Comparative metagenomics reveals a diverse range of antimicrobial resistance genes in effluents entering a river catchment

Water Science and Technology

Volumn 73, Issue 7, 2016, Pages 1541-1549

  Rowe, Will ^a   Maskell, Duncan J ^a   Pearce, Gareth P ^a   Verner Jeffreys, David W ^b   Baker Austin, Craig ^b   Ryan, Jim J ^c  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b CENTRE FOR ENVIRONMENT   (United Kingdom)

^c GLAXOSMITHKLINE   (United Kingdom)

Author keywords

Antimicrobial resistance; Aquatic environment; Metagenomics; Resistome

Indexed keywords

BACTERIA; CATCHMENTS; EFFLUENT TREATMENT; GENES; MICROORGANISMS; RESERVOIRS (WATER); RIVERS; RUNOFF; SULFUR COMPOUNDS;

ANTIMICROBIAL RESISTANCES; AQUATIC ENVIRONMENTS; ENVIRONMENTAL RESERVOIRS; GENETIC ELEMENTS; METAGENOMICS; PATHOGENIC BACTERIUM; RESISTANCE GENES; RESISTOME;

EFFLUENTS;

AMINOGLYCOSIDE; BACTERIAL PROTEIN; DNA; MOBILE GENETIC ELEMENT; SUL2 PROTEIN; SULFANILAMIDE; TETC PROTEIN; TETRACYCLINE; TETW PROTEIN; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; WASTE WATER; WATER POLLUTANT;

ANTIBIOTIC RESISTANCE; ANTIMICROBIAL ACTIVITY; AQUATIC ENVIRONMENT; BACTERIUM; CATCHMENT; COMPARATIVE STUDY; EFFLUENT; ENVIRONMENTAL ASSESSMENT; FARM; GENE; GENOMICS; PATHOGEN; RIVER WATER; WASTE TREATMENT;

ACINETOBACTER; ANTIBIOTIC RESISTANCE; ARCOBACTER BUTZLERI; ARTICLE; BACTERIUM; BUTYRIVIBRIO; CATCHMENT; COMPARATIVE STUDY; EFFLUENT; ESCHERICHIA COLI; EUBACTERIUM RECTALE; GENE IDENTIFICATION; INTEGRON; METAGENOME; METAGENOMICS; MICROBIAL DIVERSITY; MICROORGANISM DETECTION; PROTEUS; PSEUDOMONAS; RIVER; RUMINOCOCCUS BROMII; SALMONELLA ENTERICA; SPHINGOBIUM; TAXONOMY; TRANSPOSON; WASTE WATER MANAGEMENT; CHEMISTRY; DRUG EFFECTS; GENETICS; MICROBIOLOGY; MULTIDRUG RESISTANCE; WASTE WATER; WATER POLLUTANT;

ANTI-BACTERIAL AGENTS; BACTERIA; DRUG RESISTANCE, MULTIPLE, BACTERIAL; METAGENOMICS; RIVERS; WASTE WATER; WATER POLLUTANTS, CHEMICAL;

EID: 84964318929     PISSN: 02731223     EISSN: None     Source Type: Journal    
DOI: 10.2166/wst.2015.634     Document Type: Article

References (48)

