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Fertilization with Poultry Litter Increases the Abundance of Antibiotic-Resistant Bacteria in Tropical Soil: a Microcosm Study

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Abstract

Various antimicrobial agents are used in the poultry industry to treat microbial infections and prevent disease or as growth promoters. As a result, poultry litter (PL) can contain antibiotic residues (AR), antibiotic-resistant bacteria (ARB), and antibiotic resistance genes. Still, PL is used in many countries as a fertilizer and feed supplement for cattle. To evaluate whether usage of PL in agriculture leads to the accumulation of AR and ARB accumulate in the soil, we (i) measured the concentration of monensin, tylosin, ciprofloxacin, oxytetracycline, and chlortetracycline and the abundance of culturable monensin-, tylosin-, and ciprofloxacin-resistant bacteria in 15 commercial PL samples and (ii) exposed soil microcosms to two PL regimes and followed the persistence of PL-associated ARB for 128 days through cultivation on media containing antibiotics. The PL samples analyzed contained high concentrations of monensin (27–95 mg kg−1), tylosin (152–450 mg kg−1), ciprofloxacin (29–101 mg kg−1), and (oxy/chlor)tetracycline (13–87 mg kg−1). Congruently, they included large absolute and relative numbers of bacteria capable of growing on agar plates supplemented with 5 to 50 μg mL−1 monensin (medians, 107–109 CFU g−1, 0.6–45%) or 25 to 50 μg mL−1 tylosin (median, 108 CFU g−1, 14–26%). By contrast, the abundance of bacteria resistant to 25–250 μg mL−1 CP in the PL samples was much lower (median values ranging from 106 to less than 102 CFU g−1, relative abundances, < 0.13%). We observed rapid increments of 1–3 logs in the amount of culturable tylosin- and CP-resistant bacteria in most microcosms upon fertilization (n = 3/4 and n = 5/8, respectively, p < 0.01). Half of these increments were sustained across the experiment (p < 0.05), demonstrating that the introduced ARB can thrive in soil. These results show that fertilization with PL can increase the basal amount of tylosin- and CP-resistant bacteria in the soil. The environmental and sanitary consequences of this finding justify changes in PL’s manufacturing process and a debate on its approved uses in agricultural systems.

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Acknowledgements

The authors thank Astrid Leiva and Alfonso García for their help with the references and statistical analysis, respectively.

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There is no external funding to declare. The research was funded by the Vice Rectory Office for Research of the Universidad de Costa Rica (grant number B1038).

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  1. Centro de Investigación en Enfermedades Tropicales (CIET) & Facultad de Microbiología, Universidad de Costa Rica, Ciudad Universitaria Rodrigo Facio, 11501-2060, San José, Costa Rica

    Carolina Chaves-Ulate & César Rodríguez

  2. Centro Nacional de Ciencia y Tecnología de Alimentos (CITA), Universidad de Costa Rica, Ciudad Universitaria Rodrigo Facio, 11501-2060, San José, Costa Rica

    Fabio Granados-Chinchilla

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  1. Carolina Chaves-Ulate
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Table 3 Average composition and chemical analysis of n = 15 poultry litter samples collected at eight Costa Rican farms
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Chaves-Ulate, C., Granados-Chinchilla, F. & Rodríguez, C. Fertilization with Poultry Litter Increases the Abundance of Antibiotic-Resistant Bacteria in Tropical Soil: a Microcosm Study. Water Air Soil Pollut 232, 402 (2021). https://doi.org/10.1007/s11270-021-05347-1

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