Continental-scale pollution of estuaries with antibiotic resistance genes

Nature Microbiology

Volumn 2, Issue , 2017, Pages

  Zhu, Yong Guan ^a,b   Zhao, Yi ^a   Li, Bing ^c   Huang, Chu Long ^a   Zhang, Si Yu ^b   Yu, Shen ^a   Chen, Yong Shan ^a   Zhang, Tong ^d   Gillings, Michael R ^e   Su, Jian Qiang ^a  

^a INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^b RESEARCH CENTER FOR ECO ENVIRONMENTAL SCIENCES   (China)

^c TSINGHUA UNIVERSITY   (China)

^d UNIVERSITY OF HONG KONG   (Hong Kong)

^e MACQUARIE UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA;

ANTIBIOTIC RESISTANCE; BACTERIAL GENE; BACTERIUM; CHINA; ESTUARY; GENETICS; HUMAN; INTERSPERSED REPEAT; ISOLATION AND PURIFICATION; MICROBIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; SEDIMENT;

BACTERIA; CHINA; DNA, BACTERIAL; DRUG RESISTANCE, BACTERIAL; ESTUARIES; GENES, BACTERIAL; GEOLOGIC SEDIMENTS; HUMANS; INTERSPERSED REPETITIVE SEQUENCES; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 85011256332     PISSN: None     EISSN: 20585276     Source Type: Journal    
DOI: 10.1038/nmicrobiol.2016.270     Document Type: Article

References (49)