1. Bengtsson, J., Hartmann, M., Unterseher, M., Vaishampayan, P., Abarenkov, K., Durso, L., Bik, E. M., Garey, J. R., Eriksson, K. M. & Nilsson, R. H. 2012 Megraft: A software package to graft ribosomal small subunit (16S/18S) fragments onto full-length sequences for accurate species richness and sequencing depth analysis in pyrosequencing-length metagenomes and similar environmental datasets. Research in Microbiology 163 (6-7), 407-412.
2. Bengtsson-Palme, J., Boulund, F., Fick, J., Kristiansson, E. & Larsson, J. 2014 Shotgun metagenomics reveals a wide array of antibiotic resistance genes and mobile elements in a polluted lake in India. Frontiers in Microbiology 15, 648.
3. Bengtsson-Palme, J., Hartmann, M., Eriksson, K. M., Pal, C., Thorell, K., Larsson, D. G. & Nilsson, R. H. 2015 METAXA2: improved identification and taxonomic classification of small and large subunit rRNA in metagenomic data. Molecular Ecology Resources 15 (6), 1403-1414.
4. Berendonk, T. U., Manaia, C. M., Merlin, C., Fatta-Kassinos, D., Cytryn, E., Walsh, F., Burgmann, H., Sorum, H., Norstrom, M., Pons, M.-N., Kreuzinger, N., Huovinen, P., Stefani, S., Schwartz, T., Kisand, V., Baquero, F. & Martinez, J. L. 2015 Tackling antibiotic resistance: The environmental framework. Nature Reviews Microbiology 13 (5), 310-317.
5. Case, R. J., Boucher, Y., Dahllof, I., Holmstrom, C., Doolittle, W. F. & Kjelleberg, S. 2007 Use of 16S rRNA and rpoB genes as molecular markers for microbial ecology studies. Applied and Environmental Microbiology 73 (1), 278-288.
6. Chen, B., Yang, Y., Liang, X., Yu, K., Zhang, T. & Li, X. 2013 Metagenomic profiles of antibiotic resistance genes (ARGs) between human impacted estuary and deep ocean sediments. Environmental Science & Technology 47 (22), 12753-12760.
7. D'Costa, V. M., McGrann, K. M., Hughes, D. W. & Wright, G. D. 2006 Sampling the antibiotic resistome. Science 311 (5759), 374-377.
8. Dancer, D., Baker-Austin, C., Lowther, J. A., Hartnell, R. E., Lees, D. N. & Roberts, L. O. 2014 Development and integration of quantitative real-time PCR methods for detection of mitochondrial DNA and Methanobrevibacter smithii nifH gene as novel microbial source tracking tools. Environmental Forensics 15 (3), 256-264.
9. Dantas, G., Sommer, M. O., Oluwasegun, R. D. & Church, G. M. 2008 Bacteria subsisting on antibiotics. Science 320 (5872), 100-103.
10. Davies, J. & Davies, D. 2010 Origins and evolution of antibiotic resistance. Microbiology and Molecular Biology Reviews: MMBR 74 (3), 417-433.
11. Devarajan, N., Laffite, A., Graham, N. D., Meijer, M., Prabakar, K., Mubedi, J. I., Elongo, V., Mpiana, P. T., Ibelings, B. W., Wildi, W. & Pote, J. 2015 Accumulation of clinically relevant antibiotic-resistance genes, bacterial load, and metals in freshwater lake sediments in central Europe. Environmental Science & Technology 49 (11), 6528-6537.
12. Edgar, R. C. 2010 Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26 (19), 2460-2461.
13. Forsberg, K. J., Reyes, A., Wang, B., Selleck, E. M., Sommer, M. O. A. & Dantas, G. 2012 The shared antibiotic resistome of soil bacteria and human pathogens. Science 337 (6098), 1107-1111.
14. Gaze, W. H., Krone, S. M., Larsson, D. G., Li, X. Z., Robinson, J. A., Simonet, P., Smalla, K., Timinouni, M., Topp, E., Wellington, E. M., Wright, G. D. & Zhu, Y. G. 2013 Influence of humans on evolution and mobilization of environmental antibiotic resistome. Emerging Infectious Disease Journal 19 (7), doi: 10. 3201/eid1907. 120871.
15. Gillespie, J. J., Wattam, A. R., Cammer, S. A., Gabbard, J. L., Shukla, M. P., Dalay, O., Driscoll, T., Hix, D., Mane, S. P., Mao, C., Nordberg, E. K., Scott, M., Schulman, J. R., Snyder, E. E., Sullivan, D. E., Wang, C., Warren, A., Williams, K. P., Xue, T., Seung Yoo, H., Zhang, C., Zhang, Y., Will, R., Kenyon, R. W. &Sobral, B. W. 2011 PATRIC: The comprehensive bacterial bioinformatics resource with a focus on human pathogenic species. Infection and Immunity 79 (11), 4286-4298.
