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Investigating the dispersal of antibiotic resistance associated genes from manure application to soil and drainage waters in simulated agricultural farmland systems


Autoři: Schuyler D. Smith aff001;  Phillip Colgan aff002;  Fan Yang aff002;  Elizabeth L. Rieke aff002;  Michelle L. Soupir aff002;  Thomas B. Moorman aff003;  Heather K. Allen aff003;  Adina Howe aff001
Působiště autorů: Bioinformatics and Computational Biology Department, Iowa State University, Ames, Iowa, United States of America aff001;  Department of Agricultural and Biosystems Engineering, Iowa State University, Ames, Iowa, United States of America aff002;  United States Department of Agriculture, Agricultural Research Service, Ames, Iowa, United States of America aff003
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0222470

Souhrn

Manure from animals that have been treated with antibiotics is often used to fertilize agricultural soils and its application has previously been shown to enrich for genes associated with antibiotic resistance in agroecosystems. To investigate the magnitude of this effect, we designed a column experiment simulating manure-treated agricultural soil that utilizes artificial subsurface drainage to determine the duration and extent which this type of manure fertilization impacts the set of genes associated with antibiotic resistance in drainage water. We classified ARGs in manure-treated drainage effluent water by its source of origin. Overall, we found that 61% and 7% of the total abundance of ARGs found in drainage water samples could be attributed to manure enrichment and manure addition, respectively. Among these ARGs, we identified 75 genes unique to manure that persisted in both soil and drainage water throughout a drainage season typical of the Upper Midwestern United States. While most of these genes gradually decreased in abundance over time, the IS6100-associated tet(33) gene accrued. These results demonstrate the influence of manure applications on the composition of the resistome observed in agricultural drainage water and highlight the importance of anthropogenic ARGs in the environment.

Klíčová slova:

Biology and life sciences – Microbiology – Microbial control – Antimicrobials – Antibiotics – Tetracyclines – Agriculture – Agricultural soil science – Genetics – Genomics – Metagenomics – Molecular biology – Molecular biology techniques – Cloning – DNA cloning – Shotgun sequencing – Organisms – Eukaryota – Animals – Vertebrates – Amniotes – Mammals – Swine – Medicine and health sciences – Pharmacology – Antimicrobial resistance – Antibiotic resistance – Drugs – Ecology and environmental sciences – Limnology – Effluent – Soil science – Earth sciences – Marine and aquatic sciences – Research and analysis methods – Sequencing techniques


Zdroje

1. Inoue H, Minghui R. Antimicrobial resistance: translating political commitment into national action. Bull World Health Organ. 2017;95(4):242–242. doi: 10.2471/BLT.17.191890 28479615

2. Review on Antimicrobial Resistance [Internet]. Antimicrobial Resistance: Tackling a Crisis for the Health and Wealth of Nations. 2014 [cited 2019 Sep 4]. Available from: https://amr-review.org/sites/default/files/AMR Review Paper - Tackling a crisis for the health and wealth of nations_1.pdf

3. Van Boeckel TP, Brower C, Gilbert M, Grenfell BT, Levin SA, Robinson TP, et al. Global trends in antimicrobial use in food animals. Proc Natl Acad Sci U S A [Internet]. 2015;112(18):5649–54. Available from: http://www.ncbi.nlm.nih.gov/pubmed/25792457%0Ahttp://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=PMC4426470 doi: 10.1073/pnas.1503141112 25792457

4. Rogers Van Katwyk S, Grimshaw JM, Mendelson M, Taljaard M, Hoffman SJ. Government policy interventions to reduce human antimicrobial use: protocol for a systematic review and meta-analysis. Syst Rev [Internet]. 2017 Dec 13 [cited 2019 Feb 5];6(1):256. Available from: http://www.ncbi.nlm.nih.gov/pubmed/29237496 doi: 10.1186/s13643-017-0640-2 29237496

