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Tetracyclines and Tetracycline Resistance in Agricultural Soils: Microcosm and Field Studies

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Abstract

The influence of the use of antibiotics on the prevalence of resistance genes in the environment is still poorly understood. We studied the diversity of tetracycline and sulfonamide resistance genes as influenced by fertilization with pig manure in soil microcosms and at two field locations. Manure contained a high diversity of resistance genes, regardless of whether it stemmed from a farm operation with low or regular use of antibiotics. In the microcosm soils, the influence of fertilization with manure was clearly shown by an increase in the number of resistance genes in the soil after manuring. Spiking of the tetracycline compounds to the microcosms had only little additional impact on the diversity of resistance genes. Overall, the tetracycline resistance genes tet(T), tet(W), and tet(Z) were ubiquitous in soil and pig slurries, whereas tet(Y), tet(S), tet(C), tet(Q), and tet(H) were introduced to the microcosm soil by manuring. The diversity of tetracycline and sulfonamide [sul(1), sul(2), and sul(3)] resistance genes on a Swiss pasture was very high even before slurry amendment, although manure from intensive farming had not been applied in the previous years. The additional effect of manuring was small, with the tetracycline and sulfonamide resistance diversity staying at high levels for the complete growth season. At an agricultural field site in Germany, the diversity of tetracycline and sulfonamide resistance genes was considerably lower, possibly reflecting regional differences in gene diversity. This study shows that there is a considerable pool of resistance genes in soils. Although it is not possible to conclude whether this diversity is caused by the global spread of resistance genes after 50 years of tetracycline use or is due to the natural background in soil resistance genes, it highlights a role that environmental reservoirs might play in resistance gene capture.

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Acknowledgments

We thank Joanne Chee-Sanford and Vincent Perreten for providing DNA extracts of the positive control strains; Remy Hillekens, Rogier Doornbos, and Karel Wernars for advice and technical assistance; Heinrich Höper (Geological Survey of Lower Saxony, Germany) for experimental setup and sampling of the German field study; and Jan-Dirk van Elsas for critically commenting on the progress of work. The Swiss field study was partly financed by the Swiss National Research Program NRP49 “Antibiotic Resistance” (4049-63282) and the Swiss Agency for the Environment, Forests and Landscape (SAEFL).

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Authors and Affiliations

  1. Institute for Risk Assessment Sciences (IRAS), Utrecht University, PO Box 80176, 3508 TD, Utrecht, The Netherlands

    Heike Schmitt & Willem Seinen

  2. EAWAG, Dübendorf, Switzerland

    Krispin Stoob

  3. Department of Food Toxicology, University of Veterinary Medicine Hannover, Foundation, Hannover, Germany

    Gerd Hamscher

  4. RIVM, Bilthoven, The Netherlands

    Eric Smit

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  1. Heike Schmitt
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Correspondence to Heike Schmitt.

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Schmitt, H., Stoob, K., Hamscher, G. et al. Tetracyclines and Tetracycline Resistance in Agricultural Soils: Microcosm and Field Studies. Microb Ecol 51, 267–276 (2006). https://doi.org/10.1007/s00248-006-9035-y

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