Metagenomic Analysis Revealing Antibiotic Resistance Genes (ARGs) and Their Genetic Compartments in the Tibetan Environment

Environmental Science and Technology

Volumn 50, Issue 13, 2016, Pages 6670-6679

  Chen, Baowei ^a,b   Yuan, Ke ^a   Chen, Xin ^a   Yang, Ying ^a   Zhang, Tong ^c   Wang, Yawei ^d   Luan, Tiangang ^a   Zou, Shichun ^a   Li, Xiangdong ^b  

^a SUN YAT SEN UNIVERSITY   (China)

^b HONG KONG POLYTECHNIC UNIVERSITY   (Hong Kong)

^c UNIVERSITY OF HONG KONG   (Hong Kong)

^d RESEARCH CENTER FOR ECO ENVIRONMENTAL SCIENCES   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AGRICULTURAL WASTES; BACTERIA; CHEMICAL ANALYSIS; GENES; SEDIMENTS;

ANIMAL WASTES; ANTIBIOTIC RESISTANCE; ANTIBIOTIC RESISTANCE GENES; BACTERIAL COMMUNITY STRUCTURE; BETA-LACTAMS; FLUOROQUINOLONES; GENETIC ELEMENTS; METAGENOMIC ANALYSIS;

ANTIBIOTICS;

ANTIBIOTIC AGENT; BETA LACTAM ANTIBIOTIC; QUINOLONE DERIVATIVE; ANTIINFECTIVE AGENT; BETA LACTAM;

ANTHROPOGENIC EFFECT; ANTIBIOTIC RESISTANCE; BACTERIUM; DRUG RESISTANCE; GENETIC ANALYSIS; GENOMICS; MICROBIAL COMMUNITY; PRISTINE ENVIRONMENT;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC RESISTANCE GENE; ARTICLE; BACTERIUM; ENVIRONMENT; GENE; GENETICS; HUMAN; METAGENOMICS; MICROBIAL COMMUNITY; SEDIMENT; SOIL; TIBET; WASTE; ANIMAL; BACTERIAL GENE; DRUG EFFECTS;

CHINA; XIZANG;

ANIMALIA; BACTERIA (MICROORGANISMS);

ANIMALS; ANTI-BACTERIAL AGENTS; BETA-LACTAMS; DRUG RESISTANCE, MICROBIAL; GENES, BACTERIAL; HUMANS; METAGENOMICS;

EID: 84979084828     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/acs.est.6b00619     Document Type: Article

References (69)

