Effect of manure application on abundance of antibiotic resistance genes and their attenuation rates in soil: Field-scale mass balance approach

Environmental Science and Technology

Volumn 48, Issue 5, 2014, Pages 2643-2650

  Fahrenfeld, Nicole ^a   Knowlton, Katharine ^b   Krometis, Leigh Anne ^c   Hession, W Cully ^c   Xia, Kang ^b   Lipscomb, Emily ^c   Libuit, Kevin ^c   Green, Breanna Lee ^c   Pruden, Amy ^c  

^a the State University of New Jersey   (United States)

^b VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

^c Virginia Polytechnic Institute and State University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENE TRANSFER; MANURES; SOILS;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC RESISTANCE GENES; HORIZONTAL GENE TRANSFER; LOGARITHMIC DECAY; MANURE APPLICATIONS; MITIGATION STRATEGY; SOIL CONCENTRATIONS; SUBSURFACE TRANSPORT;

SOIL POLLUTION;

METAL; SURFACE WATER; ANTIINFECTIVE AGENT; MANURE;

ABUNDANCE; ANTIBIOTIC RESISTANCE; BACTERIUM; FIELD SURVEY; GROWTH RATE; MANURE; MASS BALANCE; SLURRY;

AGRICULTURAL SLURRY; ANTIBIOTIC RESISTANCE; ARG GENE; ARTICLE; BACTERIAL GENE; CATTLE; CONTROLLED STUDY; EQUIDAE; ERMF GENE; GROWTH; HORIZONTAL GENE TRANSFER; MANURE; MICROBIAL ATTENUATION; MICROBIAL GENE; NONHUMAN; SHEEP; SOIL; SUL1 GENE; SUL2 GENE; SURFACE PROPERTY; TET(G) GENE; TET(O) GENE; TET(W) GENE; ANALYSIS; ANIMAL; BACTERIUM; BOVINE; DRUG EFFECTS; GENETICS; HORSE; ISOLATION AND PURIFICATION; MICROBIOLOGY; SEASON; SEDIMENT; UNITED STATES;

ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIA; CATTLE; DRUG RESISTANCE, BACTERIAL; GENE TRANSFER, HORIZONTAL; GENES, BACTERIAL; GEOLOGIC SEDIMENTS; HORSES; MANURE; SEASONS; SHEEP; SOIL MICROBIOLOGY; VIRGINIA;

EID: 84895523528     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/es404988k     Document Type: Article

References (41)

