High throughput profiling of antibiotic resistance genes in urban park soils with reclaimed water irrigation

Environmental Science and Technology

Volumn 48, Issue 16, 2014, Pages 9079-9085

  Wang, Feng Hua ^a,b   Qiao, Min ^a   Su, Jian Qiang ^c   Chen, Zheng ^a   Zhou, Xue ^a,b   Zhu, Yong Guan ^a,c  

^a RESEARCH CENTER FOR ECO ENVIRONMENTAL SCIENCES   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTICS; GENES; IRRIGATION; POLYMERASE CHAIN REACTION; RECLAMATION; SOIL SURVEYS;

ANTIBIOTIC RESISTANCE GENES; DOMINANT MECHANISM; POSITIVE CORRELATIONS; QUANTITATIVE PCR; RAPID URBANIZATIONS; RE-CLAIMED WATER; URBAN ENVIRONMENTS; URBAN PARK SOILS;

SOILS;

AMINOGLYCOSIDE; BETA LACTAM; CHLORAMPHENICOL; FLORFENICOL; MACROLIDE; QUINOLONE; QUINOLONE DERIVATIVE; TETRACYCLINE; TRANSPOSASE; VANCOMYCIN; WATER; ANTIINFECTIVE AGENT; BACTERIAL DNA;

ANTIBIOTIC RESISTANCE; ANTIBIOTICS; DETECTION METHOD; GENE EXPRESSION; IRRIGATION; RECYCLING; URBAN AREA; WATER TREATMENT;

ACTIVATED SLUDGE; ANTIBIOTIC RESISTANCE; ARTICLE; CONTROLLED STUDY; GENETIC RESISTANCE; HIGH THROUGHPUT SEQUENCING; HUMAN; IRRIGATION (AGRICULTURE); METAGENOME; NONHUMAN; QUANTITATIVE ANALYSIS; SOIL; BACTERIAL GENE; CHINA; CITY; GENETICS; MICROBIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; RECYCLING;

ANTI-BACTERIAL AGENTS; CHINA; CITIES; DNA, BACTERIAL; DRUG RESISTANCE, MICROBIAL; GENES, BACTERIAL; REAL-TIME POLYMERASE CHAIN REACTION; RECYCLING; SOIL MICROBIOLOGY; WATER;

EID: 84906257249     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/es502615e     Document Type: Article

References (52)