16. Gillings, M. R. 2013 Evolutionary consequences of antibiotic use for the resistome, mobilome and microbial pangenome. Frontiers in Microbiology 4, 4.
17. Gullberg, E., Cao, S., Berg, O. G., Ilback, C., Sandegren, L., Hughes, D. & Andersson, D. I. 2011 Selection of resistant bacteria at very low antibiotic concentrations. PLoS Pathogen 7 (7), e1002158.
18. Gupta, S. K., Padmanabhan, B. R., Diene, S. M., Lopez-Rojas, R., Kempf, M., Landraud, L. & Rolain, J.-M. 2014 ARG-ANNOT, a new bioinformatic tool to discover antibiotic resistance genes in bacterial genomes. Antimicrobial Agents and Chemotherapy 58 (1), 212-220.
19. Harris, S., Cormican, M. & Cummins, E. 2012 The effect of conventional wastewater treatment on the levels of antimicrobial-resistant bacteria in effluent: A meta-analysis of current studies. Environmental Geochemistry and Health 34 (6), 749-762.
20. Hu, X., Zhou, Q. & Luo, Y. 2010 Occurrence and source analysis of typical veterinary antibiotics in manure, soil, vegetables and groundwater from organic vegetable bases, northern China. Environmental Pollution 158 (9), 2992-2998.
21. Kemper, N. 2008 Veterinary antibiotics in the aquatic and terrestrial environment. Ecological Indicators 8 (1), 1-13.
22. Kristiansson, E., Fick, J., Janzon, A., Grabic, R., Rutgersson, C., Weijdegard, B., Soderstrom, H. & Larsson, D. G. J. 2011 Pyrosequencing of antibiotic-contaminated river sediments reveals high levels of resistance and gene transfer elements. PLoS One 6 (2), e17038.
23. LaPara, T. M., Burch, T. R., McNamara, P. J., Tan, D. T., Yan, M. & Eichmiller, J. J. 2011 Tertiary-treated municipal wastewater is a significant point source of antibiotic resistance genes into duluth-superior harbor. Environmental Science & Technology 45 (22), 9543-9549.
24. Larsson, D. G., dePedro, C. & Paxeus, N. 2007 Effluent from drug manufactures contains extremely high levels of pharmaceuticals. Journal of Hazardous Materials 148 (3), 751-755.
25. Laxminarayan, R., Duse, A., Wattal, C., Zaidi, A. K. M., Wertheim, H. F. L., Sumpradit, N., Vlieghe, E., Hara, G. L., Gould, I. M., Goossens, H., Greko, C., So, A. D., Bigdeli, M., Tomson, G., Woodhouse, W., Ombaka, E., Peralta, A. Q., Qamar, F. N., Mir, F., Kariuki, S., Bhutta, Z. A., Coates, A., Bergstrom, R., Wright, G. D., Brown, E. D. & Cars, O. 2013 Antibiotic resistance-the need for global solutions. The Lancet Infectious Diseases 13 (12), 1057-1098.
26. Levy, S. B. & Marshall, B. 2004 Antibacterial resistance worldwide: causes, challenges and responses. Nature Medicine 10 (12 Suppl), S122-S129.
27. Li, H. & Durbin, R. 2009 Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25 (14), 1754-1760.
28. Li, J., Wang, T., Shao, B., Shen, J., Wang, S. & Wu, Y. 2012 Plasmid-mediated quinolone resistance genes and antibiotic residues in wastewater and soil adjacent to swine feedlots: potential transfer to agricultural lands. Environmental Health Perspectives 120 (8), 1144-1149.
29. Li, J., Cheng, W., Xu, L., Strong, P. J. & Chen, H. 2015 Antibiotic-resistant genes and antibiotic-resistant bacteria in the effluent of urban residential areas, hospitals, and a municipal wastewater treatment plant system. Environmental Science and Pollution Research 22 (6), 4587-4596.
30. Linares, J. F., Gustafsson, I., Baquero, F. & Martinez, J. L. 2006 Antibiotics as intermicrobial signaling agents instead of weapons. Proceedings of the National Academy of Sciences of the United States of America 103 (51), 19484-19489.
31. Lu, Z., Na, G., Gao, H., Wang, L., Bao, C. & Yao, Z. 2015 Fate of sulfonamide resistance genes in estuary environment and effect of anthropogenic activities. Science of the Total Environment 527-528C, 429-438.
