):7445-7450.
46. Riesenman P.J., Nicholson W.L. Role of the spore coat layers in Bacillus subtilis spore resistance to hydrogen peroxide, artificial UV-C, UV-B, and solar UV radiation. Appl. Environ. Microbiol. 2000, 66(2):620-626.
47. Shi P., Jia S., Zhang X.X., Zhang T., Cheng S., Li A. Metagenomic insights into chlorination effects on microbial antibiotic resistance in drinking water. Water Res. 2013, 47(1):111-120.
48. Smillie C.S., Smith M.B., Friedman J., Cordero O.X., David L.A., Alm E.J. Ecology drives a global network of gene exchange connecting the human microbiome. Nature 2011, 480(7376):241-244.
49. Sogin M.L., Morrison H.G., Huber J.A., Mark Welch D., Huse S.M., Neal P.R., Arrieta J.M., Herndl G.J. Microbial diversity in the deep sea and the underexplored "rare biosphere". Proc. Natl. Acad. Sci. U. S. A. 2006, 103(32):12115-12120.
50. Steinborn G., Hajirezaei M.R., Hofemeister J. Bac genes for recombinant bacilysin and anticapsin production in Bacillus host strains. Arch. Microbiol. 2005, 183(2):71-79.
51. Stevens C., Khan V., Lu J., Wilson C., Pusey P., Kabwe M., Igwegbe E., Chalutz E., Droby S. The germicidal and hormetic effects of UV-C light on reducing brown rot disease and yeast microflora of peaches. Crop Prot. 1998, 17(1):75-84.
52. Stover C.K., Pham X.Q., Erwin A.L., Mizoguchi S.D., Warrener P., Hickey M.J., Brinkman F.S.L. Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 2000, 406:959-964.
53. Tandukar M., Oh S., Tezel U., Konstantinidis K.T., Pavlostathis S.G. Long-term exposure to benzalkonium chloride disinfectants results in change of microbial community structure and increased antimicrobial resistance. Environ. Sci. Technol. 2013, 47(17):9730-9738.
54. Wegrzyn G., Wegrzyn A. Stress responses and replication of plasmids in bacterial cells. Microb. Cell Fact. 2002, 1:10.
55. 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.
56. Yang Y., Li B., Zou S.C., Fang H.H.P., Zhang T. Fate of antibiotic resistance genes in sewage treatment plant revealed by metagenomic approach. Water Res. 2014, 62:97-106.
57. Ye L., Zhang T., Wang T.T., Fang Z.W. Microbial structures, functions, and metabolic pathways in wastewater treatment bioreactors revealed using high-throughput sequencing. Environ. Sci. Technol. 2012, 46(24):13244-13252.
58. Zhang T., Zhang X.X., Ye L. Plasmid metagenome reveals high levels of antibiotic resistance genes and mobile genetic elements in activated sludge. PloS One 2011, 6(10):7.
59. 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(9):3435-3440.