Spread of tetracycline resistance genes at a conventional dairy farm

Frontiers in Microbiology

Volumn 6, Issue MAY, 2015, Pages

  Kyselková, Martina ^a   Jirout, Jirí ^a   Vrchotová, Nadežda ^b   Schmitt, Heike ^c   Elhottová, Dana ^a  

^a INSTITUTE OF SOIL BIOLOGY   (Czech Republic)

^b INSTITUTE OF MATHEMATICS   (Czech Republic)

^c UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Animal manure; Antibiotic resistance spread; Cattle intestinal microflora; Chlortetracycline; Dairy cattle; Dairy farm; Heavy metals; Tetracycline resistance genes

Indexed keywords

BACTERIUM LYSATE; CHLORTETRACYCLINE; COPPER; RNA 16S; TETRACYCLINE; ZINC;

ADULT; ARTICLE; BACTERIAL COLONIZATION; BACTERIUM ISOLATION; CONTROLLED STUDY; DAIRY CATTLE; DAIRYING; DNA ISOLATION; EXCRETION; FEEDING; GENE; GENE SEQUENCE; LIMIT OF DETECTION; LIMIT OF QUANTITATION; MANURE; MILK; MOLECULAR CLONING; NONHUMAN; REAL TIME POLYMERASE CHAIN REACTION; SOIL ANALYSIS; TETRACYCLINE RESISTANCE GENE;

ACINETOBACTER; ANIMALIA; BOS; CLOSTRIDIUM; LACTOBACILLUS; SHIGELLA;

EID: 84931270438     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.00536     Document Type: Article

References (41)