1. Rachakonda, S.; Cartee, L. Challenges in antimicrobial drug discovery and the potential of nucleoside antibiotics Curr. Med. Chem. 2004, 11 (6) 775-793 10.2174/0929867043455774
2. Sommer, M. O.; Dantas, G.; Church, G. M. Functional characterization of the antibiotic resistance reservoir in the human microflora Science 2009, 325 (5944) 1128-1131 10.1126/science.1176950
3. Livermore, D. M. Has the era of untreatable infections arrived? J. Antimicrob. Chemother. 2009, 64 (4) 29-36 10.1093/jac/dkp255
4. D'Costa, V. M.; McGrann, K. M.; Hughes, D. W.; Wright, G. D. Sampling the antibiotic resistome Science 2006, 311 (5759) 374-377 10.1126/science.1120800
5. Nathan, C. Antibiotics at the crossroads Nature 2004, 431 (7011) 899-902 10.1038/431899a
6. Wenzel, R. P.; Edmond, M. B. Managing antibiotic resistance N. Engl. J. Med. 2000, 343 (26) 1961-1963 10.1056/NEJM200012283432610
7. Hughes, V. M.; Datta, N. Conjugative Plasmids in Bacteria of the Pre-Antibiotic Era Nature 1983, 302 (5910) 725-726 10.1038/302725a0
8. Davis, C. E.; Anandan, J. Evolution of R Factor. A Study of a Preantibiotic Community in Borneo N. Engl. J. Med. 1970, 282 (3) 117-122 10.1056/NEJM197001152820302
9. Knapp, C. W.; Dolfing, J.; Ehlert, P. A. I.; Graham, D. W. Evidence of Increasing Antibiotic Resistance Gene Abundances in Archived Soils since 1940 Environ. Sci. Technol. 2010, 44 (2) 580-587 10.1021/es901221x
10. Bhullar, K.; Waglechner, N.; Pawlowski, A.; Koteva, K.; Banks, E. D.; Johnston, M. D.; Barton, H. A.; Wright, G. D. Antibiotic Resistance Is Prevalent in an Isolated Cave Microbiome PLoS One 2012, 7 (4) e34953 10.1371/journal.pone.0034953
11. Toth, M.; Smith, C.; Frase, H.; Mobashery, S.; Vakulenko, S. An Antibiotic-Resistance Enzyme from a Deep-Sea Bacterium J. Am. Chem. Soc. 2010, 132 (2) 816-823 10.1021/ja908850p
12. Brown, M. G.; Balkwill, D. L. Antibiotic Resistance in Bacteria Isolated from the Deep Terrestrial Subsurface Microb. Ecol. 2009, 57 (3) 484-493 10.1007/s00248-008-9431-6
13. Newman, D. J.; Cragg, G. M.; Snader, K. M. Natural products as sources of new drugs over the period 1981-2002 J. Nat. Prod. 2003, 66 (7) 1022-1037 10.1021/np030096l
14. Baltz, R. H. Renaissance in antibacterial discovery from actinomycetes Curr. Opin. Pharmacol. 2008, 8 (5) 557-563 10.1016/j.coph.2008.04.008
15. Jang, K. H.; Nam, S. J.; Locke, J. B.; Kauffman, C. A.; Beatty, D. S.; Paul, L. A.; Fenical, W. Anthracimycin, a Potent Anthrax Antibiotic from a Marine-Derived Actinomycete Angew. Chem., Int. Ed. 2013, 52 (30) 7822-7824 10.1002/anie.201302749
16. Dantas, G.; Sommer, M. O. A.; Oluwasegun, R. D.; Church, G. M. Bacteria Subsisting on Antibiotics Science 2008, 320 (5872) 100-103 10.1126/science.1155157
17. Cordero, O. X.; Wildschutte, H.; Kirkup, B.; Proehl, S.; Ngo, L.; Hussain, F.; Le Roux, F.; Mincer, T.; Polz, M. F. Ecological populations of bacteria act as socially cohesive units of antibiotic production and resistance Science 2012, 337 (6099) 1228-1231 10.1126/science.1219385
18. Wright, G. D. The antibiotic resistome: the nexus of chemical and genetic diversity Nat. Rev. Microbiol. 2007, 5 (3) 175-186 10.1038/nrmicro1614
19. D'Costa, V. M.; King, C. E.; Kalan, L.; Morar, M.; Sung, W. W. L.; 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 10.1038/nature10388
