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Catchment-scale export of antibiotic resistance genes and bacteria from an agricultural watershed in central Iowa


Autoři: Timothy P. Neher aff001;  Lanying Ma aff001;  Thomas B. Moorman aff002;  Adina C. Howe aff001;  Michelle L. Soupir aff001
Působiště autorů: Department of Agricultural and Biosystems Engineering, Iowa State University, Ames, Iowa, United States of America aff001;  National Laboratory for Agriculture and the Environment, USDA-ARS, Ames, Iowa, United States of America aff002
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0227136

Souhrn

Antibiotics are administered to livestock in animal feeding operations (AFOs) for the control, prevention, and treatment of disease. Manure from antibiotic treated livestock contains unmetabolized antibiotics that provide selective pressure on bacteria, facilitating the expression of anti-microbial resistance (AMR). Manure application on row crops is an agronomic practice used by growers to meet crop nutrient needs; however, it can be a source of AMR to the soil and water environment. This study in central Iowa aims to directly compare AMR indicators in outlet runoff from two adjacent (221 to 229 ha) manured and non-manured catchments (manure comparison), and among three catchments (600 to 804 ha) with manure influence, no known manure application (control), and urban influences (mixed land use comparison). Monitored AMR indicators included antibiotic resistance genes (ARGs) ermB, ermF (macrolide), tetA, tetM, tetO, tetW (tetracycline), sul1, sul2 (sulfonamide), aadA2 (aminoglycoside), vgaA, and vgaB (pleuromutilin), and tylosin and tetracycline resistant enterococci bacteria. Results of the manure comparison showed significantly higher (p<0.05) tetracycline and tylosin resistant bacteria from the catchment with manure application in 2017, but no differences in 2018, possibly due to changes in antibiotic use resulting from the Veterinary Feed Directive. Moreover, the ARG analysis indicated a larger diversity of ARGs at the manure amended catchment. The mixed land use comparison showed the manure amended catchment had significantly higher (p<0.05) tetracycline resistant bacteria in 2017 and significantly higher tylosin resistant bacteria in 2017 and 2018 than the urban influenced catchment. The urban influenced catchment had significantly higher ermB concentrations in both sampling years, however the manure applied catchment runoff consisted of higher relative abundance of total ARGs. Additionally, both catchments showed higher AMR indicators compared to the control catchment. This study identifies four ARGs that might be specific to AMR as a result of agricultural sources (tetM, tetW, sul1, sul2) and optimal for use in watershed scale monitoring studies for tracking resistance in the environment.

Klíčová slova:

Agricultural soil science – Antibiotic resistance – Antibiotics – Enterococcus – Livestock care – Ribosomal RNA – Tetracyclines – Watersheds


Zdroje

1. Lipsitch M., Singer R. S., & Levin B. R. (2002). Antibiotics in agriculture: When is it time to close the barn door? Proceedings of the National Academy of Sciences, 99(9), 5752–5754. doi: 10.1073/pnas.092142499 11983874

2. Van Boeckel T. P., Brower C., Gilbert M., Grenfell B. T., Levin S. A., Robinson T. P.,et al (2015). Global trends in antimicrobial use in food animals. Proceedings of the National Academy of Sciences, 112(18), 5649–5654. doi: 10.1073/pnas.1503141112 25792457

3. FDA. (2016). Summary Report on Antimicrobials Sold or Distributed for Use in Food-Producing Animals.

4. Washington M. T., Moorman T. B., Soupir M. L., Shelley M., & Morrow A. J. (2018). Monitoring tylosin and sulfamethazine in a tile-drained agricultural watershed using polar organic chemical integrative sampler (POCIS). Science of The Total Environment, 612(Supplement C), 358–367. doi: 10.1016/j.scitotenv.2017.08.090 28854391

5. Mira P. M., Meza J. C., Nandipati A., & Barlow M. (2015). Adaptive Landscapes of Resistance Genes Change as Antibiotic Concentrations Change. Molecular Biology and Evolution, 32(10), 2707–2715. doi: 10.1093/molbev/msv146 26113371

