Metagenomic profiles of antibiotic resistance genes (ARGs) between human impacted estuary and deep ocean sediments

Environmental Science and Technology

Volumn 47, Issue 22, 2013, Pages 12753-12760

  Chen, Baowei ^a   Yang, Ying ^b   Liang, Ximei ^c   Yu, Ke ^b   Zhang, Tong ^b   Li, Xiangdong ^a  

^a HONG KONG POLYTECHNIC UNIVERSITY   (Hong Kong)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

^c SOUTH CHINA SEA INSTITUTE OF OCEANOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANTHROPOGENIC IMPACTS; ANTIBIOTIC RESISTANCE GENES; AQUATIC ENVIRONMENTS; DEEP OCEAN SEDIMENTS; ENVIRONMENTAL STRESS; PRISTINE ENVIRONMENTS; RESISTANCE MECHANISMS; RESISTANCE TO ANTIBIOTICS;

AMIDES; ANTIBIOTICS; METABOLITES; SULFUR COMPOUNDS;

SEDIMENTS;

AMINOGLYCOSIDE ANTIBIOTIC AGENT; ANTIBIOTIC AGENT; ANTIBIOTIC RESISTANCE PROTEIN; BETA LACTAM; ERYTHROMYCIN; FOSFOMYCIN; FOSMIDOMYCIN; GENOMIC DNA; LACTAM; NORFLOXACIN; OFLOXACIN; POLYPEPTIDE ANTIBIOTIC AGENT; PROTEIN; QUINOLINE DERIVED ANTIINFECTIVE AGENT; SULFADIMIDINE; SULFONAMIDE; TETRACYCLINE; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; TRANSPOSON;

ABUNDANCE; ANTHROPOGENIC EFFECT; ANTIBIOTIC RESISTANCE; CORRELATION; GENE; GENOTYPE; PRISTINE ENVIRONMENT; SEDIMENT CHEMISTRY;

ANTIBIOTIC RESISTANCE; ARTICLE; CHEMICAL ANALYSIS; CONCENTRATION (PARAMETERS); ESTUARY; GENOTYPE; HIGH THROUGHPUT SEQUENCING; INTEGRON; METAGENOMICS; PLASMID; SEA; SEDIMENT; WATER ANALYSIS; WATER CONTAMINATION; ANIMAL; BACTERIAL GENE; CHINA; DRUG EFFECTS; GENETIC VARIABILITY; GENETICS; GEOGRAPHY; HUMAN; HUMAN ACTIVITIES; MICROBIOLOGY; TRANSPOSON;

PACIFIC OCEAN; SOUTH CHINA SEA;

ANIMALS; ANTI-BACTERIAL AGENTS; CHINA; DNA TRANSPOSABLE ELEMENTS; DRUG RESISTANCE, MICROBIAL; ESTUARIES; GENES, BACTERIAL; GENETIC VARIATION; GENOTYPE; GEOGRAPHY; GEOLOGIC SEDIMENTS; HUMAN ACTIVITIES; HUMANS; METAGENOMICS; OCEANS AND SEAS;

EID: 84888224383     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/es403818e     Document Type: Article

References (70)