1. Aminov, R. I., Chee-Sanford, J. C., Garrigues, N., Teferedegne, B., Krapac, I. J., White, B. A., et al. (2002). Development, validation, and application of PCR primers for detection of tetracycline efflux genes of Gram-negative bacteria. Appl. Environ. Microbiol. 68, 1786-1793. doi: 10.1128/AEM.68.4.1786-1793.2002.
2. Baker-Austin, C., Wright, M. S., Stepanauskas, R., and McArthur, J. V. (2006). Co-selection of antibiotic and metal resistance. Trends Microbiol. 14, 176-182. doi: 10.1016/j.tim.2006.02.006.
3. Barkovskii, A. L., and Bridges, C. (2012). Persistence and profiles of tetracycline resistance genes in swine farms and impact of operational practices on their occurrence in farms' vicinities. Water Air Soil Pollut. 223, 49-62. doi: 10.1007/s11270-011-0838-1.
4. Chee-Sanford, J. C., Mackie, R. I., Koike, S., Krapac, I. G., Lin, Y.-F., Yannarell, A. C., et al. (2009). Fate and transport of antibiotic residues and antibiotic resistance genes following land application of manure waste. J. Environ. Qual. 38, 1086-1108. doi: 10.2134/jeq2008.0128.
5. Chowdhury, P. R., McKinnon, J., Wyrsch, E., Hammond, J. M., Charles, I. G., and Djordjevic, S. P. (2014). Genomic interplay in bacterial communities: implications for growth promoting practices in animal husbandry. Front. Microbiol. 5:394. doi: 10.3389/fmicb.2014.00394.
6. Clarke, K. R., and Gorley, R. N. (2006). PRIMER v6: User Manual/Tutorial. Plymouth: PRIMER-E.
7. Dowd, S. E., Callaway, T. R., Wolcott, R. D., Sun, Y., McKeehan, T., Hagevoort, R. G., et al. (2008). Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP). BMC Microbiol. 8:125. doi: 10.1186/1471-2180-8-125.
8. Durso, L. M., and Cook, K. L. (2014). Impacts of antibiotic use in agriculture: what are the benefits and risks? Curr. Opin. Microbiol. 19, 37-44. doi: 10.1016/j.mib.2014.05.019.
9. Durso, L. M., Harhay, G. P., Bono, J. L., and Smith, T. P. (2011). Virulence-associated and antibiotic resistance genes of microbial populations in cattle feces analyzed using a metagenomic approach. J. Microbiol. Methods 84, 278-282. doi: 10.1016/j.mimet.2010.12.008.
10. Durso, L. M., Harhay, G. P., Smith, T. P., Bono, J. L., De Santis, T. Z., Harhay, D. M., et al. (2010). Animal-to-animal variation in fecal microbial diversity among beef cattle. Appl. Environ. Microbiol. 76, 4858-4862. doi: 10.1128/AEM.00207-10.
11. Forsberg, K. J., Reyes, A., Wang, B., Selleck, E. M., Sommer, M. O. A., and Dantas, G. (2012). The shared antibiotic resistome of soil bacteria and human pathogens. Science 337, 1107-1111. doi: 10.1126/science.1220761.
12. Galvão, K. N. (2011). "Identifying and treating uterine disease in dairy cows," in Proceedings 47th Florida Dairy Production Conference (Gainesville, FL).
13. Goshen, T., and Shpigel, N. Y. (2006). Evaluation of intrauterine antibiotic treatment of clinical metritis and retained fetal membranes in dairy cows. Theriogenology 66, 2210-2218. doi: 10.1016/j.theriogenology.2006.07.017.
14. Gullberg, E., Albrecht, L. M., Karlsson, C., Sandegren, L., and Andersson, D. I. (2014). Selection of a multidrug resistance plasmid by sublethal levels of antibiotics and heavy metals. mBio 5, e01918-e01914. doi: 10.1128/mBio.01918-14.
15. Hajurka, J., Nagy, J., Popelka, P., Rozanska, H., Sokol, J., Cabadaj, R., et al. (2003). Tetracycline concentrations in blood and milk of cows following intrauterine treatment of acute or subacute/chronic endometritis. Bull. Vet. Inst. Pulawy 47, 435-448. Available online at: http://bulletin.piwet.pulawy.pl/index.php/archive-pdf-a-abstracts/45/568-bull-vet-inst-pulawy-47-435-447-2003.
16. Hall, T. A. (1999). Bioedit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41, 95-98.
17. Hong, P. Y., Li, X., Yang, X., Shinkai, T., Zhang, Y., Wang, X., et al. (2012). Monitoring airborne biotic contaminants in the indoor environment of pig and poultry confinement buildings. Environ. Microbiol. 14, 1420-1431. doi: 10.1111/j.1462-2920.2012.02726.x.
18. Hong, P. Y., Yannarell, A., Dai, Q., Ekizoglu, M., and Mackie, R. I. (2013). Monitoring the perturbation of soil and groundwater microbial communities due to pig production activities. Appl. Environ. Microbiol. 79, 2620-2629. doi: 10.1128/AEM.03760-12.
19. Jechalke, S., Heuer, H., Siemens, J., Amelung, W., and Smalla, K. (2014). Fate and effects of veterinary antibiotics in soil. Trends Microbiol. 22, 536-545. doi: 10.1016/j.tim.2014.05.005.
20. Kobashi, Y., Hasebe, A., Nishio, M., and Uchiyama, H. (2007). Diversity of tetracycline resistance genes in bacteria isolated from various agricultural environments. Microbes Environ. 22, 44-51. doi: 10.1264/jsme2.22.44.
21. Koenig, J. E., Spor, A., Scalfone, N., Fricker, A. D., Stombaugh, J., Knight, R., et al. (2011). Succession of microbial consortia in the developing infant gut microbiome. Proc. Natl. Acad. Sci. U.S.A. 108, 4578-4585. doi: 10.1073/pnas.1000081107.