1. Forsberg, K. J.; Reyes, A.; Wang, B.; 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
2. Casey, J. A.; Curriero, F. C.; Cosgrove, S. E.; Nachman, K. E.; Schwartz, B. S. High-density livestock operations, crop field application of manure, and risk of community-associated methicillin-resistant Staphylococcus aureus infection in Pennsylvania JAMA Intern. Med. 2013, 1980-1990
3. Chee-Sanford, J. C.; Mackie, R. I.; Koike, S.; Krapac, I. G.; Lin, Y.-F.; Yannarell, A. C.; Maxwell, S.; Aminov, R. I. Fate and transport of antibiotic residues and antibiotic resistance genes following land application of manure waste J. Environ. Qual. 2009, 38 (3) 1086-1108
4. Aga, D. S.; Goldfish, R.; Kulshrestha, P. Application of ELISA in determining the fate of tetracyclines in land-applied livestock wastes Analyst 2003, 128 (6) 658-662
5. Pakpour, S.; Jabaji, S.; Chenier, M. R. Frequency of antibiotic resistance in a swine facility 2.5 years after a ban on antibiotics Microb. Ecol. 2012, 63, 41-50
6. Zhang, F.; Li, Y.; Yang, M.; Li, W. Content of heavy metals in animal feeds and manures from farms of different scales in northeast China Int. J. Environ. Res. Public Health 2012, 9 (8) 2658-2668
7. Chee-Sanford, J. C.; Aminov, R. I.; Krapac, I. J.; Garrigues-Jeanjean, N.; Mackie, R. I. Occurrence and diversity of tetracycline tesistance genes in lagoons and groundwater underlying two swine production facilities Appl. Environ. Microbiol. 2001, 67 (4) 1494-1502
8. McKinney, C. W.; Loftin, K. A.; Meyer, M. T.; Davis, J. G.; Pruden, A. Tet and sul antibiotic resistance genes in livestock lagoons of various operation type, configuration, and antibiotic occurrence Environ. Sci. Technol. 2010, 44 (16) 6102-6109
9. Smith, M. S.; Yang, R. K.; Knapp, C. W.; Niu, Y.; Peak, N.; Hanfelt, M. M.; Galland, J. C.; Graham, D. W. Quantification of tetracycline resistance genes in feedlot lagoons by real-time PCR Appl. Environ. Microbiol. 2004, 70 (12) 7372-7377
10. Jechalke, S.; Focks, A.; Rosendahl, I.; Groeneweg, J.; Siemens, J.; Heuer, H.; Smalla, K. Structural and functional response of the soil bacterial community to application of manure from difloxacin-treated pigs FEMS Microbiol. Ecol. 2014, 87, 78-88
11. Koike, S.; Krapac, I. G.; Oliver, H. D.; Yannarell, A. C.; Chee-Sanford, J. C.; Aminov, R. I.; Mackie, R. I. Monitoring and source tracking of tetracycline resistance genes in lagoons and groundwater adjacent to swine production facilities over a 3-year period Appl. Environ. Microbiol. 2007, 73 (15) 4813-4823
12. Mackie, R. I.; Koike, S.; Krapac, I.; Chee-Sanford, J.; Maxwell, S.; Aminov, R. I. Tetracycline residues and tetracycline resistance genes in groundwater impacted by swine production facilities Anim. Biotechnol. 2006, 17 (2) 157-176
13. 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
14. Sengelov, G.; Agerso, Y.; Halling-Sorensen, B.; Baloda, S. B.; Andersen, J. S.; Jensen, L. B. Bacterial antibiotic resistance levels in Danish farmland as a result of treatment with pig manure slurry Environ. Int. 2003, 28 (7) 587-595
15. Byrne-Bailey, K. G.; Gaze, W. H.; Kay, P.; Boxall, A. B. A.; Hawkey, P. M.; Wellington, E. M. H. Prevalence of sulfonamide resistance genes in bacterial isolates from manured agricultural soils and pig slurry in the United Kingdom Antimicrob. Agents Chemother. 2009, 53 (2) 696-702
16. Heuer, H.; Smalla, K. Manure and sulfadiazine synergistically increased bacterial antibiotic resistance in soil over at least two months Environ. Microbiol. 2007, 9 (3) 657-666
17. Heuer, H.; Solehati, Q.; Focks, A.; Thiele-Bruhn, S.; Smalla, K. Accumulation of sulfonamide resistance genes in arable soils due to repeated application of manure containing sulfadiazine Appl. Environ. Microbiol. 2011, 77, 2527-2530
18. Joy, S. R.; Bartelt-Hunt, S.; Snow, D.; Gilley, J. E.; Woodbury, B.; Parker, D.; Marx, D. B.; Li, X. Fate and transport of antimicrobials and antimicrobial resistance genes in soil and runoff following land application of swine manure slurry Environ. Sci. Technol. 2013, 47, 12081-12088
19. 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, 3435-3440
20. Knapp, C. W.; McCluskey, S. M.; Singh, B. K.; Campbell, C. D.; Hudson, G.; Graham, D. W. Antibiotic resistance gene abundances correlate with metal and geochemical conditions in archived Scottish soils PLoS One 2011, 6 (11) e27300
21. Berg, J.; Thorsen, M. K.; Holm, P. E.; Jensen, J.; Nybroe, O.; Brandt, K. K. Cu exposure under field conditions coselects for antibiotic resistance as determined by a novel cultivation-independent bacterial community tolerance assay Environ. Sci. Technol. 2010, 44 (22) 8724-8728