1. Sommer, M. O.; Dantas, G.; Church, G. M. Functional characterization of the antibiotic resistance reservoir in the human microflora Science 2009, 325 (5944) 1128-31
2. Livermore, D. M. Has the era of untreatable infections arrived? J. Antimicrob. Chemoth. 2009, 64 (4) 29-36
3. D'Costa, V. M.; McGrann, K. M.; Hughes, D. W.; Wright, G. D. Sampling the antibiotic resistome Science 2006, 311 (5759) 374-377
4. Forsberg, K. J.; Reyes, A.; Bin, W.; Selleck, E. M.; Sommer, M. O. A.; Dantas, G. The shared antibiotic resistome of soil bacteria and human pathogens Science 2012, 337 (6098) 1107-1111
5. Baltz, R. H. Renaissance in antibacterial discovery from actinomycetes Curr. Opin. Pharmacol. 2008, 8 (5) 557-563
6. Dantas, G.; Sommer, M. O. A.; Oluwasegun, R. D.; Church, G. M. Bacteria subsisting on antibiotics Science 2008, 320 (5872) 100-103
7. 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) 1228-31
8. Wright, G. D. The antibiotic resistome: the nexus of chemical and genetic diversity Nat. Rev. Microbiol. 2007, 5 (3) 175-186
9. Wright, G. D. The antibiotic resistome Expert. Opin. Drug. Dis. 2010, 5 (8) 779-788
10. 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
11. 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
12. 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
13. Brown, M. G.; Balkwill, D. L. Antibiotic resistance in bacteria isolated from the deep terrestrial subsurface Microbial. Ecol. 2009, 57 (3) 484-493
14. Hughes, V. M.; Datta, N. Conjugative plasmids in bacteria of the pre-antibiotic era Nature 1983, 302 (5910) 725-726
15. Davis, C. E.; Anandan, J. Evolution of R factor. A study of a preantibiotic community in Borneo New. Engl. J. Med. 1970, 282 (3) 117-122
16. Thaller, M. C.; Migliore, L.; Marquez, C.; Tapia, W.; Cedeno, V.; Rossolini, G. M.; Gentile, G. Tracking acquired antibiotic resistance in commensal bacteria of Galápagos Land Iguanas: No man, no resistance PLoS One 2010, 5 (2) e8989
17. 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
18. Durso, L. M.; Miller, D. N.; Wienhold, B. J. Distribution and quantification of antibiotic resistant genes and bacteria across agricultural and non-agricultural metagenomes PLoS One 2012, 7 (11) e48325
19. Port, J. A.; Wallace, J. C.; Griffith, W. C.; Faustman, E. M. Metagenomic profiling of microbial composition and antibiotic resistance determinants in Puget Sound PLoS One 2012, 7 (10) e48000
20. 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
21. Zhang, X. X.; Zhang, T.; Fang, H. H. Antibiotic resistance genes in water environment Appl. Microbiol. Biotechnol. 2009, 82 (3) 397-414
22. Xu, W. H.; Zhang, G.; Zou, S. C.; Li, X. D.; Liu, Y. C. Determination of selected antibiotics in the Victoria Harbour and the Pearl River, South China using high-performance liquid chromatography-electrospray ionization tandem mass spectrometry Environ. Pollut. 2007, 145 (3) 672-679
23. 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, 1410-1416
24. Liu, B.; Pop, M. ARDB-antibiotic resistance genes database Nucleic Acids Res. 2009, 37, D443-D447
25. 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
26. 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
27. 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
28. Landers, T. F.; Cohen, B.; Wittum, T. E.; Larson, E. L. A review of antibiotic use in food animals: Perspective, policy, and potential Public Health Rep. 2012, 127 (1) 4-22
29. Zinner, S. H. Antibiotic use: Present and future New Microbiol. 2007, 30 (3) 321-325