5. Davies J, Davies D. Origins and Evolution of Antibiotic Resistance. Microbiol Mol Biol Rev [Internet]. 2010 [cited 2019 Feb 11];74(3):1092–2172. Available from: http://mmbr.asm.org/

6. Phillips I, Casewell M, Cox T, De Groot B, Friis C, Jones R, et al. Does the use of antibiotics in food animals pose a risk to human health? A critical review of published data. J Antimicrob Chemother. 2004;53(1):28–52. doi: 10.1093/jac/dkg483 14657094

7. Zhu Y-G, Johnson TA, Su J-Q, Qiao M, Guo G-X, Stedtfeld RD, et al. Diverse and abundant antibiotic resistance genes in Chinese swine farms. Proc Natl Acad Sci [Internet]. 2013;110(9):3435–40. Available from: http://www.pnas.org/lookup/doi/10.1073/pnas.1222743110 23401528

8. Looft T, Johnson TA, Allen HK, Bayles DO, Alt DP, Stedtfeld RD, et al. In-feed antibiotic effects on the swine intestinal microbiome. Proc Natl Acad Sci [Internet]. 2012;109(5):1691–6. Available from: http://www.pnas.org/cgi/doi/10.1073/pnas.1120238109 22307632

9. You Y, Silbergeld EK. Learning from agriculture: Understanding low-dose antimicrobials as drivers of resistome expansion. Front Microbiol. 2014;5(JUN):1–10.

10. Udikovic-Kolic N, Wichmann F, Broderick NA, Handelsman J. Bloom of resident antibiotic-resistant bacteria in soil following manure fertilization. Proc Natl Acad Sci. 2014;111(42):15202–7. doi: 10.1073/pnas.1409836111 25288759

11. Chen Q, An X, Li H, Su J, Ma Y, Zhu YG. Long-term field application of sewage sludge increases the abundance of antibiotic resistance genes in soil. Environ Int. 2016;92–93:1–10. doi: 10.1016/j.envint.2016.03.026 27043971

12. Yu Z, Gunn L, Wall P, Fanning S. Antimicrobial resistance and its association with tolerance to heavy metals in agriculture production. Food Microbiol. 2017;64:23–32. doi: 10.1016/j.fm.2016.12.009 28213031

13. Wu N, Qiao M, Zhang B, Cheng W Da, Zhu YG. Abundance and diversity of tetracycline resistance genes in soils adjacent to representative swine feedlots in China. Environ Sci Technol. 2010;44(18):6933–9. doi: 10.1021/es1007802 20707363

14. Jechalke S, Heuer H, Siemens J, Amelung W, Smalla K. Fate and effects of veterinary antibiotics in soil. Trends Microbiol [Internet]. 2014 Sep 1 [cited 2019 Feb 5];22(9):536–45. Available from: https://www.sciencedirect.com/science/article/pii/S0966842X14001140?via%3Dihub doi: 10.1016/j.tim.2014.05.005 24950802

15. Rieke EL, Moorman TB, Douglass EL, Soupir ML. Seasonal variation of macrolide resistance gene abundances in the South Fork Iowa River Watershed. Sci Total Environ [Internet]. 2018;610–611:1173–9. Available from: https://doi.org/10.1016/j.scitotenv.2017.08.116 28847138

16. Zucker, Brown. Agricultural Drainage Bulletin 871–98. 1998; Available from: http://ohioline.osu.edu/b871/b871_4.html

17. Van Goethem MW, Pierneef R, Bezuidt OKI, Van De Peer Y, Cowan DA, Makhalanyane TP. A reservoir of ‘historical’ antibiotic resistance genes in remote pristine Antarctic soils. Microbiome [Internet]. 2018;6(40):12. Available from: https://doi.org/10.1186/s40168-018-0424-5

18. Dinnes DL, Karlen DL, Jaynes DB, Kaspar TC, Hatfield JL, Colvin TS, et al. Nitrogen Management Strategies to Reduce Nitrate Leaching in Tile-Drained Midwestern Soils. Agron J. 2002;94(1):153.