20. Xiong, W.; Sun, Y.; Zhang, T.; Ding, X.; Li, Y.; Wang, M.; Zeng, Z. Antibiotics, Antibiotic Resistance Genes, and Bacterial Community Composition in Fresh Water Aquaculture Environment in China Microb. Ecol. 2015, 70 (2) 425-432 10.1007/s00248-015-0583-x
21. 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 10.1016/j.watres.2013.02.042
22. Gootz, T. D. The global problem of antibiotic resistance Crit. Rev. Immunol. 2010, 30 (1) 79-93 10.1615/CritRevImmunol.v30.i1.60
23. Bellanger, X.; Guilloteau, H.; Bonot, S.; Merlin, C. Demonstrating plasmid-based horizontal gene transfer in complex environmental matrices: a practical approach for a critical review Sci. Total Environ. 2014, 493, 872-82 10.1016/j.scitotenv.2014.06.070
24. Elsaied, H.; Stokes, H. W.; Kitamura, K.; Kurusu, Y.; Kamagata, Y.; Maruyama, A. Marine integrons containing novel integrase genes, attachment sites, attI, and associated gene cassettes in polluted sediments from Suez and Tokyo Bays ISME J. 2011, 5 (7) 1162-1177 10.1038/ismej.2010.208
25. Liu, X. B.; Yao, T. D.; Kang, S. C.; Jiao, N. A. Z.; Zeng, Y. H.; Liu, Y. Q. Bacterial Community of the Largest Oligosaline Lake, Namco on the Tibetan Plateau Geomicrobiol. J. 2010, 27 (8) 669-682 10.1080/01490450903528000
26. Wang, J. B.; Zhu, L. P.; Daut, G.; Ju, J. T.; Lin, X.; Wang, Y.; Zhen, X. L. Investigation of bathymetry and water quality of Lake Nam Co, the largest lake on the central Tibetan Plateau, China Limnology 2009, 10 (2) 149-158 10.1007/s10201-009-0266-8
27. Xia, Z. H.; Xu, B. Q.; Mugler, I.; Wu, G. J.; Gleixner, G.; Sachse, D.; Zhu, L. P. Hydrogen isotope ratios of terrigenous n-alkanes in lacustrine surface sediment of the Tibetan Plateau record the precipitation signal Geochem. J. 2008, 42 (4) 331-338 10.2343/geochemj.42.331
28. 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 10.1021/es4017365
29. 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 10.1073/pnas.1222743110
30. 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. 2015, 9 (11) 2490-2502 10.1038/ismej.2015.59
31. Liang, X. M.; Chen, B. W.; Nie, X. P.; Shi, Z.; Huang, X. P.; Li, X. D. The distribution and partitioning of common antibiotics in water and sediment of the Pearl River Estuary, South China Chemosphere 2013, 92 (11) 1410-1416 10.1016/j.chemosphere.2013.03.044
32. Altschul, S. F.; Madden, T. L.; Schaffer, A. A.; Zhang, J.; Zhang, Z.; Miller, W.; Lipman, D. J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs Nucleic Acids Res. 1997, 25 (17) 3389-402 10.1093/nar/25.17.3389
33. Mackelprang, R.; Waldrop, M. P.; DeAngelis, K. M.; David, M. M.; Chavarria, K. L.; Blazewicz, S. J.; Rubin, E. M.; Jansson, J. K. Metagenomic analysis of a permafrost microbial community reveals a rapid response to thaw Nature 2011, 480 (7377) 368-371 10.1038/nature10576
34. Huson, D. H.; Auch, A. F.; Qi, J.; Schuster, S. C. MEGAN analysis of metagenomic data Genome Res. 2007, 17 (3) 377-386 10.1101/gr.5969107
35. Liu, B.; Pop, M. ARDB-Antibiotic Resistance Genes Database Nucleic Acids Res. 2009, 37, D443-D447 10.1093/nar/gkn656
36. Moura, A.; Soares, M.; Pereira, C.; Leitao, N.; Henriques, I.; Correia, A. INTEGRALL: a database and search engine for integrons, integrases and gene cassettes Bioinformatics 2009, 25 (8) 1096-1098 10.1093/bioinformatics/btp105
37. 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 10.1371/journal.pone.0026041