6. Schwaiger K., Harms K., Hölzel C., Meyer K., Karl M., & Bauer J. (2009). Tetracycline in liquid manure selects for co-occurrence of the resistance genes tet(M) and tet(L) in Enterococcus faecalis. Veterinary Microbiology, 139(3), 386–392. http://dx.doi.org/10.1016/j.vetmic.2009.06.005

7. Kim S. Y., Kuppusamy S., Kim J. H., Yoon Y.-E., Kim K.-R., & Lee Y. B. (2016). Occurrence and diversity of tetracycline resistance genes in the agricultural soils of South Korea. Environmental Science and Pollution Research, 23(21), 22190–22196. doi: 10.1007/s11356-016-7574-4 27638788

8. Sanderson H., Fricker C., Brown R. S., Majury A., & Liss S. N. (2016). Antibiotic resistance genes as an emerging environmental contaminant. Environmental Reviews, 24(2), 205–218. doi: 10.1139/er-2015-0069

9. Heuer H., Schmitt H., & Smalla K. (2011). Antibiotic resistance gene spread due to manure application on agricultural fields. Current Opinion in Microbiology, 14(3), 236–243. doi: 10.1016/j.mib.2011.04.009 21546307

10. O'Neill J. (2016). Tackling Drug-Resistant Infections Globally: Final Report and Recommendations. THE REVIEW ON ANTIMICROBIAL RESISTANCE. Retrieved from https://amr-review.org/sites/default/files/160518_Final%20paper_with%20cover.pdf

11. Bowen Z., Hanqin T., Chaoqun L., Dangal S. R. S., Jia Y., & Shufen P. (2017). Global manure nitrogen production and application in cropland during 1860–2014: a 5 arcmin gridded global dataset for Earth system modeling. Earth System Science Data, 9(2), 667–678. doi: 10.5194/essd-9-667-2017

12. Khaleel R., Reddy K. R., & Overcash M. R. (1981). Changes in Soil Physical Properties Due to Organic Waste Applications: A Review1. Journal of Environmental Quality, 10(2), 133–141. doi: 10.2134/jeq1981.00472425001000020002x

13. Unc A., & Goss M. J. (2004). Transport of bacteria from manure and protection of water resources. Applied Soil Ecology, 25(1), 1–18. https://doi.org/10.1016/j.apsoil.2003.08.007

14. West B. M., Liggit P., Clemans D. L., & Francoeur S. N. (2011). Antibiotic Resistance, Gene Transfer, and Water Quality Patterns Observed in Waterways near CAFO Farms and Wastewater Treatment Facilities. Water, Air, & Soil Pollution, 217(1), 473–489. doi: 10.1007/s11270-010-0602-y

15. Collins R., Elliott S., & Adams R. (2005). Overland flow delivery of faecal bacteria to a headwater pastoral stream. Journal of Applied Microbiology, 99(1), 126–132. doi: 10.1111/j.1365-2672.2005.02580.x 15960672

16. Tomer M. D., Moorman T. B., & Rossi C. G. (2008). Assessment of the Iowa River's South Fork watershed: Part 1. Water quality. Journal of Soil and Water Conservation, 63(6), 360–370. doi: 10.2489/jswc.63.6.360

17. Fausey N. R., Brown L. C., Belcher H. W., & Kanwar R. S. (1995). Drainage and Water Quality in Great Lakes and Cornbelt States. Journal of Irrigation and Drainage Engineering, 121(4), 283–288. doi: 10.1061/(ASCE)0733-9437(1995)121:4(283)

18. Fausey, N. R., Doering, E. J., & M.L., P. (1987). Purposes and Benefits of Drainage. In G. A. Pavelis (Ed.), Farm Drainage in the United States: History, Status, and Prospects (Vol. Issue 1455, pp. 48): Miscellaneous Publication.