1. Stoll, C.; Sidhu, J. P.; Tiehm, A.; Toze, S. Prevalence of clinically relevant antibiotic resistance genes in surface water samples collected from Germany and Australia Environ. Sci. Technol. 2012, 46 (17) 9716-9726
2. 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
3. Cooper, M. A.; Shlaes, D. Fix the antibiotics pipeline Nature 2011, 472, 32
4. Gogarten, J. P.; Townsend, J. P. Horizontal gene transfer, genome innovation and evolution Nat. Rev. Microbiol. 2005, 3 (9) 679-687
5. Schluter, A.; Szczepanowski, R.; Puhler, A.; Top, E. M. Genomics of IncP-1 antibiotic resistance plasmids isolated from wastewater treatment plants provides evidence for a widely accessible drug resistance gene pool FEMS Microbiol. Rev. 2007, 31 (4) 449-477
6. Mao, D.; Luo, Y.; Mathieu, J.; Wang, Q.; Feng, L.; Mu, Q.; Feng, C.; Alvarez, P. J. Persistence of extracellular DNA in river sediment facilitates antibiotic resistance gene propagation Environ. Sci. Technol. 2014, 48 (1) 71-78
7. Pruden, A. Balancing water sustainability and public health goals in the face of growing concerns about antibiotic resistance Environ. Sci. Technol. 2014, 48 (1) 5-14
8. Gao, P.; Munir, M.; Xagoraraki, I. Correlation of tetracycline and sulfonamide antibiotics with corresponding resistance genes and resistant bacteria in a conventional municipal wastewater treatment plant Sci. Total Environ. 2012, 421-422, 173-183
9. Chen, H.; Zhang, M. Effects of advanced treatment systems on the removal of antibiotic resistance genes in wastewater treatment plants from Hangzhou, China Environ. Sci. Technol. 2013, 47 (15) 8157-8163
10. Zhang, X. X.; Zhang, T. Occurrence, abundance, and diversity of tetracycline resistance genes in 15 sewage treatment plants across China and other global locations Environ. Sci. Technol. 2011, 45 (7) 2598-2604
11. 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
12. Rizzo, L.; Manaia, C.; Merlin, C.; Schwartz, T.; Dagot, C.; Ploy, M. C.; Michael, I.; 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
13. 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
14. Li, B.; Zhang, T. Mass flows and removal of antibiotics in two municipal wastewater treatment plants Chemosphere 2011, 83 (9) 1284-1289
15. Auerbach, E. A.; Seyfried, E. E.; McMahon, K. D. Tetracycline resistance genes in activated sludge wastewater treatment plants Water Res. 2007, 41 (5) 1143-1151
16. Li, B.; Zhang, T. Biodegradation and adsorption of antibiotics in the activated sludge process Environ. Sci. Technol. 2010, 44 (9) 3468-3473
17. Zhang, T.; Zhang, M.; Zhang, X. X.; Fang, H. P. H. Tetracycline resistance genes and tetracycline resistance lactose-fermenting Enterobacteriaceae in activated sludge of sewage treatment plant Environ. Sci. Technol. 2009, 43 (10) 3455-3460
18. Szczepanowski, R.; Linke, B.; Krahn, I.; Gartemann, K. H.; Gützkow, T.; Eichler, W.; Pühler, A.; 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
19. Wang, F. H.; Qiao, M.; Lv, Z. E.; Guo, G. X.; Jia, Y.; Su, Y. H.; Zhu, Y. G. Impact of reclaimed water irrigation on antibiotic resistance in public parks, Beijing, China Environ. Pollut. 2014, 184, 247-253
20. Negreanu, Y.; Pasternak, Z.; Jurkevitch, E.; Cytryn, E. Impact of treated wastewater irrigation on antibiotic resistance in agricultural soils Environ. Sci. Technol. 2012, 46 (9) 4800-4808
21. Czekalski, N.; Díez, E. G.; Bürgmann, H. Wastewater as a point source of antibiotic-resistance genes in the sediment of a freshwater lake ISME J. 2014, 10.1038/ismej.2014.8
22. Zhang, T.; Li, B. Occurrence, transformation, and fate of antibiotics in municipal wastewater treatment plants Crit. Rev. Environ. Sci. Technol. 2011, 41 (11) 951-998
23. Fahrenfeld, N.; Ma, Y.; O'Brien, M.; Pruden, A. Reclaimed water as a reservoir of antibiotic resistance genes: Distribution system and irrigation implications Front. Microbiol. 2013, 4, 1-10
24. Allen, H. K.; Moe, L. A.; Rodbumrer, J.; Gaarder, A.; Handelsman, J. Functional metagenomics reveals diverse beta-lactamases in a remote Alaskan soil ISME J. 2009, 3 (2) 243-251
25. D'Costa, V. M.; King, C. E.; Kalan, L.; Morar, M.; Sung, W. W.; Schwarz, C.; Froese, D.; Zazula, G.; Calmels, F.; Debruyne, R.; Golding, G. B.; Poinar, H. N.; Wright, G. D. Antibiotic resistance is ancient Nature 2011, 477 (7365) 457-461
26. Zhou, J. Z.; Bruns, M. A.; Tiedje, J. M. DNA recovery from soils of diverse composition Appl. Environ. Microbiol. 1996, 62 (2) 316-322
27. 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 PNAS 2013, 110 (9) 3435-3440
28. Stedtfeld, R. D.; Baushke, S. W.; Tourlousse, D. M.; Miller, S. M.; Stedtfeld, T. M.; Gulari, E.; Tiedje, J. M.; Hashsham, S. A. Development and experimental validation of a predictive threshold cycle equation for quantification of virulence and marker genes by high-throughput nanoliter-volume PCR on the openarray platform Appl. Environ. Microbiol. 2011, 74 (12) 3831-3838
29. Zhang, D. D.; Lin, L. F.; Luo, Z. X.; Yan, C. Z.; Zhang, X. Occurrence of selected antibiotics in Jiulongjiang River in various season, South China J. Environ. Monit. 2011, 13 (7) 1953-1960