32. Mather, A. E., Reid, S. W. J., Maskell, D. J., Parkhill, J., Fookes, M. C., Harris, S. R., Brown, D. J., Coia, J. E., Mulvey, M. R., Gilmour, M. W., Petrovska, L., de Pinna, E., Kuroda, M., Akiba, M., Izumiya, H., Connor, T. R., Suchard, M. A., Lemey, P., Mellor, D. J., Haydon, D. T. & Thomson, N. R. 2013 Distinguishable epidemics of multidrug-resistant Salmonella typhimurium DT104 in different hosts. Science 341 (6153), 1514-1517.
33. Moura, A., Soares, M., Pereira, C., Leitao, N., Henriques, I. & Correia, A. N. 2009 INTEGRALL: A database and search engine for integrons, integrases and gene cassettes. Bioinformatics 25 (8), 1096-1098.
34. Phillips, I., Casewell, M., Cox, T., De Groot, B., Friis, C., Jones, R., Nightingale, C., Preston, R. & Waddell, J. 2004 Does the use of antibiotics in food animals pose a risk to human health A critical review of published data. The Journal of Antimicrobial Chemotherapy 53 (1), 28-52.
35. Port, J. A., Cullen, A. C., Wallace, J. C., Smith, M. N. & Faustman, E. M. 2014 Metagenomic frameworks for monitoring antibiotic resistance in aquatic environments. Environmental Health Perspectives 122 (3), 222-228.
36. Pruden, A., Pei, R., Storteboom, H. & Carlson, K. H. 2006 Antibiotic resistance genes as emerging contaminants: studies in northern Colorado. Environmental Science & Technology 40 (23), 7445-7450.
37. Rowe, W., Baker, K. S., Verner-Jeffreys, D., Baker-Austin, C., Ryan, J. J., Maskell, D. & Pearce, G. 2015 Search engine for antimicrobial resistance: A cloud compatible pipeline and web interface for rapidly detecting antimicrobial resistance genes directly from sequence data. PLoS One 10 (7), e0133492.
38. Segata, N. 2014 GraPhlAn. https://bitbucket. org/nsegata/ graphlan/wiki/Home.
39. Segata, N., Izard, J., Waldron, L., Gevers, D., Miropolsky, L., Garrett, W. & Huttenhower, C. 2011 Metagenomic biomarker discovery and explanation. Genome Biology 12 (6), R60.
40. Segata, N., Waldron, L., Ballarini, A., Narasimhan, V., Jousson, O. & Huttenhower, C. 2012 Metagenomic microbial community profiling using unique clade-specific marker genes. Nature Methods 9 (8), 811-814.
41. Tao, R., Ying, G. G., Su, H. C., Zhou, H. W. & Sidhu, J. P. 2010 Detection of antibiotic resistance and tetracycline resistance genes in Enterobacteriaceae isolated from the Pearl rivers in South China. Environmental Pollution 158 (6), 2101-2109.
42. Tsafnat, G., Copty, J. & Partridge, S. R. 2011 RAC: Repository of antibiotic resistance cassettes. Database 2011.
43. Wang, J., Mao, D., Mu, Q. & Luo, Y. 2015 Fate and proliferation of typical antibiotic resistance genes in five full-scale pharmaceutical wastewater treatment plants. Science of the Total Environment 526, 366-373.
44. Wellington, E. M. H., Boxall, A. B. A., Cross, P., Feil, E. J., Gaze, W. H., Hawkey, P. M., Johnson-Rollings, A. S., Jones, D. L., Lee, N. M., Otten, W., Thomas, C. M. & Williams, A. P. 2013 The role of the natural environment in the emergence of antibiotic resistance in Gram-negative bacteria. The Lancet Infectious Diseases 13 (2), 155-165.
45. WHO 2012 The Evolving Threat of Antimicrobial Resistance-Options for Action. WHO (ed.), Geneva, Switzerland.
46. Wright, G. D. 2007 The antibiotic resistome: The nexus of chemical and genetic diversity. Nature reviews. Microbiology 5 (3), 175-186.
47. Zhang, X. X. & Zhang, T. 2011 Occurrence, abundance, and diversity of tetracycline resistance genes in 15 sewage treatment plants across China and other global locations. Environmental Science & Technology 45 (7), 2598-2604.
48. Zhang, X. X., Zhang, T. & Fang, H. H. 2009 Antibiotic resistance genes in water environment. Applied Microbiology and Biotechnology 82 (3), 397-414.