Untreated urban waste contaminates Indian river sediments with resistance genes to last resort antibiotics

Water Research

Volumn 124, Issue , 2017, Pages 388-397

  Marathe, Nachiket P ^a,b   Pal, Chandan ^a,b,e   Gaikwad, Swapnil S ^c   Jonsson, Viktor ^b,d   Kristiansson, Erik ^b,d   Larsson, D G Joakim ^a,b  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

^c UNIVERSITY OF PUNE   (India)

^d CHALMERS UNIVERSITY OF TECHNOLOGY   (Sweden)

^e Ministry for Primary Industries   (New Zealand)

Author keywords

Acinetobacter; Antibiotic resistance; Carbapenemase; India; mcr 1; NDM; River sediments

Indexed keywords

ANTIBIOTICS; BACTERIA; BIOMARKERS; RIVERS; RNA; SEDIMENTS; SEWAGE TREATMENT; WASTEWATER TREATMENT;

ACINETOBACTERS; ANTIBIOTIC RESISTANCE; CARBAPENEMASE; INDIA; MCR-1; RIVER SEDIMENTS;

GENES;

AMINOGLYCOSIDE DERIVATIVE; ANTIBIOTIC AGENT; BETA LACTAM DERIVATIVE; CARBAPENEMASE; CHLORAMPHENICOL; MACROLIDE; SULFONAMIDE; TETRACYCLINE DERIVATIVE; TIGECYCLINE; TRIMETHOPRIM DERIVATIVE; ANTIINFECTIVE AGENT; RNA 16S;

ABUNDANCE; ANTIBIOTIC RESISTANCE; ANTIBIOTICS; BACTERIUM; DISCHARGE; FLUVIAL DEPOSIT; GENE; GENOMICS; MICROBIAL COMMUNITY; SEWAGE TREATMENT; SPECIES DIVERSITY; TOXIN; URBAN AREA; VIRULENCE; WASTE;

ACINETOBACTER; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL VIRULENCE; CONTROLLED STUDY; METAGENOME; METAGENOMICS; MICROBIAL COMMUNITY; NONHUMAN; PRIORITY JOURNAL; RIVER; SEDIMENT; WATER CONTAMINATION; WATER QUALITY; BACTERIAL GENE; CITY; CROSS INFECTION; ENVIRONMENTAL MONITORING; GENETICS; INDIA; WATER SUPPLY;

INDIA; MAHARASHTRA; PUNE;

ACINETOBACTER; BACTERIA (MICROORGANISMS);

ANTI-BACTERIAL AGENTS; CITIES; CROSS INFECTION; DRUG RESISTANCE, MICROBIAL; ENVIRONMENTAL MONITORING; GENES, BACTERIAL; GEOLOGIC SEDIMENTS; INDIA; RIVERS; RNA, RIBOSOMAL, 16S; WATER SUPPLY;

EID: 85026733733     PISSN: 00431354     EISSN: 18792448     Source Type: Journal    
DOI: 10.1016/j.watres.2017.07.060     Document Type: Article

References (76)