38. Zhang, G.; Niu, F.; Ma, X.; Liu, W.; Dong, M.; Feng, H.; An, L.; Cheng, G. Phylogenetic diversity of bacteria isolates from the Qinghai-Tibet Plateau permafrost region Can. J. Microbiol. 2007, 53 (8) 1000-1010 10.1139/W07-031
39. Yun, J. L.; Ju, Y. W.; Deng, Y. C.; Zhang, H. X. Bacterial Community Structure in Two Permafrost Wetlands on the Tibetan Plateau and Sanjiang Plain, China Microb. Ecol. 2014, 68 (2) 360-369 10.1007/s00248-014-0415-4
40. Rui, J.; Li, J.; Wang, S.; An, J.; Liu, W. T.; Lin, Q.; Yang, Y.; He, Z.; Li, X. Responses of Bacterial Communities to Simulated Climate Changes in Alpine Meadow Soil of the Qinghai-Tibet Plateau Appl. Environ. Microbiol. 2015, 81 (17) 6070-6077 10.1128/AEM.00557-15
41. Jiang, H.; Dong, H.; Yu, B.; Liu, X.; Li, Y.; Ji, S.; Zhang, C. L. Microbial response to salinity change in Lake Chaka, a hypersaline lake on Tibetan plateau Environ. Microbiol. 2007, 9 (10) 2603-2621 10.1111/j.1462-2920.2007.01377.x
42. Liu, Y. Q.; Yao, T. D.; Jiao, N. Z.; Zhu, L. P.; Hu, A. Y.; Liu, X. B.; Gao, J.; Chen, Z. Q. Salinity Impact on Bacterial Community Composition in Five High-Altitude Lakes from the Tibetan Plateau, Western China Geomicrobiol. J. 2013, 30 (5) 462-469 10.1080/01490451.2012.710709
43. Tan, H. M.; Deng, Q. L.; Cao, L. X. Ruminant feces harbor diverse uncultured symbiotic actinobacteria World J. Microbiol. Biotechnol. 2014, 30 (3) 1093-1100 10.1007/s11274-013-1529-4
44. 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 10.1021/es403818e
45. Munck, C.; Albertsen, M.; Telke, A.; Ellabaan, M.; Nielsen, P. H.; Sommer, M. O. Limited dissemination of the wastewater treatment plant core resistome Nat. Commun. 2015, 6, 8452 10.1038/ncomms9452
46. Wright, G. D. The antibiotic resistome: the nexus of chemical and genetic diversity Nat. Rev. Microbiol. 2007, 5 (3) 175-186 10.1038/nrmicro1614
47. Fredrickson, J. K.; Garland, T. R.; Hicks, R. J.; Thomas, J. M.; Li, S. W.; Mcfadden, K. M. Lithotrophic and heterotrophic bacteria in deep subsurface sediments and their relation to sediment properties Geomicrobiol. J. 1989, 7 (1-2) 53-66 10.1080/01490458909377849
48. Zhang, X. X.; Zhang, T.; Fang, H. H. Antibiotic resistance genes in water environment Appl. Microbiol. Biotechnol. 2009, 82 (3) 397-414 10.1007/s00253-008-1829-z
49. Li, X. Z.; Plesiat, P.; Nikaido, H. The Challenge of Efflux-Mediated Antibiotic Resistance in Gram-Negative Bacteria Clin. Microbiol. Rev. 2015, 28 (2) 337-418 10.1128/CMR.00117-14
50. Bellido, J. L. M.; Guirao, G. Y.; Zufiaurre, N. G.; Manzanares, A. A. Efflux-mediated antibiotic resistance in Gram-positive bacteria Rev. Med. Microbiol. 2002, 13 (1) 1-13 10.1097/00013542-200201000-00001
51. Silver, S. Bacterial resistances to toxic metal ions - a review Gene 1996, 179 (1) 9-19 10.1016/S0378-1119(96)00323-X
52. Ryan, B. M.; Dougherty, T. J.; Beaulieu, D.; Chuang, J.; Dougherty, B. A.; Barrett, J. F. Efflux in bacteria: what do we really know about it? Expert Opin. Invest. Drugs 2001, 10 (8) 1409-1422 10.1517/13543784.10.8.1409
53. Taylor, D. L.; Bina, X. W. R.; Bina, J. E. Vibrio cholerae vexH Encodes a Multiple Drug Efflux Pump That Contributes to the Production of Cholera Toxin and the Toxin Co-Regulated Pilus PLoS One 2012, 7 (5) e38208 10.1371/journal.pone.0038208
54. El Ghachi, M.; Bouhss, A.; Blanot, D.; Mengin-Lecreulx, D. The bacA gene of Escherichia coli encodes an undecaprenyl pyrophosphate phosphatase activity J. Biol. Chem. 2004, 279 (29) 30106-30113 10.1074/jbc.M401701200