30. Chen, B.; Yang, Y.; Liang, X.; Yu, K.; Zhang, T.; Li, X. Metagenomic profiles of antibiotic resistance genes (ARGs) between human impacted estuary and deep ocean sediments Environ. Sci. Technol. 2013, 47 (22) 12753-12760
31. Ziglam, H. M.; Finch, R. G. Limitations of presently available glycopeptides in the treatment of Gram-positive infection Clin. Microbiol. Infect. 2001, 7, 53-65
32. 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) e26041
33. Enne, V. I.; Livermore, D. M.; Stephens, P.; Hall, L. M. C. Persistence of sulphonamide resistance in Escherichia coli in the UK despite national prescribing restriction Lancet 2001, 357 (9265) 1325-1328
34. Chen, H.; Zhang, M. Occurrence and removal of antibiotic resistance genes in municipal wastewater and rural domestic sewage treatment systems in eastern China Environ. Int. 2013, 55, 9-14
35. Peak, N.; Knapp, C. W.; Yang, R. K.; Hanfelt, M. M.; Smith, M. S.; Aga, D. S.; Graham, D. W. Abundance of six tetracycline resistance genes in wastewater lagoons at cattle feedlots with different antibiotic use strategies Environ. Microbiol. 2007, 9 (1) 143-151
36. Frenk, S.; Hadar, Y.; Minz, D. Resilience of soil bacterial community to irrigation with water of different qualities under Mediterranean climate Environ. Microbiol. 2014, 16 (2) 559-569
37. Gatica, J.; Cytryn, E. Impact of treated wastewater irrigation on antibiotic resistance in the soil microbiome Environ. Sci. Pollut. Res. 2013, 20 (6) 3529-3538
38. Shi, Y. L.; Gao, L. H.; Li, W. H.; Liu, J. M.; Cai, Y. Q. Investigation of fluoroquinolones, sulfonamides and macrolides in long-term wastewater irrigation soil in Tianjin, China Bull. Environ. Contam. Toxicol. 2012, 89 (4) 857-861
39. Storteboom, H.; Arabi, M.; Jessica, G. D.; Pruden, A. Tracking antibiotic resistance genes in the South Platte River basin using molecular signatures of urban, agricultural, and pristine sources Environ. Sci. Technol. 2010, 44 (19) 7397-7404
40. Chen, B. W.; Liang, X. M.; Huang, X. P.; Zhang, T.; Li, X. D. Differentiating anthropogenic impacts on ARGs in the Pearl River Estuary by using suitable gene indicators Water Res. 2013, 47 (8) 2811-2820
41. Rizzotti, L.; Gioia, F. L.; Dellaglio, F.; Torriani, S. Molecular diversity and transferability of the tetracycline resistance gene tet (M), carried on Tn 916-1545 family transposons, in enterococci from a total food chain Antonie Van Leeuwenhoek 2009, 96 (1) 43-52
42. Chopra, I.; Roberts, M. Tetracycline antibiotics: Mode of action, applications, molecular biology, and epidemiology of bacterial resistance Microbiol. Mol. Biol. Rev. 2001, 65 (2) 232-260
43. Kazimierczak, K. A.; Flint, H. J.; Scott, K. P. Comparative analysis of sequences flanking tet (W) resistance genes in multiple species of gut bacteria Antimicrob. Agents Chemother. 2006, 50 (8) 2632-2639
44. Eikmeyer, F.; Hadiati, A.; Szczepanowski, R.; Wibberg, D.; Schneiker-Bekel, S.; Rogers, L. M.; Brown, C. J.; Top, E. M.; Puhler, A.; Schluter, A. The complete genome sequences of four new IncN plasmids from wastewater treatment plant effluent provide new insights into IncN plasmid diversity and evolution Plasmid 2012, 68 (1) 13-24
45. Coudron, P. E.; Moland, E. S.; Thomson, K. S. Occurrence and detection of AmpC beta-lactamases among Escherichia coli, Klebsiella pneumoniae, and Proteus mirabilis isolates at a veterans medical center J. Clin. Microbiol. 2000, 38 (5) 1791-1796
46. Doublet, B.; Schwarz, S.; Kehrenberg, C.; Cloeckaert, A. Florfenicol resistance gene floR is part of a novel transposon Antimicrob. Agents Chemother. 2005, 49 (5) 2106-2108
47. Okitsu, N.; Kaieda, S.; Yano, H.; Nakano, R.; Hosaka, Y.; Okamoto, R.; Kobayashi, T.; Inoue, M. Characterization of ermB gene transposition by Tn 1545 and Tn 917 in macrolide-resistant Streptococcus pneumoniae isolates J. Clin. Microbiol. 2005, 43 (1) 168-173
48. Jechalke, S.; Kopmann, C.; Rosendahl, I.; Groeneweg, J.; Weichelt, V.; Krö gerrecklenfort, E.; Brandes, N.; Nordwig, M.; Ding, G. C.; Siemens, J.; Heuer, H.; Smalla, K. Increased abundance and transferability of resistance genes after field application of manure from sulfadiazine-treated pigs Appl. Environ. Microbiol. 2013, 79 (5) 1704-1711
49. 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
50. Linares, J. F.; Gustafsson, I.; Baquero, F.; Martinez, J. L. Antibiotics as intermicrobial signaling agents instead of weapons PNAS 2006, 103 (51) 19484-19489
51. Stanton, T. B.; Humphrey, S. B. Persistence of antibiotic resistance: Evaluation of a probiotic approach using antibiotic-sensitive megasphaera elsdenii strains to prevent colonization of swine by antibiotic-resistant strains. Applied Environ. Microbiol. 2011, 77 (20) 7158-7166
52. Looft, T.; Johnson, T. A.; Allen, H. K.; Bayles, D. O.; Alt, D. P.; Stedtfeld, R. D.; Sul, W. J.; Stedtfeld, T. M.; Chai, B.; Cole, J. R.; Hashsham, S. A.; Tiedje, J. M.; Stanton, T. B. In-feed antibiotic effects on the swine intestinal microbiome PNAS 2012, 109 (5) 1691-1696