1. Ahammad, Z.S., Sreekrishnan, T.R., Hands, C.L., Knapp, C.W., Graham, D.W., Increased waterborne blaNDM-1 resistance gene abundances associated with seasonal human pilgrimages to the upper ganges river. Environ. Sci. Technol. 48:5 (2014), 3014–3020.
2. Ames, S.K., Gardner, S.N., Marti, J.M., Slezak, T.R., Gokhale, M.B., Allen, J.E., Using populations of human and microbial genomes for organism detection in metagenomes. Genome Res. 25:7 (2015), 1056–1067.
3. Amini, S., Tavazoie, S., Antibiotics and the post-genome revolution. Curr. Opin. Microbiol. 14:5 (2011), 513–518.
4. Aminov, R.I., Evolution in action: dissemination of tet(X) into pathogenic microbiota. Front. Microbiol., 4, 2013, 192.
5. Bengtsson-Palme, J., Boulund, F., Fick, J., Kristiansson, E., Larsson, D.G.J., Shotgun metagenomics reveals a wide array of antibiotic resistance genes and mobile elements in a polluted lake in India. Front. Microbiol., 5, 2014, 648.
6. Bengtsson-Palme, J., Angelin, M., Huss, M., Kjellqvist, S., Kristiansson, E., Palmgren, H., Larsson, D.G.J., Johansson, A., The human gut microbiome as a transporter of antibiotic resistance genes between continents. Antimicrob. Agents Chemother. 59:10 (2015), 6551–6560.
7. Bengtsson-Palme, J., Hartmann, M., Eriksson, K.M., Pal, C., Thorell, K., Larsson, D.G.J., Nilsson, R.H., METAXA2: improved identification and taxonomic classification of small and large subunit rRNA in metagenomic data. Mol. Ecol. Resour. 15:6 (2015), 1403–1414.
8. Bengtsson-Palme, J., Hammaren, R., Pal, C., Ostman, M., Bjorlenius, B., Flach, C.F., Fick, J., Kristiansson, E., Tysklind, M., Larsson, D.G.J., Elucidating selection processes for antibiotic resistance in sewage treatment plants using metagenomics. Sci. Total Environ. 572 (2016), 697–712.
9. Bengtsson-Palme, J., Larsson, D.G.J., Kristiansson, E., Using metagenomics to investigate human and environmental resistomes. J. Antimicrob. Chemother., 2017, 10.1093/jac/dkx199 (published ahead of print).
10. Benjamini, Y., Hochberg, Y., Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the royal statistical society. Ser. B Methodol., 1995, 289–300.
11. 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., Tackling antibiotic resistance: the environmental framework. Nat. Rev. Microbiol. 13:5 (2015), 310–317.
12. Cerqueira, G.C., Earl, A.M., Ernst, C.M., Grad, Y.H., Dekker, J.P., Feldgarden, M., Chapman, S.B., Reis-Cunha, J.L., Shea, T.P., Young, S., Zeng, Q., Delaney, M.L., Kim, D., Peterson, E.M., O'Brien, T.F., Ferraro, M.J., Hooper, D.C., Huang, S.S., Kirby, J.E., Onderdonk, A.B., Birren, B.W., Hung, D.T., Cosimi, L.A., Wortman, J.R., Murphy, C.I., Hanage, W.P., Multi-institute analysis of carbapenem resistance reveals remarkable diversity, unexplained mechanisms, and limited clonal outbreaks. Proc. Natl. Acad. Sci. U. S. A. 114:5 (2017), 1135–1140.
13. Chapman, J.S., Disinfectant resistance mechanisms, cross-resistance, and co-resistance. Int. Biodeterior. Biodegrad. 51:4 (2003), 271–276.
14. 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. 47:22 (2013), 12753–12760.
15. Chen, L., Zheng, D., Liu, B., Yang, J., Jin, Q., VFDB 2016: hierarchical and refined dataset for big data analysis—10 years on. Nucleic acids Res. 44:D1 (2016), D694–D697.
16. Corcoran, E., Sick Water?: the Central Role of Wastewater Management in Sustainable Development: a Rapid Response Assessment. 2010, UNEP/Earthprint.
17. D'Onorio de Meo, P., D'Antonio, M., Griggio, F., Lupi, R., Borsani, M., Pavesi, G., Castrignano, T., Pesole, G., Gissi, C., MitoZoa 2.0: a database resource and search tools for comparative and evolutionary analyses of mitochondrial genomes in Metazoa. Nucleic Acids Res. 40:Database issue (2012), D1168–D1172.
18. Edgar, R.C., Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:19 (2010), 2460–2461.
19. Falagas, M.E., Lourida, P., Poulikakos, P., Rafailidis, P.I., Tansarli, G.S., Antibiotic treatment of infections due to carbapenem-resistant Enterobacteriaceae: systematic evaluation of the available evidence. Antimicrob. Agents Chemother. 58:2 (2014), 654–663.