19. Brendel C. E., Soupir M. L., Long L. A. M., Helmers M. J., Ikenberry C. D., & Kaleita A. L. (2019). Catchment-scale Phosphorus Export through Surface and Drainage Pathways. Journal of Environmental Quality, 48(1), 117–126. doi: 10.2134/jeq2018.07.0265 30640359

20. Williams M. R., King K. W., & Fausey N. R. (2015). Contribution of tile drains to basin discharge and nitrogen export in a headwater agricultural watershed. Agricultural Water Management, 158, 42–50. https://doi.org/10.1016/j.agwat.2015.04.009

21. Garder J. L., Moorman T. B., & Soupir M. L. (2014). Transport and Persistence of Tylosin-Resistant Enterococci, erm Genes, and Tylosin in Soil and Drainage Water from Fields Receiving Swine Manure. Journal of Environmental Quality, 43(4), 1484–1493. doi: 10.2134/jeq2013.09.0379 25603096

22. Luby E. M., Moorman T. B., & Soupir M. L. (2016). Fate and transport of tylosin-resistant bacteria and macrolide resistance genes in artificially drained agricultural fields receiving swine manure. Science of The Total Environment, 550, 1126–1133. doi: 10.1016/j.scitotenv.2016.01.132 26874610

23. Rieke E. L., Moorman T. B., Douglass E. L., & Soupir M. L. (2018). Seasonal variation of macrolide resistance gene abundances in the South Fork Iowa River Watershed. Science of The Total Environment, 610–611, 1173–1179. doi: 10.1016/j.scitotenv.2017.08.116 28847138

24. Pappas A., Kanwar E., S., Baker R., L., Lorimor J., C., . (2008). Fecal Indicator Bacteria in Subsurface Drain Water Following Swine Manure Application. Transactions of the ASABE, 51(5), 1567–1573. https://doi.org/10.13031/2013.25313

25. Brendel C., & Soupir M. (2017). Relating Watershed Characteristics to Elevated Stream Escherichia coli Levels in Agriculturally Dominated Landscapes: An Iowa Case Study. Water, 9(3), 154.

26. Jamieson R., Gordon R., Sharples K., Stratton G., & Madani A. (2002). Movement and persistence of fecal bacteria in agricultural soils and subsurface drainage water: A review. Canadian Biosystems Engineering, 44(1), 1–9.

27. Knapp C. W., Dolfing J., Ehlert P. A. I., & Graham D. W. (2010). Evidence of Increasing Antibiotic Resistance Gene Abundances in Archived Soils since 1940. Environmental Science & Technology, 44(2), 580–587. doi: 10.1021/es901221x 20025282

28. Uyaguari-Díaz M. I., Croxen M. A., Luo Z., Cronin K. I., Chan M., Baticados W. N., et al. (2018). Human Activity Determines the Presence of Integron-Associated and Antibiotic Resistance Genes in Southwestern British Columbia. Frontiers in microbiology, 9, 852–852. doi: 10.3389/fmicb.2018.00852 29765365

29. Prior, J. C. (2017). Des Moines Lobe. Retrieved from https://www.iihr.uiowa.edu/igs/des-moines-lobe/?doing_wp_cron=1571670623.3457748889923095703125

30. District, S. C. S. a. W. C. (2011). Black Hawk Lake Watershed Management Plan. Retrieved from file:///C:/Users/tpneher/Downloads/blackhawk1%20(6).pdf

31. Chopra I., Hawkey P. M., & Hinton M. (1992). Tetracyclines, molecular and clinical aspects. Journal of Antimicrobial Chemotherapy, 29(3), 245–277. doi: 10.1093/jac/29.3.245 1592696

32. Fohner A. E., Sparreboom A., Altman R. B., & Klein T. E. (2017). PharmGKB summary: Macrolide antibiotic pathway, pharmacokinetics/pharmacodynamics. Pharmacogenetics and genomics, 27(4), 164–167. doi: 10.1097/FPC.0000000000000270 28146011

33. Dobriyal P., Badola R., Tuboi C., & Hussain S. A. (2017). A review of methods for monitoring streamflow for sustainable water resource management. Applied Water Science, 7(6), 2617–2628. doi: 10.1007/s13201-016-0488-y

34. APHA. (1998). Standard Methods for the Examination of Water and Wastewater. American Public Health Association.

35. CLSI. (2010). Performance standards for antimicrobial susceptibility testing; twentieth informational supplement Clinical and Laboratory Standards Institute: CLSI Wayne, PA.