55. Su, J. Q.; Wei, B.; Ou-Yang, W. Y.; Huang, F. Y.; Zhao, Y.; Xu, H. J.; Zhu, Y. G. Antibiotic Resistome and Its Association with Bacterial Communities during Sewage Sludge Composting Environ. Sci. Technol. 2015, 49 (12) 7356-7363 10.1021/acs.est.5b01012
56. Wu, D.; Huang, Z. T.; Yang, K.; Graham, D.; Xie, B. Relationships between Antibiotics and Antibiotic Resistance Gene Levels in Municipal Solid Waste Leachates in Shanghai, China Environ. Sci. Technol. 2015, 49 (7) 4122-4128 10.1021/es506081z
57. Martinez-Rosales, C.; Fullana, N.; Musto, H.; Castro-Sowinski, S. Antarctic DNA moving forward: genomic plasticity and biotechnological potential FEMS Microbiol. Lett. 2012, 331 (1) 1-9 10.1111/j.1574-6968.2012.02531.x
58. Beuls, E.; Modrie, P.; Deserranno, C.; Mahillon, J. High-Salt Stress Conditions Increase the pAW63 Transfer Frequency in Bacillus thuringiensis Appl. Environ. Microbiol. 2012, 78 (19) 7128-7131 10.1128/AEM.01105-12
59. Yang, X. W.; Jian, H. H.; Wang, F. P. pSW2, a Novel Low-Temperature-Inducible Gene Expression Vector Based on a Filamentous Phage of the Deep-Sea Bacterium Shewanella piezotolerans WP3 Appl. Environ. Microbiol. 2015, 81 (16) 5519-5526 10.1128/AEM.00906-15
60. Luo, Y.; Mao, D. Q.; Rysz, M.; Zhou, D. X.; Zhang, H. J.; Xu, L.; Alvarez, P. J. J. Trends in Antibiotic Resistance Genes Occurrence in the Haihe River, China Environ. Sci. Technol. 2010, 44 (19) 7220-7225 10.1021/es100233w
61. Chen, B. W.; Liang, X. M.; Nie, X. P.; Huang, X.; Zou, S. C.; Li, X. D. The role of class I integrons in the dissemination of sulfonamide resistance genes in the Pearl River and Pearl River Estuary, South China J. Hazard. Mater. 2015, 282, 61-67 10.1016/j.jhazmat.2014.06.010
62. Di Conza, J. A.; Gutkind, G. O. [Integrons: gene collectors] Rev. Argent Microbiol. 2010, 42 (1) 63-78
63. Shah, S. Q. A.; Colquhoun, D. J.; Nikuli, H. L.; Sorum, H. Prevalence of Antibiotic Resistance Genes in the Bacterial Flora of Integrated Fish Farming Environments of Pakistan and Tanzania Environ. Sci. Technol. 2012, 46 (16) 8672-8679 10.1021/es3018607
64. Yan, H.; Li, L.; Zong, M. H.; Alam, M. J.; Shinoda, S.; Shi, L. Occurrence and Characteristics of Class 1 and 2 Integrons in Clinical Bacterial Isolates from Patients in South China J. Health Sci. 2010, 56 (4) 442-450 10.1248/jhs.56.442
65. Ndi, O. L.; Barton, M. D. Incidence of class 1 integron and other antibiotic resistance determinants in Aeromonas spp. from rainbow trout farms in Australia J. Fish Dis. 2011, 34 (8) 589-599 10.1111/j.1365-2761.2011.01272.x
66. Wright, M. S.; Baker-Austin, C.; Lindell, A. H.; Stepanauskas, R.; Stokes, H. W.; McArthur, J. V. Influence of industrial contamination on mobile genetic elements: class 1 integron abundance and gene cassette structure in aquatic bacterial communities ISME J. 2008, 2 (4) 417-428 10.1038/ismej.2008.8
67. Partridge, S. R.; Tsafnat, G.; Coiera, E.; Iredell, J. R. Gene cassettes and cassette arrays in mobile resistance integrons FEMS Microbiol. Rev. 2009, 33 (4) 757-784 10.1111/j.1574-6976.2009.00175.x
68. Cytryn, E. The soil resistome: The anthropogenic, the native, and the unknown Soil Biol. Biochem. 2013, 63, 18-23 10.1016/j.soilbio.2013.03.017
69. Fredrickson, J. K.; Hicks, R. J.; Li, S. W.; Brockman, F. J. Plasmid incidence in bacteria from deep subsurface sediments Appl. Environ. Microbiol. 1988, 54 (12) 2916-2923