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Insights into the fates of plasmids and antimicrobial resistance genes during swine manure treatment and related factors based on plasmidome and metagenome analyses

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Abstract

Swine manure treatment plants are important reservoirs of plasmid-harboring antibiotic resistance genes (ARGs) and physicochemical contaminants, but the changes in the abundances of plasmids and ARGs, and their interactions with the physicochemical properties of manure, are still unclear. Thus, in the present study, plasmidome and metagenome analyses were conducted for samples collected at different stages in the swine manure treatment process. The results indicated that anaerobic digestion and aerobic digestion were the most efficient stages for reducing the abundances of ARGs in swine manure. However, the plasmids associated with ARGs were not effectively removed in these stages. Through the whole treatment process, the IncL/M, IncQ1, IncHI2A, IncA/C, and IncN plasmid groups had strong correlations (r > 0.8, P < 0.01) with most ARG types, thereby indicating that these plasmids play important roles in the persistence of ARGs in this environment. Furthermore, the pH, total nitrogen, total phosphorus, and four heavy metals (Cu, Zn, As, and Fe) significantly affected the abundances of seven ARG subtypes (tetB(P), ant(6)-Ia, tet44, aph(3′′)-Ib, mefB, tet(L), and tet(39)). In particular, florfenicol had the most positive correlations with ARGs. Our results indicated that nutrients, heavy metals, and antibiotics all contributed to the presence and persistence of plasmid-harboring ARGs. This study provides insights into the fate of plasmids and ARGs, and related factors during the swine manure treatment process, thereby facilitating the development of a new treatment technique for removing ARGs and reducing the public health risk associated with livestock production.

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Data availability

All of the sequences in the plasmid database analyzed in the present study are available via the NCBI RefSeq repository (https://ftp.ncbi.nlm.nih.gov/refseq/release/plasmid/) (2020–11-16). The nucleotide sequences in the plasmidome and metagenome were deposited in the GSA database, and they are publicly available under accession number PRJCA004346.

Code availability

The code used in this study to generate the plasmid database is available at Github (https://gist.github.com/Alice-shui/88d39ffe3509172e32826772b5b88aa6).

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Funding

This study was supported by the General Program of National Natural Science Foundation of China (grant number [U21A20257]), Key R&D Program of Sichuan province (grant numbers [22ZDZX0011], [2020ZYD003], [2020YFN0147], and [2021YFH0192]), and Project of Science and Technology Bureau of Banan District Chongqing (grant number [BN2020-115]).

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Authors and Affiliations

  1. Animal Disease Prevention and Food Safety Key Laboratory of Sichuan Province, Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, 29 Wangjiang Road, Chengdu, 610010, NOSichuan, China

    Junrui Shui, Hongmei Tuo, Jingyi Feng, Yuxuan Feng, Wen Su, Cong Lin, Haoyu Zhang, Zunfang Tu, Hongning Wang & Anyun Zhang

  2. Laboratory of Gastrointestinal Microbiology, Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing, 210095, China

    Jinxin Liu

  3. Central Agricultural Broadcasting and Television School (Banan, Chongqing), Chongqing, 401320, China

    Xialan Zhang

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  1. Junrui Shui
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  12. Anyun Zhang
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Contributions

Conceptualization: Junrui Shui, Hongmei Tuo, Anyun Zhang; Methodology: Junrui Shui, Hongmei Tuo, Anyun Zhang; formal analysis and investigation: Hongmei Tuo, Junrui Shui; writing—original draft: Junrui Shui, Hongmei Tuo, Jinxin Liu, Anyun Zhang; writing—review & editing: Junrui Shui, Anyun Zhang, Jinxin Liu, Xialan Zhang, Jingyi Feng, Yuxuan Feng, Wen Su, Cong Lin, Haoyu Zhang, Zunfang Tu; funding acquisition: Anyun Zhang, Hongning Wang.

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Correspondence to Anyun Zhang.

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Shui, J., Tuo, H., Liu, J. et al. Insights into the fates of plasmids and antimicrobial resistance genes during swine manure treatment and related factors based on plasmidome and metagenome analyses. Environ Sci Pollut Res 29, 69037–69047 (2022). https://doi.org/10.1007/s11356-022-20574-7

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