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Bacterial communities regulate temporal variations of the antibiotic resistome in soil following manure amendment

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Abstract

The increasing emergence of antibiotic-resistant genes (ARGs) represents a global threat to human health. Land application of animal manure is known to contribute considerably to the propagation and dispersal of antibiotic resistance in agro-ecosystems. Yet, the primary determinants of the fate of the soil resistome remain obscure. In this study, a pot experiment was conducted to examine temporal changes in ARGs, mobile genetic elements (MGEs), and bacterial communities in a weakly developed loamy soil (an entisol known as calcareous purple soil) upon addition of pig or chicken manure. On the day of manure application, substantial increases in the diversity and relative abundance of ARGs were observed in soil amended with raw pig manure. At the same time, no obvious changes were observed for soil amended with chicken manure. Antibiotic resistance in pig manure-amended soils rapidly decreased over time to a level that was still higher than that of unamended soil at 100 days after manure application. The results of the Mantel test and Procrustes analysis indicated that ARG profiles in soil were significantly correlated with the structure of the bacterial phylogeny. Variation partitioning analysis further revealed that the bacterial community played a major role in regulating the temporal changes in ARGs in soil following manure application. Increased numbers and relative abundances of MGEs and their significant positive correlations with ARGs were observed, which suggest that a potential contribution from lateral gene transfer to the persistence and spread of ARGs should not be overlooked. Overall, our findings provide a better understanding of the mechanisms underlying the dynamics of ARGs in entisols following manure application and have practical implications for managing manure applications in entisols of the study area and other areas.

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All data generated or analyzed during this study are included in this published article and its supplementary information files.

Funding

This study was financially supported by the National Key Research and Development Program of China (Grant No. 2016YFD0800203), the Major Science and Technology Program of Sichuan Province (Grant No. 2018SZDZX0029), the National Natural Science Foundation of China (Grant Nos. 42007361 and 41771521), and the 135 Strategic Program of the CAS Institute of Mountain Hazards and Environment (Grant No. SDS-135-1702).

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  1. Key Laboratory of Mountain Surface Processes and Ecological Regulation, Institute of Mountain Hazards and Environment, Chinese Academy of Sciences, Chengdu, 610041, China

    Jianhua Cheng, Xiangyu Tang & Chen Liu

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  1. Jianhua Cheng
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Jianhua Cheng and Chen Liu did the incubation experiments and laboratory analyses. Jianhua Cheng performed the statistical analyses and wrote the first draft of this manuscript. Xiangyu Tang supervised the project and completed the final version of the manuscript. All authors improved and approved the final manuscript.

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Correspondence to Xiangyu Tang.

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Cheng, J., Tang, X. & Liu, C. Bacterial communities regulate temporal variations of the antibiotic resistome in soil following manure amendment. Environ Sci Pollut Res 28, 29241–29252 (2021). https://doi.org/10.1007/s11356-021-12746-8

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