1. Culliton, T. J. Population: distribution, density, and growth (State of the Coast Report, NOAA, 1998); http://oceanservice.noaa.gov/websites/retiredsites/sotc-pdf/POP.PDF.
2. Lotze, H. K. et al. Depletion, degradation, and recovery potential of estuaries and coastal seas. Science 312, 1806-1809 (2006).
3. He, Q. et al. Economic development and coastal ecosystem change in China. Sci. Rep. 4, 5995 (2014).
4. Da, C., Liu, G. & Yuan, Z. Analysis of HCHs and DDTs in a sediment core from the Old Yellow River estuary, China. Ecotoxicol. Environ. Saf. 100, 171-177 (2014).
5. Wu, G., Shang, J., Pan, L. & Wang, Z. Heavy metals in surface sediments from nine estuaries along the coast of Bohai Bay, Northern China. Mar. Pollut. Bull. 82, 194-200 (2014).
6. Pruden, A., Pei, R., Storteboom, H. & Carlson, K. H. Antibiotic resistance genes as emerging contaminants: studies in northern Colorado. Environ. Sci. Technol. 40, 7445-7450 (2006).
7. Knapp, C. W., Dolfing, J., Ehlert, P. A. & Graham, D. W. Evidence of increasing antibiotic resistance gene abundances in archived soils since 1940. Environ. Sci. Technol. 44, 580-587 (2009).
8. Segawa, T. et al. Distribution of antibiotic resistance genes in glacier environments. Environ. Microbiol. Rep. 5, 127-134 (2013).
9. Drudge, C. N. et al. Diversity of integron- and culture-associated antibiotic resistance genes in freshwater floc. Appl. Environ. Microbiol. 78, 4367-4372 (2012).
10. McKinney, C. W. & Pruden, A. Ultraviolet disinfection of antibiotic resistant bacteria and their antibiotic resistance genes in water and wastewater. Environ. Sci. Technol. 46, 13393-13400 (2012).
11. Wang, F. H. et al. High throughput profiling of antibiotic resistance genes in urban park soils with reclaimed water irrigation. Environ Sci Technol. 48, 9079-9085 (2014).
12. Ouyang, W. Y., Huang, F. Y., Zhao, Y., Li, H. & Su, J. Q. Increased levels of antibiotic resistance in urban stream of Jiulongjiang River, China. Appl. Microbiol. Biotechnol. 99, 5697-5707 (2015).
13. Czekalski, N., Gascon Diez, E. & Burgmann, H. Wastewater as a point source of antibiotic-resistance genes in the sediment of a freshwater lake. ISME J. 8, 1381-1390 (2014).
14. Gaze, W. H. et al. Impacts of anthropogenic activity on the ecology of class 1 integrons and integron-associated genes in the environment. ISME J. 5, 1253-1261 (2011).
15. Amos, G. C., Zhang, L., Hawkey, P. M., Gaze, W. H. & Wellington, E. M. Functional metagenomic analysis reveals rivers are a reservoir for diverse antibiotic resistance genes. Vet. Microbiol. 171, 441-447 (2014).
16. Khan, G. A., Berglund, B., Khan, K. M., Lindgren, P.-E. & Fick, J. Occurrence and abundance of antibiotics and resistance genes in rivers, canal and near drug formulation facilities-a study in Pakistan. PLoS ONE 8, e62712 (2013).
17. Zhang, Q. Q., Ying, G. G., Pan, C. G., Liu, Y. S. & Zhao, J. L. Comprehensive evaluation of antibiotics emission and fate in the river basins of China: source analysis, multimedia modeling, and linkage to bacterial resistance. Environ. Sci. Technol. 49, 6772-6782 (2015).
18. Kolpin, D. W. et al. Pharmaceuticals, hormones, and other organic wastewater contaminants in US streams, 1999-2000: a national reconnaissance. Environ. Sci. Technol. 36, 1202-1211 (2002).
19. Ochman, H., Lawrence, J. G. & Groisman, E. A. Lateral gene transfer and the nature of bacterial innovation. Nature 405, 299-304 (2000).
20. Chen, B., Liang, X., Huang, X., Zhang, T. & Li, X. Differentiating anthropogenic impacts on ARGs in the Pearl River estuary by using suitable gene indicators. Water Res. 47, 2811-2820 (2013).
21. Forsberg, K. J. et al. Bacterial phylogeny structures soil resistomes across habitats. Nature 509, 612-616 (2014).
22. Michael, I. et al. Urban wastewater treatment plants as hotspots for the release of antibiotics in the environment: a review. Water Res. 47, 957-995 (2013).
23. Cytryn, E. The soil resistome: the anthropogenic, the native, and the unknown. Soil Biol. Biochem. 63, 18-23 (2013).
24. Partridge, S. R., Tsafnat, G., Coiera, E. & Iredell, J. R. Gene cassettes and cassette arrays in mobile resistance integrons. FEMS Microbiol. Rev. 33, 757-784 (2009).
25. Newman, M. E. Modularity and community structure in networks. Proc. Natl Acad. Sci. USA 103, 8577-8582 (2006).
26. Zhu, Y. G. et al. Diverse and abundant antibiotic resistance genes in Chinese swine farms. Proc. Natl Acad. Sci. USA 110, 3435-3440 (2013).
27. Oppegaard, H., Steinum, T. M. & Wasteson, Y. Horizontal transfer of a multi-drug resistance plasmid between coliform bacteria of human and bovine origin in a farm environment. Appl. Environ. Microbiol. 67, 3732-3734 (2001).
28. Zhang, R., Eggleston, K., Rotimi, V. & Zeckhauser, R. J. Antibiotic resistance as a global threat: evidence from China, Kuwait and the United States. Global. Health 2, 6 (2006).
29. RUBIN, M. et al. Gram-positive infections and the use of vancomycin in 550 episodes of fever and neutropenia. Ann. Intern. Med. 108, 30-35 (1988).
30. D'Costa, V. M. et al. Antibiotic resistance is ancient. Nature 477, 457-461 (2011).
31. Gilmore, M. S. & Hoch, J. A. Antibiotic resistance: a vancomycin surprise. Nature 399, 524-527 (1999).
32. Lauderdale, T. L. et al. Effect of banning vancomycin analogue avoparcin on vancomycin-resistant enterococci in chicken farms in Taiwan. Environ. Microbiol. 9, 819-823 (2007).
33. Perry, J. A., Westman, E. L. & Wright, G. D. The antibiotic resistome: what's new? Curr. Opin. Microbiol. 21, 45-50 (2014).
34. Gillings, M. R. et al. Using the class 1 integron-integrase gene as a proxy for anthropogenic pollution. ISME J. 9, 1269-1279 (2015).
35. Gillings, M. et al. The evolution of class 1 integrons and the rise of antibiotic resistance. J. Bacteriol. 190, 5095-5100 (2008).
36. Gillings, M. R. Integrons: past, present, and future. Microbiol. Mol. Biol. Rev. 78, 257-277 (2014).
37. Su, J. Q. et al. Antibiotic resistome and its association with bacterial communities during sewage sludge composting. Environ. Sci. Technol. 49, 7356-7363 (2015).
38. Dini-Andreote, F., Stegen, J. C., van Elsas, J. D. & Salles, J. F. Disentangling mechanisms that mediate the balance between stochastic and deterministic processes in microbial succession. Proc. Natl Acad. Sci. USA 112, E1326-E1332 (2015).
39. Gillings, M. R. & Stokes, H. Are humans increasing bacterial evolvability? Trends Ecol. Evol. 27, 346-352 (2012).
40. Stokes, H. W. & Gillings, M. R. Gene flow, mobile genetic elements and the recruitment of antibiotic resistance genes into Gram-negative pathogens. FEMS. Microbiol. Rev. 35, 790-819 (2011).
41. Liu, Y.-Y. et al. Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: a microbiological and molecular biological study. Lancet. Infect. Dis. 16, 161-168 (2016).
42. Huang, Y. et al. Simultaneous extraction of four classes of antibiotics in soil, manure and sewage sludge and analysis by liquid chromatography-tandem mass spectrometry with the isotope-labelled internal standard method. Anal. Methods 5, 3721 (2013).
43. Looft, T. et al. In-feed antibiotic effects on the swine intestinal microbiome. Proc. Natl Acad. Sci. USA 109, 1691-1696 (2012).
44. Xu, H.-J. et al. Biochar impacts soil microbial community composition and nitrogen cycling in an acidic soil planted with rape. Environ. Sci. Technol. 48, 9391-9399 (2014).
45. Kuczynski, J. et al. Using QIIME to analyze 16S rRNA gene sequences from microbial communities. Curr. Protoc. Bioinformatics 10, 10.7 (2011).
46. Edgar, R. C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460-2461 (2010).
47. Klappenbach, J. A., Saxman, P. R., Cole, J. R. & Schmidt, T. M. Rrndb: the ribosomal RNA operon copy number database. Nucleic Acids Res. 29, 181-184 (2001).
48. Kolde, R. Pheatmap: pretty heatmaps, R package v. 16 (R Foundation for Statistical Computing, 2012).
49. Li, B. et al. Metagenomic and network analysis reveal wide distribution and co-occurrence of environmental antibiotic resistance genes. ISME J. 9, 2490-2502 (2015).