22. Kyselková, M., Jirout, J., Chronáková, A., Vrchotová, N., Bradley, R., Schmitt, H., et al. (2013). Cow excrements enhance the occurrence of tetracycline resistance genes in soil regardless of their oxytetracycline content. Chemosphere 93, 2413-2418. doi: 10.1016/j.chemosphere.2013.08.058.
23. Kyselková, M., Kotrbová, L., Bhumibhamon, G., Chroòáková, A., Jirout, J., Vrchotová, N., et al. (2015). Tetracycline resistence genes persist in soil amended with cattle feces independently from chlortetracycline selection pressure. Soil Biol. Biochem. 81, 259-265. doi: 10.1016/j.soilbio.2014.11.018.
24. Lamendella, R., Santo Domingo, J. W., Ghosh, S., Martinson, J., and Oerther, D. B. (2011). Comparative fecal metagenomics unveils unique functional capacity of the swine gut. BMC Microbiol. 11:103. doi: 10.1186/1471-2180-11-103.
25. Ling, A. L., Pace, N. R., Hernandez, M. T., and LaPara, T. M. (2013). Tetracycline resistance and class 1 integron genes associated with indoor and outdoor aerosols. Environ. Sci. Technol. 47, 4046-4052. doi: 10.1021/es400238g.
26. Looft, T., Johnson, T. A., Allen, H. K., Bayles, D. O., Alt, D. P., Stedtfeld, R. D., et al. (2012). In-feed antibiotic effects on the swine intestinal microbiome. Proc. Natl. Acad. Sci. U.S.A. 109, 1691-1696. doi: 10.1073/pnas.1120238109.
27. McDonagh, S., Maidji, E., Ma, W., Chang, H. T., Fisher, S., and Pereira, L. (2004). Viral and bacterial pathogens at the maternal-fetal interface. J. Infect. Dis. 190, 826-834. doi: 10.1086/422330.
28. Palmer, C., Bik, E. M., DiGiulio, D. B., Relman, D. A., and Brown, P. O. (2007). Development of the human infant intestinal microbiota. PLoS Biol. 5:e177. doi: 10.1371/journal.pbio.0050177.
29. Peak, N., Knapp, C. W., Yang, R. K., Hanfelt, M. M., Smith, M. S., Aga, D. S., et al. (2007). Abundance of six tetracycline resistance genes in wastewater lagoons at cattle feedlots with different antibiotic use strategies. Environ. Microbiol. 9, 143-151. doi: 10.1111/j.1462-2920.2006.01123.x.
30. Pruden, A., Pei, R., Storteboom, H., and Carlson, K. H. (2006). Antibiotic resistance genes as emerging contaminants: studies in northern Colorado. Environ. Sci. Technol. 40, 7445-7450. doi: 10.1021/es060413l.
31. Roberts, M. C. (2005). Update on acquired tetracycline resistance genes. FEMS Microbiol. Lett. 245, 195-203. doi: 10.1016/j.femsle.2005.02.034.
32. Rybaříková, J., Dolejská, M., Materna, D., Literák, I., and Čížek, A. (2010). Phenotypic and genotypic characteristics of antimicrobial resistant Escherichia coli isolated from symbovine flies, cattle and sympatric insectivorous house martins from a farm in the Czech Republic (2006-2007). Res. Vet. Sci. 89, 179-183. doi: 10.1016/j.rvsc.2010.02.016.
33. Santamaría, J., López, L., and Soto, C. Y. (2011). Detection and diversity evaluation of tetracycline resistance genes in grassland-based production systems in Colombia, South America. Front. Microbiol. 2, 1-10. doi: 10.3389/fmicb.2011.00252.
34. Sawant, A. A., Hegde, N. V., Straley, B. A., Donaldson, S. C., Love, B. C., Knabel, S. J., et al. (2007). Antimicrobial-resistant enteric bacteria from dairy cattle. Appl. Environ. Microbiol. 73, 156-163. doi: 10.1128/AEM.01551-06.
35. Smith, D. L., Dushoff, J., and Morris, J. G. (2005). Agricultural antibiotics and human health. PLoS Med. 2:e232. doi: 10.1371/journal.pmed.0020232.
36. Thompson, C. L., Wang, B., and Holmes, A. J. (2008). The immediate environment during postnatal development has long-term impact on gut community structure in pigs. ISME J. 2, 739-748. doi: 10.1038/ismej.2008.29.
37. van Essen-Zandbergen, A., Smith, H., Veldman, K., and Mevius, D. (2009). In vivo transfer of an incFIB plasmid harbouring a class 1 integron with gene cassettes dfrA1-aadA1. Vet. Microbiol. 137, 402-407. doi: 10.1016/j.vetmic.2009.02.004.
38. Wang, R., Wei, R., Chen, M., and Wang, T. (2010). A new, simple and rapid HPLC method for determination of chlortetracycline in pig solid manure. Ital. J. Anim. Sci. 9, 190-193. doi: 10.4081/ijas.2010.e37.
39. Wichmann, F., Udikovic-Kolic, N., Andrew, S., and Handelsman, J. (2014). Diverse antibiotic resistance genes in dairy cow manure. mBio 5, e01017-e01013. doi: 10.1128/mBio.01017-13.
40. Zhang, Y., Snow, D. D., Parker, D., Zhou, Z., and Li, X. (2013). Intracellular and extracellular antimicrobial resistance genes in the sludge of livestock waste management structures. Environ. Sci. Technol. 47, 10206-10213. doi: 10.1021/es401964s.
41. Zhu, Y.-G., Johnson, T. A., Su, J.-Q., Qiao, M., Guo, G.-X., Stedtfeld, R. D., et al. (2013). Diverse and abundant antibiotic resistance genes in Chinese swine farms. Proc. Natl. Acad. Sci. U.S.A. 110, 3435-3440. doi: 10.1073/pnas.1222743110.