30. Fredrickson, J. K.; Hicks, R. J.; Li, S. W.; Brockman, F. J. Plasmid incidence in bacteria from deep subsurface sediments Appl. Environ. Microb. 1988, 54 (12) 2916-2923
31. Kurusu, Y.; Yoshimura, S.; Tanaka, M.; Nakamura, T.; Maruyama, A.; Higashihara, T. Genetic transformation system for a psychrotrophic deep-sea bacterium: Isolation and characterization of a psychrotrophic plasmid Mar. Biotechnol. 2001, 3 (2) 96-99
32. Hughes, C. C.; Kauffman, C. A.; Jensen, P. R.; Fenical, W. Structures, reactivities, and antibiotic properties of the marinopyrroles A-F J. Org. Chem. 2010, 75 (10) 3240-3250
33. Amann, R. I.; Ludwig, W.; Schleifer, K. H. Phylogenetic identification and in situ detection of individual microbial cells without cultivation Microbiol. Rev. 1995, 59 (1) 143-69
34. Tenson, T.; Lovmar, M.; Ehrenberg, M. The mechanism of action of macrolides, lincosamides and streptogramin B reveals the nascent peptide exit path in the ribosome J. Mol. Biol. 2003, 330 (5) 1005-1014
35. Kobayashi, N.; Nishino, K.; Yamaguchi, A. novel macrolide-specific ABC-type efflux transporter in Escherichia coli J. Bacteriol. 2001, 183 (19) 5639-44
36. Modali, S. D.; Zgurskaya, H. I. The periplasmic membrane proximal domain of MacA acts as a switch in stimulation of ATP hydrolysis by MacB transporter Mol. Microbiol. 2011, 81 (4) 937-51
37. Shin, S. H.; Kim, S.; Kim, J. Y.; Lee, S.; Um, Y.; Oh, M. K.; Kim, Y. R.; Lee, J.; Yang, K. S. Complete genome sequence of Enterobacter aerogenes KCTC 2190 J. Bacteriol. 2012, 194 (9) 2373-2374
38. Husain, F.; Nikaido, H. Substrate path in the AcrB multidrug efflux pump of Escherichia coli Mol. Microbiol. 2010, 78 (2) 320-330
39. Padilla, E.; Llobet, E.; Domenech-Sanchez, A.; Martinez-Martinez, L.; Bengoechea, J. A.; Alberti, S. Klebsiella pneumoniae AcrAB efflux pump contributes to antimicrobial resistance and virulence Antimicrob. Agents Chemother. 2010, 54 (1) 177-183
40. Lacroix, F. J. C.; Cloeckaert, A.; Grepinet, O.; Pinault, C.; Popoff, M. Y.; Waxin, H.; Pardon, P. Salmonella typhimurium acrB-like gene: Identification and role in resistance to biliary salts and detergents and in murine infection Fems. Microbiol. Lett. 1996, 135 (2-3) 161-167
41. Stone, K. J.; Stroming, J. Mechanism of action of bacitracin-complexation with metal ion and C55-isoprenyl pyrophosphate Proc. Natl. Acad. Sci. U.S.A. 1971, 68 (12) 3223-3227
42. Hsuchen, C. C.; Feingold, D. S. Mechanism of polymyxin-B-action and selectivity toward biologic membranes Biochemistry 1973, 12 (11) 2105-2111
43. Schindler, P. R.; Teuber, M. Action of polymyxin B on bacterial membranes: morphological changes in the cytoplasm and in the outer membrane of Salmonella typhimurium and Escherichia coli B Antimicrob. Agents Ch. 1975, 8 (1) 95-104
44. 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) 30106-13
45. Gatzeva-Topalova, P. Z.; May, A. P.; Sousa, M. C. Crystal structure of Escherichia coli ArnA (PmrI) decarboxylase domain. A key enzyme for lipid A modification with 4-amino-4-deoxy-l-arabinose and polymyxin resistance Biochemistry 2004, 43 (42) 13370-9
46. Gatzeva-Topalova, P. Z.; May, A. P.; Sousa, M. C. Structure and mechanism of ArnA: conformational change implies ordered dehydrogenase mechanism in key enzyme for polymyxin resistance Structure 2005, 13 (6) 929-42
47. Silver, S. Bacterial resistances to toxic metal ions-A review Gene 1996, 179 (1) 9-19