36. Stedtfeld R. D., Guo X., Stedtfeld T. M., Sheng H., Williams M. R., Hauschild K., et al. (2018). Primer set 2.0 for highly parallel qPCR array targeting antibiotic resistance genes and mobile genetic elements. FEMS Microbiology Ecology, 94(9). doi: 10.1093/femsec/fiy130 30052926

37. Schmittgen T. D., & Livak K. J. (2008). Analyzing real-time PCR data by the comparative CT method. Nature Protocols, 3, 1101. doi: 10.1038/nprot.2008.73 18546601

38. Mishra A., Benham B. L., & Mostaghimi S. (2008). Bacterial Transport from Agricultural Lands Fertilized with Animal Manure. Water, Air, and Soil Pollution, 189(1), 127–134. doi: 10.1007/s11270-007-9561-3

39. Thurston-Enriquez J. A., Gilley J. E., & Eghball B. (2005). Microbial quality of runoff following land application of cattle manure and swine slurry. Journal of Water and Health, 3(2), 157–171. doi: 10.2166/wh.2005.0015 16075941

40. Warnemuende, E. A., Kanwar, R. S., Baker, J. L., Lorimor, J. C., Mickelson, S., & S.W. Melvin, a. (2001). INDICATOR BACTERIA IN SUBSURFACE DRAIN WATER FOLLOWING SWINE MANURE APPLICATION. Paper presented at the 2001 ASAE Annual Meeting, St. Joseph, MI. http://elibrary.asabe.org/abstract.asp?aid=4425&t=5

41. Díaz F. J., O’Geen A. T., & Dahlgren R. A. (2010). Efficacy of constructed wetlands for removal of bacterial contamination from agricultural return flows. Agricultural Water Management, 97(11), 1813–1821. https://doi.org/10.1016/j.agwat.2010.06.015

42. Richkus J., Wainger L. A., & Barber M. C. (2016). Pathogen reduction co-benefits of nutrient best management practices. PeerJ, 4, e2713. doi: 10.7717/peerj.2713 27904807

43. Soni B., Bartelt-Hunt S. L., Snow D. D., Gilley J. E., Woodbury B. L., Marx D. B., et al (2015). Narrow Grass Hedges Reduce Tylosin and Associated Antimicrobial Resistance Genes in Agricultural Runoff. Journal of Environmental Quality, 44, 895–902. doi: 10.2134/jeq2014.09.0389 26024269

44. McKinney C. W., Dungan R. S., Moore A., & Leytem A. B. (2018). Occurrence and abundance of antibiotic resistance genes in agricultural soil receiving dairy manure. FEMS Microbiology Ecology, 94(3). doi: 10.1093/femsec/fiy010 29360961

45. Van Goethem M. W., Pierneef R., Bezuidt O. K. I., Van De Peer Y., Cowan D. A., et al. (2018). A reservoir of 'historical' antibiotic resistance genes in remote pristine Antarctic soils. Microbiome, 6(1), 40–40. doi: 10.1186/s40168-018-0424-5 29471872

46. Zhang Y.-J., Hu H.-W., Gou M., Wang J.-T., Chen D., & He J.-Z. (2017). Temporal succession of soil antibiotic resistance genes following application of swine, cattle and poultry manures spiked with or without antibiotics. Environmental Pollution, 231, 1621–1632. doi: 10.1016/j.envpol.2017.09.074 28964602