19. Helmers MJ, Zhou X, Asbjornsen H, Kolka R, Tomer MD, Cruse RM. Sediment Removal by Prairie Filter Strips in Row-Cropped Ephemeral Watersheds. J Environ Qual. 2012;41:1531. doi: 10.2134/jeq2011.0473 23099945

20. McIsaac GF, Hu X. Net N input and riverine N export from Illinois agricultural watersheds with and without extensive tile drainage. Biogeochemistry. 2004 Sep;70(2):253–73.

21. Dale VH, Wright D, Kling CL, Boynton W, Meyer JL, Mankin K, et al. Hypoxia in the Northern Gulf of Mexico. New York, NY: Springer New York; 2010. (Springer Series on Environmental Management).

22. Garder JL, Moorman TB, Soupir ML. Transport and Persistence of Tylosin-Resistant Enterococci, erm Genes, and Tylosin in Soil and Drainage Water from Fields Receiving Swine Manure. J Environ Qual—Surf Water Qual. 2014;43(4):1484–93.

23. Luby EM, Moorman TB, Soupir ML. Fate and transport of tylosin-resistant bacteria and macrolide resistance genes in artificially drained agricultural fields receiving swine manure. Sci Total Environ [Internet]. 2016;550:1126–33. Available from: https://doi.org/10.1016/j.scitotenv.2016.01.132 26874610

24. Pruden A, Pei R, Storteboom H, Carlson KH. Antibiotic resistance genes as emerging contaminants: Studies in northern Colorado. Environ Sci Technol. 2006;40(23):7445–50. doi: 10.1021/es060413l 17181002

25. D’Costa VM, King CE, Kalan L, Morar M, Sung WWL, Schwarz C, et al. Antibiotic resistance is ancient. Nature [Internet]. 2011 Sep [cited 2019 Feb 11];477(7365):457–61. Available from: http://www.nature.com/articles/nature10388 doi: 10.1038/nature10388 21881561

26. Allen HK, Donato J, Wang HH, Cloud-Hansen KA, Davies J, Handelsman J. Call of the wild: antibiotic resistance genes in natural environments. Nat Rev Microbiol [Internet]. 2010 Apr 1 [cited 2019 Feb 11];8(4):251–9. Available from: http://www.nature.com/articles/nrmicro2312 doi: 10.1038/nrmicro2312 20190823

27. Allen HK, Moe LA, Rodbumrer J, Gaarder A, Handelsman J. Functional metagenomics reveals diverse Β-lactamases in a remote Alaskan soil. ISME J. 2009;3(2):243–51. doi: 10.1038/ismej.2008.86 18843302

28. Martinez JL. The role of natural environments in the evolution of resistance traits in pathogenic bacteria. 2009;(April):2521–30.

29. Martínez JL. Natural Antibiotic Resistance and Contamination by Antibiotic Resistance Determinants: The Two Ages in the Evolution of Resistance to Antimicrobials. Front Microbiol. 2012;3(January):2010–2.

30. Section S, Rieke EL, Moorman TB, Soupir ML, Yang F, Howe A. Assessing Pathogen Presence in an Intensively Tile Drained, Agricultural Watershed. 2018;

31. Rieke EL, Soupir ML, Moorman TB, Yang F, Howe AC. Temporal Dynamics of Bacterial Communities in Soil and Leachate Water After Swine Manure Application. Front Microbiol. 2018;9.

32. Bolger AM, Lohse M, Usadel B. Genome analysis Trimmomatic: a flexible trimmer for Illumina sequence data. 2014 [cited 2019 Sep 5];30(15):2114–20. Available from: http://www.usadellab.org/cms/index

33. Mcarthur AG, Waglechner N, Nizam F, Yan A, Azad MA, Baylay AJ, et al. The Comprehensive Antibiotic Resistance Database. 2013 [cited 2019 Sep 5]; Available from: http://innatedb.ca/

34. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;

35. Fish JA, Chai B, Wang Q, Sun Y, Brown CT, Tiedje JM, et al. FunGene: The functional gene pipeline and repository. Front Microbiol. 2013;4(OCT):1–14.