22. Knapp, C. S.; Dolfing, J.; Ehlert, P. A.; Graham, D. W. Evidence of increasing antibiotic resistance gene abundances in archived soils since 1940 Environ. Sci. Technol. 2010, 44, 580-587
23. Ghosh, S.; LaPara, T. M. The effects of subtherapeutic antibiotic use in farm animals on the proliferation and persistence of antibiotic resistance among soil bacteria ISME J. 2007, 1 (3) 191-203
24. Yang, H.; Byelashov, O. A.; Geornaras, I.; Goodridge, L. D.; Nightingale, K. K.; Belk, K. E.; Smith, G. C.; Sofos, J. N. Presence of antibiotic-resistant commensal bacteria in samples from agricultural, city, and national park environments evaluated by standard culture and real-time PCR methods Can. J. Microbiol. 2010, 56 (9) 761-770
25. Zhou, Z.; Raskin, L.; Zilles, J. L. Effects of swine manure on macrolide, lincosamide, and streptogramin B antimicrobial resistance in soils Appl. Environ. Microbiol. 2010, 76 (7) 2218-2224
26. Ma, Y.; Wilson, C. A.; Novak, J. T.; Riffat, R.; Aynur, S.; Murthy, S.; Pruden, A. Effect of various sludge digestion conditions on sulfonamide, macrolide, and tetracycline resistance genes and class I integrons Environ. Sci. Technol. 2011, 45 (18) 7855-7861
27. Suzuki, M. T.; Taylor, L. T.; DeLong, E. F. Quantitative analysis of small-subunit rRNA genes in mixed microbial populations via 5′-nuclease assays Appl. Environ. Microbiol. 2000, 66 (11) 4605-4614
28. Chen, J.; Yu, Z.; Michel, F. C.; Wittum, T.; Morrison, M. Development and application of real-time PCR assays for quantification of erm genes conferring resistance to macrolides-lincosamides-streptogramin B in livestock manure and manure management systems Appl. Environ. Microbiol. 2007, 73 (14) 4407-4416
29. Aminov, R.; Garrigues-Jeanjean, N.; Mackie, R. Molecular ecology of tetracycline resistance: development and validation of primers for detection of tetracycline resistance genes encoding ribosomal protection proteins Appl. Environ. Microbiol. 2001, 67 (1) 22-32
30. Aminov, R. I.; Chee-Sanford, J. C.; Garrigues, N.; Teferedegne, B.; Krapac, I. J.; White, B. A.; Mackie, R. I. Development, validation, and application of PCR primers for detection of tetracycline efflux genes of Gram-negative bacteria Appl. Environ. Microbiol. 2002, 68 (4) 1786-1793
31. Dutka-Malen, S.; Evers, S.; Courvalin, P. Detection of glycopeptide resistance genotypes and identification to the species level of clinically relevant enterococci by PCR J. Clin. Microbiol. 1995, 33 (1) 24-27
32. Fahrenfeld, N. L.; Ma, Y.; O'Brien, M.; Pruden, A., Reclaimed water as a reservoir of antibiotic resistance genes: distribution system and irrigation implications. Front. Microbiol. 2013, 4.
33. Selvam, A.; Xu, D.; Zhao, Z.; Wong, J. W. C. Fate of tetracycline, sulfonamide and fluoroquinolone resistance genes and the changes in bacterial diversity during composting of swine manure Bioresour. Technol. 2012, 126, 383-390
34. Wu, N.; Qiao, M.; Zhang, B.; Cheng, W.-D.; Zhu, Y.-G. Abundance and diversity of tetracycline resistance genes in soils adjacent to representative swine feedlots in China Environ. Sci. Technol. 2010, 44 (18) 6933-6939
35. McKinney, C. W.; Pruden, A. Ultraviolet disinfection of antibiotic resistant bacteria and their antibiotic resistance genes in water and wastewater Environ. Sci. Technol. 2012, 46, 13393-13400
36. Burch, T. R.; Sadowsky, M. J.; LaPara, T. M., Aerobic digestion reduces the quantity of antibiotic resistance genes in residual municipal wastewater solids. Front. Microbiol. 2013, 4.
37. Zhang, Y.; Snow, D. D.; Parker, D.; Zhou, Z.; Li, X. Intracellular and Extracellular Antimicrobial Resistance Genes in the Sludge of Livestock Waste Management Structures Environ. Sci. Technol. 2013, 47 (18) 10206-10213
38. Walter, M. T.; Walter, M. F.; Brooks, E. S.; Steenhuis, T. S.; Boll, J.; Weiler, K. Hydrologically sensitive areas: Variable source area hydrology implications for water quality risk assessment J. Soil Water Conserv. 2000, 55 (3) 277-284
39. Easton, Z. M.; Fuka, D. R.; Walter, M. T.; Cowan, D. M.; Schneiderman, E. M.; Steenhuis, T. S. Re-conceptualizing the soil and water assessment tool (SWAT) model to predict runoff from variable source areas J. Hydrol. 2008, 348 (3-4) 279-291
40. Poté, J.; Ceccherini, M. T.; Van, V. T.; Rosselli, W.; Wildi, W.; Simonet, P.; Vogel, T. M. Fate and transport of antibiotic resistance genes in saturated soil columns Eur. J. Soil Biol. 2003, 39 (2) 65-71
41. Rysz, M.; Alvarez, P. Transport of antibiotic-resistant bacteria and resistance-carrying plasmids through porous media Water Sci. Technol. 2006, 54 (11-12) 363-370