20. Fu, Y., Du, X., Ji, J., Chen, Y., Jiang, Y., Yu, Y., Epidemiological characteristics and genetic structure of blaNDM-1 in non-baumannii Acinetobacter spp. in China. J. Antimicrob. Chemother., 2012, dks192.
21. Gaze, W.H., Zhang, L., Abdouslam, N.A., Hawkey, P.M., Calvo-Bado, L., Royle, J., Brown, H., Davis, S., Kay, P., Boxall, A.B., Wellington, E.M., Impacts of anthropogenic activity on the ecology of class 1 integrons and integron-associated genes in the environment. ISME J. 5:8 (2011), 1253–1261.
22. Gelband, H., Miller-Petrie, M., Pant, S., Gandra, S., Levinson, J., Barter, D., White, A., Laxminarayan, R., Ganguly, N., Kariuki, S., The state of the World's antibiotics 2015. Wound Heal. South. Afr. 8:2 (2015), 30–34.
23. Gilbert, J.A., de Vries, L.E., Vallès, Y., Agersø, Y., Vaishampayan, P.A., García-Montaner, A., Kuehl, J.V., Christensen, H., Barlow, M., Francino, M.P., The gut as reservoir of antibiotic resistance: microbial diversity of tetracycline resistance in mother and infant. PLoS One, 6(6), 2011, e21644.
24. Graham, D.W., Collignon, P., Davies, J., Larsson, D.G.J., Snape, J., Underappreciated role of regionally poor water quality on globally increasing antibiotic resistance. Environ. Sci. Technol. 48:20 (2014), 11746–11747.
25. Heilig, G.K., World Urbanization Prospects the 2011 Revision. 2012, United Nations, Department of Economic and Social Affairs (DESA), Population Division, Population Estimates and Projections Section, New York.
26. Hrenovic, J., Goic-Barisic, I., Kazazic, S., Kovacic, A., Ganjto, M., Tonkic, M., Carbapenem-resistant isolates of Acinetobacter baumannii in a municipal wastewater treatment plant, Croatia, 2014. Euro Surveill., 21(15), 2016.
27. Johnson, A.P., Woodford, N., Global spread of antibiotic resistance: the example of New Delhi metallo-beta-lactamase (NDM)-mediated carbapenem resistance. J. Med. Microbiol. 62:Pt 4 (2013), 499–513.
28. Jones, L.S., Carvalho, M.J., Toleman, M.A., White, P.L., Connor, T.R., Mushtaq, A., Weeks, J.L., Kumarasamy, K.K., Raven, K.E., Torok, M.E., Peacock, S.J., Howe, R.A., Walsh, T.R., Characterization of plasmids in extensively drug-resistant acinetobacter strains isolated in India and Pakistan. Antimicrob. Agents Chemother. 59:2 (2015), 923–929.
29. Jonsson, V., Österlund, T., Nerman, O., Kristiansson, E., Variability in metagenomic count data and its influence on the identification of differentially abundant genes. J. Comput. Biol. 24:4 (2017), 311–326.
30. Khajuria, A., Praharaj, A.K., Kumar, M., Grover, N., Molecular characterization of carbapenem resistant isolates of acinetobacter baumannii in an intensive care unit of a tertiary care centre at central India. J. Clin. Diagn. Res. 8:5 (2014), DC38–40.
31. Kumar, M., Saha, S., Subudhi, E., More furious than ever: Escherichia coli-Acquired Co-resistance toward colistin and carbapenems. Clin. Infect. Dis., 2016, ciw508.
32. Kummerer, K., Resistance in the environment. J. Antimicrob. Chemother. 54:2 (2004), 311–320.
33. LaPara, T.M., Burch, T.R., McNamara, P.J., Tan, D.T., Yan, M., Eichmiller, J.J., Tertiary-treated municipal wastewater is a significant point source of antibiotic resistance genes into duluth-superior harbor. Environ. Sci. Technol. 45:22 (2011), 9543–9549.
34. Laxminarayan, R., Chaudhury, R.R., Antibiotic resistance in India: drivers and opportunities for action. PLoS Med., 13(3), 2016, e1001974.
35. Leski, T.A., Bangura, U., Jimmy, D.H., Ansumana, R., Lizewski, S.E., Li, R.W., Stenger, D.A., Taitt, C.R., Vora, G.J., Identification of blaOXA-51-like, blaOXA-58, blaDIM-1, and blaVIM carbapenemase genes in hospital Enterobacteriaceae isolates from Sierra Leone. J. Clin. Microbiol. 51:7 (2013), 2435–2438.
36. Leski, T.A., Bangura, U., Jimmy, D.H., Ansumana, R., Lizewski, S.E., Stenger, D.A., Taitt, C.R., Vora, G.J., Multidrug-resistant tet(X)-containing hospital isolates in Sierra Leone. Int. J. Antimicrob. Agents 42:1 (2013), 83–86.
37. Li, D., Yu, T., Zhang, Y., Yang, M., Li, Z., Liu, M., Qi, R., Antibiotic resistance characteristics of environmental bacteria from an oxytetracycline production wastewater treatment plant and the receiving river. Appl. Environ. Microbiol. 76:11 (2010), 3444–3451.