36. McMurdie PJ, Holmes S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One. 2013 Jan;8(4):e61217. doi: 10.1371/journal.pone.0061217 23630581

37. Smith S. Phylosmith: an R-package for reproducible and efficient microbiome analysis with phyloseq-objects. J Open Source Softw. 2019;4(38).

38. Wagner J. vegan: Community Ecology Package. 2019; Available from: https://cran.r-project.org/package=vegan

39. Martinez JL, Sánchez MB, Martínez-Solano L, Hernandez A, Garmendia L, Fajardo A, et al. Functional role of bacterial multidrug efflux pumps in microbial natural ecosystems. FEMS Microbiol Rev [Internet]. 2009 Mar 1 [cited 2019 Feb 12];33(2):430–49. Available from: https://academic.oup.com/femsre/article-lookup/doi/10.1111/j.1574-6976.2008.00157.x 19207745

40. Groh JL, Luo Q, Ballard JD, Krumholz LR. Genes that enhance the ecological fitness of Shewanella oneidensis MR-1 in sediments reveal the value of antibiotic resistance. Appl Environ Microbiol [Internet]. 2007 Jan [cited 2019 Feb 12];73(2):492–8. Available from: http://www.ncbi.nlm.nih.gov/pubmed/17114320 doi: 10.1128/AEM.01086-06 17114320

41. Poole K. Efflux-mediated antimicrobial resistance. Antibiotic Discovery and Development. 2014. 349–395 p.

42. Abril C, Brodard I, Perreten V. Two novel antibiotic resistance genes, tet(44) and ant(6)-Ib, are located within a transferable pathogenicity island in Campylobacter fetus subsp. fetus. Antimicrob Agents Chemother [Internet]. 2010/05/17. 2010 Jul;54(7):3052–5. Available from: https://www.ncbi.nlm.nih.gov/pubmed/20479200 doi: 10.1128/AAC.00304-10 20479200

43. Tauch A, Götker S, Pühler A, Kalinowski J, Thierbach G. The 27.8-kb R-plasmid pTET3 from Corynebacterium glutamicum encodes the aminoglycoside adenyltransferase gene cassette aadA9 and the regulated tetracycline efflux system Tet 33 flanked by active copies of the widespread insertion sequence IS6100. Plasmid. 2002;48(2):117–29. 12383729

44. Marti R, Tien Y-C, Murray R, Scott A, Sabourin L, Topp E. Safely Coupling Livestock and Crop Production Systems: How Rapidly Do Antibiotic Resistance Genes Dissipate in Soil following a Commercial Application of Swine or Dairy Manure? Appl Environ Microbiol. 2014;80(10):3258–65. doi: 10.1128/AEM.00231-14 24632259

45. Riber L, Poulsen PHB, Al-Soud WA, Skov Hansen LB, Bergmark L, Brejnrod A, et al. Exploring the immediate and long-term impact on bacterial communities in soil amended with animal and urban organic waste fertilizers using pyrosequencing and screening for horizontal transfer of antibiotic resistance. FEMS Microbiol Ecol. 2014;90(1):206–24. doi: 10.1111/1574-6941.12403 25087596

46. Muurinen J, Stedtfeld R, Karkman A, Tiedje J, Virta M. Influence of Manure Application on the Environmental Resistome under Finnish Agricultural Practice with Restricted Antibiotic Use. 2017;

47. Johnson TA, Stedtfeld RD, Wang Q, Cole JR, Hashsham SA, Looft T, et al. Clusters of Antibiotic Resistance Genes Enriched Together Stay Together in Swine Agriculture. MBio [Internet]. 2016;7(2):1–11. Available from: http://mbio.asm.org/content/7/2/e02214-15.abstract


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