47. Fahrenfeld N., Knowlton K., Krometis L. A., Hession W. C., Xia K., Lipscomb E., et al. (2014). Effect of Manure Application on Abundance of Antibiotic Resistance Genes and Their Attenuation Rates in Soil: Field-Scale Mass Balance Approach. Environmental Science & Technology, 48(5), 2643–2650. doi: 10.1021/es404988k 24483241

48. Berendsen B. J. A., Lahr J., Nibbeling C., Jansen L. J. M., Bongers I. E. A., Wipfler E. L., et al. (2018). The persistence of a broad range of antibiotics during calve, pig and broiler manure storage. Chemosphere, 204, 267–276. doi: 10.1016/j.chemosphere.2018.04.042 29660540

49. Li B.-B., Shen J.-Z., Cao X.-Y., Wang Y., Dai L., Huang S.-Y.,et al. (2010). Mutations in 23S rRNA gene associated with decreased susceptibility to tiamulin and valnemulin in Mycoplasma gallisepticum. FEMS Microbiology Letters, 308(2), 144–149. doi: 10.1111/j.1574-6968.2010.02003.x 20487023

50. Miller K., Dunsmore C. J., Fishwick C. W. G., & Chopra I. (2008). Linezolid and Tiamulin Cross-Resistance in &lt;em&gt;Staphylococcus aureus&lt;/em&gt; Mediated by Point Mutations in the Peptidyl Transferase Center. Antimicrobial Agents and Chemotherapy, 52(5), doi: 10.1128/AAC.01015-07 1737

51. Pringle M., Poehlsgaard J., Vester B., & Long K. S. (2004). Mutations in ribosomal protein L3 and 23S ribosomal RNA at the peptidyl transferase centre are associated with reduced susceptibility to tiamulin in Brachyspira spp. isolates. Molecular Microbiology, 54(5), 1295–1306. doi: 10.1111/j.1365-2958.2004.04373.x 15554969

52. Paukner S., & Riedl R. (2017). Pleuromutilins: Potent Drugs for Resistant Bugs-Mode of Action and Resistance. Cold Spring Harb Perspect Med, 7(1). doi: 10.1101/cshperspect.a027110 27742734

53. Allen H. K., Donato J., Wang H. H., Cloud-Hansen K. A., Davies J., & Handelsman J. (2010). Call of the wild: antibiotic resistance genes in natural environments. Nat Rev Microbiol, 8(4), 251–259. doi: 10.1038/nrmicro2312 20190823

54. Storteboom H., Arabi M., Davis J. G., Crimi B., & Pruden A. (2010). Tracking Antibiotic Resistance Genes in the South Platte River Basin Using Molecular Signatures of Urban, Agricultural, And Pristine Sources. Environmental Science & Technology, 44(19), 7397–7404. doi: 10.1021/es101657s 20809616

55. Hill R., Keely S., Brinkman N., Wheaton E., Leibowitz S., Jahne M., et al. (2018). The Prevalence of Antibiotic Resistance Genes in US Waterways and Their Relationship to Water Quality and Land Use Indicators.

56. Zhou Z.-C., Feng W.-Q., Han Y., Zheng J., Chen T., Wei Y.-Y., et al. (2018). Prevalence and transmission of antibiotic resistance and microbiota between humans and water environments. Environment International, 121, 1155–1161. doi: 10.1016/j.envint.2018.10.032 30420129

57. Ghanbari F., Ghajavand H., Havaei R., Jami M.-S., Khademi F., Heydari L., et al. (2016). Distribution of erm genes among Staphylococcus aureus isolates with inducible resistance to clindamycin in Isfahan, Iran. Advanced biomedical research, 5, 62–62. doi: 10.4103/2277-9175.179184 27135031

58. Jechalke S., Heuer H., Siemens J., Amelung W., & Smalla K. (2014). Fate and effects of veterinary antibiotics in soil. Trends in Microbiology, 22(9), 536–545. doi: 10.1016/j.tim.2014.05.005 24950802


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