38. Li, B., Yang, Y., Ma, L., Ju, F., Guo, F., Tiedje, J.M., Zhang, T., Metagenomic and network analysis reveal wide distribution and co-occurrence of environmental antibiotic resistance genes. ISME J. 9:11 (2015), 2490–2502.
39. Liu, M., Zhang, Y., Yang, M., Tian, Z., Ren, L., Zhang, S., Abundance and distribution of tetracycline resistance genes and mobile elements in an oxytetracycline production wastewater treatment system. Environ. Sci. Technol. 46:14 (2012), 7551–7557.
40. Liu, Y.-Y., Wang, Y., Walsh, T.R., Yi, L.-X., Zhang, R., Spencer, J., Doi, Y., Tian, G., Dong, B., Huang, X., Yu, L.-F., Gu, D., Ren, H., Chen, X., Lv, L., He, D., Zhou, H., Liang, Z., Liu, J.-H., Shen, J., 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. 16:2 (2016), 161–168.
41. MacConkey, A., Lactose-fermenting bacteria in faeces. J. Hyg. 5:03 (1905), 333–379.
42. Marathe, N., Shetty, S., Lanjekar, V., Ranade, D., Shouche, Y., Changes in human gut flora with age: an Indian familial study. BMC Microbiol., 12(1), 2012, 1.
43. Marathe, N.P., Regina, V.R., Walujkar, S.A., Charan, S.S., Moore, E.R.B., Larsson, D.G.J., Shouche, Y.S., A treatment plant receiving waste water from multiple bulk drug manufacturers is a reservoir for highly multi-drug resistant integron-bearing bacteria. PLoS One, 8(10), 2013, e77310.
44. Marti, E., Jofre, J., Balcazar, J.L., Prevalence of antibiotic resistance genes and bacterial community composition in a river influenced by a wastewater treatment plant. PLoS One, 8(10), 2013, e78906.
45. Martinez, J.L., Environmental pollution by antibiotics and by antibiotic resistance determinants. Environ. Pollut. 157:11 (2009), 2893–2902.
46. Martínez, J.L., Coque, T.M., Baquero, F., What is a resistance gene? Ranking risk in resistomes. Nat. Rev. Microbiol. 13:2 (2015), 116–123.
47. Mossel, D., Mengerink, W., Scholts, H., Use of a modified MacConkey agar medium for the selective growth and enumeration of Enterobacteriaceae. J. Bacteriol., 84(2), 1962, 381.
48. Narain, S.P.P., Banerjee, S., Chaudhuri, J., Excreta Matters: How Urban India Is Soaking up Water, Polluting Rivers and Drowning in its Own Waste. 2012, Centre for Science and Environment, India, New Delhi.
49. Oksanen, J., Kindt, R., Legendre, P., O'Hara, B., Stevens, M.H.H., Oksanen, M.J., Suggests, M., The vegan package. Community Ecol. Package, 10, 2007.
50. Olaitan, A.O., Morand, S., Rolain, J.M., Mechanisms of polymyxin resistance: acquired and intrinsic resistance in bacteria. Front. Microbiol., 5, 2014, 643.
51. Pal, C., Bengtsson-Palme, J., Rensing, C., Kristiansson, E., Larsson, D.G.J., BacMet: antibacterial biocide and metal resistance genes database. Nucleic Acids Res. 42:Database issue (2014), D737–D743.
52. Pal, C., Bengtsson-Palme, J., Kristiansson, E., Larsson, D.G.J., Co-occurrence of resistance genes to antibiotics, biocides and metals reveals novel insights into their co-selection potential. BMC Genomics, 16(1), 2015, 964.
53. Pal, C., Bengtsson-Palme, J., Kristiansson, E., Larsson, D.G.J., The structure and diversity of human, animal and environmental resistomes. Microbiome, 4(1), 2016, 54.
54. Patwardhan, R., Dhakephalkar, P., Niphadkar, K., Chopade, B., A study on nosocomial pathogens in ICU with special reference to multiresistant Acinetobacter baumannii harbouring multiple plasmids. Indian J. Med. Res., 128(2), 2008, 178.
55. Picão, R.C., Cardoso, J.P., Campana, E.H., Nicoletti, A.G., Petrolini, F.V., Assis, D.M., Juliano, L., Gales, A.C., The route of antimicrobial resistance from the hospital effluent to the environment: focus on the occurrence of KPC-producing Aeromonas spp. and Enterobacteriaceae in sewage. Diagn. Microbiol. Infect. Dis. 76:1 (2013), 80–85.
56. Pradhan, N.P., Bhat, S., Ghadage, D., Nosocomial infections in the medical ICU: a retrospective study highlighting their prevalence, microbiological profile and impact on ICU stay and mortality. J. Assoc. Phys. India 62:10 (2014), 18–21.
57. Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J., Glockner, F.O., The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41:Database issue (2013), D590–D596.
58. Queenan, A.M., Bush, K., Carbapenemases: the versatile beta-lactamases. Clin. Microbiol. Rev. 20:3 (2007), 440–458 table of contents.
59. 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. 447 (2013), 345–360.
60. Rodriguez-Mozaz, S., Chamorro, S., Marti, E., Huerta, B., Gros, M., Sanchez-Melsio, A., Borrego, C.M., Barcelo, D., Balcazar, J.L., Occurrence of antibiotics and antibiotic resistance genes in hospital and urban wastewaters and their impact on the receiving river. Water Res. 69 (2015), 234–242.
61. Seiler, C., Berendonk, T.U., Heavy metal driven co-selection of antibiotic resistance in soil and water bodies impacted by agriculture and aquaculture. Front. Microbiol., 3, 2012, 399.
62. Sidrach-Cardona, R., Hijosa-Valsero, M., Marti, E., Balcazar, J.L., Becares, E., Prevalence of antibiotic-resistant fecal bacteria in a river impacted by both an antibiotic production plant and urban treated discharges. Sci. Total Environ. 488–489 (2014), 220–227.
63. Skov, R., Monnet, D., Plasmid-mediated colistin resistance (mcr-1 gene): three months later, the story unfolds. Euro Surveill., 21(9), 2016, 30155.
64. Tacao, M., Correia, A., Henriques, I.S., Low prevalence of carbapenem-resistant bacteria in river water: resistance is mostly related to intrinsic mechanisms. Microb. Drug Resist. 21:5 (2015), 497–506.
65. Thi Khanh Nhu, N., Riordan, D.W., Do Hoang Nhu, T., Thanh, D.P., Thwaites, G., Huong Lan, N.P., Wren, B.W., Baker, S., Stabler, R.A., The induction and identification of novel Colistin resistance mutations in Acinetobacter baumannii and their implications. Sci. Rep., 6, 2016, 28291.
66. Visca, P., Seifert, H., Towner, K.J., Acinetobacter infection–an emerging threat to human health. IUBMB Life 63:12 (2011), 1048–1054.
67. Walsh, T.R., Weeks, J., Livermore, D.M., Toleman, M.A., Dissemination of NDM-1 positive bacteria in the New Delhi environment and its implications for human health: an environmental point prevalence study. Lancet Infect. Dis. 11:5 (2011), 355–362.
68. Walther-Rasmussen, J., Hoiby, N., OXA-type carbapenemases. J. Antimicrob. Chemother. 57:3 (2006), 373–383.
69. Warnes, G.R., Bolker, B., Bonebakker, L., Gentleman, R., Huber, W., Liaw, A., Lumley, T., Maechler, M., Magnusson, A., Moeller, S., gplots: Various R Programming Tools for Plotting Data. 2009 R package version 2(4).
70. 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., The role of the natural environment in the emergence of antibiotic resistance in Gram-negative bacteria. Lancet Infect. Dis. 13:2 (2013), 155–165.
71. Wright, G.D., Antibiotic resistance in the environment: a link to the clinic?. Curr. Opin. Microbiol. 13:5 (2010), 589–594.
72. Xavier, B., Lammens, C., Ruhal, R., Kumar-Singh, S., Butaye, P., Goossens, H., Malhotra-Kumar, S., Identification of a novel plasmid-mediated colistin-resistance gene, mcr-2, in Escherichia coli, Belgium, June 2016. Euro Surveill. Bull. Européen les Mal. Transm. Eur. Commun. Dis. Bull., 21(27), 2016.
73. Xin, F., Cai, D., Sun, Y., Guo, D., Wu, Z., Jiang, D., Exploring the diversity of Acinetobacter populations in river water with genus-specific primers and probes. J. General Appl. Microbiol. 60:2 (2014), 51–58.
74. Yang, W., Moore, I.F., Koteva, K.P., Bareich, D.C., Hughes, D.W., Wright, G.D., TetX is a flavin-dependent monooxygenase conferring resistance to tetracycline antibiotics. J. Biol. Chem. 279:50 (2004), 52346–52352.
75. Zhang, Y., Marrs, C.F., Simon, C., Xi, C., Wastewater treatment contributes to selective increase of antibiotic resistance among Acinetobacter spp. Sci. Total Environ. 407:12 (2009), 3702–3706.
76. Zurfuh, K., Poirel, L., Nordmann, P., Nüesch-Inderbinen, M., Hächler, H., Stephan, R., Occurrence of the plasmid-borne mcr-1 colistin resistance gene in extended-spectrum-β-lactamase-producing Enterobacteriaceae in river water and imported vegetable samples in Switzerland. Antimicrob. Agents Chemother. 60:4 (2016), 2594–2595.