48. Rosen, B. P. Bacterial resistance to heavy metals and metalloids J. Biol. Inorg. Chem. 1996, 1 (4) 273-277
49. Koronakis, V.; Eswaran, J.; Hughes, C. Structure and function of tolC: The bacterial exit duct for proteins and drugs Annu. Rev. Biochem. 2004, 73, 467-489
50. 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
51. 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? Exp. Opin. Invest. Drugs 2001, 10 (8) 1409-1422
52. Zhou, A. F.; Baidoo, E.; He, Z. L.; Mukhopadhyay, A.; Baumohl, J. K.; Benke, P.; Joachimiak, M. P.; Xie, M.; Song, R.; Arkin, A. P.; Hazen, T. C.; Keasling, J. D.; Wall, J. D.; Stahl, D. A.; Zhou, J. Z. Characterization of NaCl tolerance in Desulfovibrio vulgaris Hildenborough through experimental evolution ISME J. 2013, 7 (9) 1790-1802
53. 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
54. Storteboom, H.; Arabi, M.; Davis, J. G.; Crimi, B.; 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
55. Graham, D. W.; Olivares-Rieumont, S.; Knapp, C. W.; Lima, L.; Werner, D.; Bowen, E. Antibiotic resistance gene abundances associated with waste discharges to the Almendares River near Havana, Cuba Environ. Sci. Technol. 2011, 45 (2) 418-424
56. Song, J. S.; Jeon, J. H.; Lee, J. H.; Jeong, S. H.; Jeong, B. C.; Kim, S. J.; Lee, J. H.; Lee, S. H. Molecular characterization of TEM-type beta-lactamases identified in cold-seep sediments of Edison seamount (south of Lihir Island, Papua New Guinea) J. Microbiol. 2005, 43 (2) 172-178
57. Hall, B. G.; Barlow, M. Evolution of the serine beta-lactamases: Past, present and future Drug Resist. Update 2004, 7 (2) 111-123
58. Pruden, A.; Arabi, M.; Storteboom, H. N. Correlation between upstream human activities and riverine antibiotic resistance genes Environ. Sci. Technol. 2012, 46 (21) 11541-11549
59. 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
60. 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
61. 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
62. Baquero, F.; Negri, M. C.; Morosini, M. I.; Blazquez, J. Antibiotic-selective environments Clin. Infect. Dis. 1998, 27 (Suppl 1) S5-11
63. Normark, B. H.; Normark, S. Evolution and spread of antibiotic resistance J. Intern. Med. 2002, 252 (2) 91-106
64. Maiden, M. C. J. Horizontal genetic exchange, evolution, and spread of antibiotic resistance in bacteria Clin. Infect. Dis. 1998, 27, S12-S20
65. Mazel, D.; Davies, J. Antibiotic resistance in microbes Cell. Mol. Life Sci. 1999, 56 (9-10) 742-754
66. Pu, X. Y.; Zhang, Q. J.; Pan, J. C.; Shen, Z. Q.; Zhang, W. Spontaneous mutation frequency and molecular mechanisms of Shigella flexneri fluoroquinolone resistance under antibiotic selective stress World J. Microb. Biot. 2013, 29 (2) 365-371
67. Woodford, N.; Ellington, M. J. The emergence of antibiotic resistance by mutation Clin. Microbiol. Infec. 2007, 13 (1) 5-18
68. Martinez, J. L.; Baquero, F. Mutation frequencies and antibiotic resistance Antimicrob. Agents Ch. 2000, 44 (7) 1771-1777
69. Doublet, B.; Weill, F. X.; Fabre, L.; Chaslus-Dancla, E.; Cloeckaert, A. Variant Salmonella genomic island 1 antibiotic resistance gene cluster containing a novel 3′-N-aminoglycoside acetyltransferase gene cassette, aac(3)-id, in Salmonella enterica serovar Newport Antimicrob. Agents Ch. 2004, 48 (10) 3806-3812
70. Venturini, C.; Beatson, S. A.; Djordjevic, S. P.; Walker, M. J. Multiple antibiotic resistance gene recruitment onto the enterohemorrhagic Escherichia coli virulence plasmid Faseb. J. 2010, 24 (4) 1160-1166