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Antibiotic resistome and associated bacterial communities in agricultural soil following the amendments of swine manure–derived fermentation bed waste

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Abstract

The practice of utilizing animal manures on land is widespread in agriculture, but it has raised concerns about the possible spread of antibiotic resistance genes (ARGs) and the potential risk it poses to public health through food production. Fermentation bed culture is an effective circular agricultural practice commonly utilized in pig farming that minimizes the environmental impact of livestock farming. However, this method generates a significant amount of fermentation bed waste (FBW), which can be turned into organic fertilizer for land application. The objective of this research was to examine the impacts of amending agricultural soil samples with swine manure–derived FBW on microbial communities, mobile genetic elements (MGEs), and ARG profiles over different periods. The study findings indicated that the amendment of swine manure–derived FBW significantly increased the diversity and abundance of ARGs and MGEs during the early stages of amendment, but this effect diminished over time, and after 12 months of FBW amendments, the levels returned to those comparable to control samples. The shift in the bacterial communities played a significant role in shaping the patterns of ARGs. Actinobacteriota, Proteobacteria, and Bacteroidetes were identified as the primary potential hosts of ARGs through metagenomic binning analysis. Furthermore, the pH of soil samples was identified as the most important property in driving the composition of the bacterial community and soil resistome. These findings provided valuable insights into the temporal patterns and dissemination risks of ARGs in FBW-amended agriculture soil, which could contribute to the development of effective strategies to manage the dissemination risks of FBW-derived ARGs.

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Data availability

The raw metagenomic sequence data were publicly available in the NCBI BioProject database with the accession number of PRJNA953804.

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Acknowledgements

This work was supported by Fujian Special Fund for Scientific Research Institutes in the Public Interest (2020R1034002); Natural Science Foundation of Xiamen, China (3502Z202272400); and external cooperation project of Fujian Academy of Agricultural Sciences (DWHZ2021-15). The authors thank Yunfeng Agricultural and Animal Husbandry Cooperative, Maiping Li from the Baota District Animal Husbandry and Veterinary Service Center, and Xiyong Zhang for assisting with the sampling process.

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Zhizhen Pan, conceptualization, methodology, investigation, writing (original draft), visualization, data curation; Zheng Chen, methodology, investigation, resources; Liting Zhu, methodology, software, formal analysis; Ricardo David Avellán-Llaguno, methodology, software, formal analysis; Bo Liu, writing (review and editing), funding acquisition; Qiansheng Huang: conceptualization, methodology, writing (original draft), writing (review and editing), visualization, supervision, funding acquisition. All authors contributed to the article and approved the submitted version.

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Correspondence to Qiansheng Huang.

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Pan, Z., Chen, Z., Zhu, L. et al. Antibiotic resistome and associated bacterial communities in agricultural soil following the amendments of swine manure–derived fermentation bed waste. Environ Sci Pollut Res 30, 104520–104531 (2023). https://doi.org/10.1007/s11356-023-29691-3

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  • DOI: https://doi.org/10.1007/s11356-023-29691-3

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