Field-based evidence for the prevalence of soil antibiotic resistomes under long-term antibiotic-free fertilization

Growing evidence suggests that the use of manure containing residual antibiotics universally leads to an increase in soil antibiotic resistance genes (ARGs). However, there is limited understanding of the influence of long-term antibiotic-free fertilization and the differences between antibiotic-fre...

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Main Authors: Yuhao Fu, Fang Hu, Fang Wang, Min Xu, Zhongjun Jia, Wulf Amelung, Zhi Mei, Xiaozeng Han, Marko Virta, Xin Jiang, James M. Tiedje
Format: Article
Language:English
Published: Elsevier 2025-01-01
Series:Environment International
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Online Access:http://www.sciencedirect.com/science/article/pii/S016041202400789X
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author Yuhao Fu
Fang Hu
Fang Wang
Min Xu
Zhongjun Jia
Wulf Amelung
Zhi Mei
Xiaozeng Han
Marko Virta
Xin Jiang
James M. Tiedje
author_facet Yuhao Fu
Fang Hu
Fang Wang
Min Xu
Zhongjun Jia
Wulf Amelung
Zhi Mei
Xiaozeng Han
Marko Virta
Xin Jiang
James M. Tiedje
author_sort Yuhao Fu
collection DOAJ
description Growing evidence suggests that the use of manure containing residual antibiotics universally leads to an increase in soil antibiotic resistance genes (ARGs). However, there is limited understanding of the influence of long-term antibiotic-free fertilization and the differences between antibiotic-free manure and chemical fertilizer on soil ARGs. This study aimed to quantify the assembly patterns of the antibiotic resistome by in situ probing bacterial community and environmental variations in field soils that have been subjected to long-term exposure to chemical fertilizer and/or manure from animals without antibiotic amendments. Long-term fertilization slightly impacts the diversity of antibiotic resistomes, with 85.5 % of total ARGs and mobile genetic elements (MGEs) being common across all treatment types, while significantly increasing their abundances from 0.68 to a maximum of 0.90 copies/16S rRNA. The rise in ARG abundances was less pronounced when using antibiotic-free manure compared to chemical fertilizer, particularly for Rank Ⅱ ARGs. However, when antibiotic-free manure and chemical fertilizer were combined, a significant increase in nutrients (such as available nitrogen and organic matter) and MGEs occurred, leading to the enrichment of soil microbial populations, especially in certain resistant species, and Rank Ⅰ and Ⅱ ARGs. Despite the influence of various factors like bacterial communities, soil properties, heavy metals, and MGEs, the MGEs had the most significant standardized effects on shaping ARGs through both direct and indirect pathways. Our findings indicates that while of antibiotic-free manure can lower the risk of antibiotic residues and promote sustainable farming practices, it may not fully eliminate the prevalence of ARGs, highlighting the need for more comprehensive strategies to address antibiotic resistance in agriculture rather than simply prohibiting the use of antibiotics.
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spelling doaj-art-8593f0fc336c4365b14809bb5cc26e512025-01-24T04:44:02ZengElsevierEnvironment International0160-41202025-01-01195109202Field-based evidence for the prevalence of soil antibiotic resistomes under long-term antibiotic-free fertilizationYuhao Fu0Fang Hu1Fang Wang2Min Xu3Zhongjun Jia4Wulf Amelung5Zhi Mei6Xiaozeng Han7Marko Virta8Xin Jiang9James M. Tiedje10State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, Nanjing 211135, China; University of Chinese Academy of Sciences, Beijing 100049, ChinaState Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, Nanjing 211135, China; University of Chinese Academy of Sciences, Beijing 100049, China; Chongqing Changan Automobile Co., Ltd., Chongqing 400023, ChinaState Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, Nanjing 211135, China; University of Chinese Academy of Sciences, Beijing 100049, China; Corresponding authors at: University of Chinese Academy of Sciences, Beijing 100049, China.State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, Nanjing 211135, China; University of Chinese Academy of Sciences, Beijing 100049, ChinaUniversity of Chinese Academy of Sciences, Beijing 100049, China; State Key Laboratory of Black Soils Conservation and Utilization, Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Changchun, ChinaAgrosphere Institute (IBG-3), Forschungszentrum Jülich GmbH, Jülich 52428, Germany; Institute of Crop Science and Resource Conservation (INRES)-Soil Science and Soil Ecology, University of Bonn, Bonn, GermanyState Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, Nanjing 211135, China; University of Chinese Academy of Sciences, Beijing 100049, ChinaUniversity of Chinese Academy of Sciences, Beijing 100049, China; Key Laboratory of Mollisols Agroecology, Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Harbin 150081, China; Corresponding authors at: University of Chinese Academy of Sciences, Beijing 100049, China.Department of Microbiology, University of Helsinki, Viikinkaari 9, 00014, FinlandState Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, Nanjing 211135, China; University of Chinese Academy of Sciences, Beijing 100049, ChinaCenter for Microbial Ecology, Department of Plant, Soil and Microbial Sciences, Michigan State University, East Lansing, MI 48824, United StatesGrowing evidence suggests that the use of manure containing residual antibiotics universally leads to an increase in soil antibiotic resistance genes (ARGs). However, there is limited understanding of the influence of long-term antibiotic-free fertilization and the differences between antibiotic-free manure and chemical fertilizer on soil ARGs. This study aimed to quantify the assembly patterns of the antibiotic resistome by in situ probing bacterial community and environmental variations in field soils that have been subjected to long-term exposure to chemical fertilizer and/or manure from animals without antibiotic amendments. Long-term fertilization slightly impacts the diversity of antibiotic resistomes, with 85.5 % of total ARGs and mobile genetic elements (MGEs) being common across all treatment types, while significantly increasing their abundances from 0.68 to a maximum of 0.90 copies/16S rRNA. The rise in ARG abundances was less pronounced when using antibiotic-free manure compared to chemical fertilizer, particularly for Rank Ⅱ ARGs. However, when antibiotic-free manure and chemical fertilizer were combined, a significant increase in nutrients (such as available nitrogen and organic matter) and MGEs occurred, leading to the enrichment of soil microbial populations, especially in certain resistant species, and Rank Ⅰ and Ⅱ ARGs. Despite the influence of various factors like bacterial communities, soil properties, heavy metals, and MGEs, the MGEs had the most significant standardized effects on shaping ARGs through both direct and indirect pathways. Our findings indicates that while of antibiotic-free manure can lower the risk of antibiotic residues and promote sustainable farming practices, it may not fully eliminate the prevalence of ARGs, highlighting the need for more comprehensive strategies to address antibiotic resistance in agriculture rather than simply prohibiting the use of antibiotics.http://www.sciencedirect.com/science/article/pii/S016041202400789XAntibiotic resistomeLong-term fertilizationAntibiotic-free manureBacterial communityBlack soil
spellingShingle Yuhao Fu
Fang Hu
Fang Wang
Min Xu
Zhongjun Jia
Wulf Amelung
Zhi Mei
Xiaozeng Han
Marko Virta
Xin Jiang
James M. Tiedje
Field-based evidence for the prevalence of soil antibiotic resistomes under long-term antibiotic-free fertilization
Environment International
Antibiotic resistome
Long-term fertilization
Antibiotic-free manure
Bacterial community
Black soil
title Field-based evidence for the prevalence of soil antibiotic resistomes under long-term antibiotic-free fertilization
title_full Field-based evidence for the prevalence of soil antibiotic resistomes under long-term antibiotic-free fertilization
title_fullStr Field-based evidence for the prevalence of soil antibiotic resistomes under long-term antibiotic-free fertilization
title_full_unstemmed Field-based evidence for the prevalence of soil antibiotic resistomes under long-term antibiotic-free fertilization
title_short Field-based evidence for the prevalence of soil antibiotic resistomes under long-term antibiotic-free fertilization
title_sort field based evidence for the prevalence of soil antibiotic resistomes under long term antibiotic free fertilization
topic Antibiotic resistome
Long-term fertilization
Antibiotic-free manure
Bacterial community
Black soil
url http://www.sciencedirect.com/science/article/pii/S016041202400789X
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