Decoding the trajectory of antibiotic resistance genes in saline and alkaline soils: Insights from different fertilization regimes

The soil salinity and alkalinity play an important role in the occurrence and proliferation of antibiotic resistance genes (ARGs). Yet, little is known the underlying mechanism by which soil salinity and alkalinity affect antibiotic resistance evolution. Here we investigated the ARGs variation in so...

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Main Authors: Dandan Zhang, Jie Li, Guilong Zhang, Yan Xu
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/S0160412024008341
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author Dandan Zhang
Jie Li
Guilong Zhang
Yan Xu
author_facet Dandan Zhang
Jie Li
Guilong Zhang
Yan Xu
author_sort Dandan Zhang
collection DOAJ
description The soil salinity and alkalinity play an important role in the occurrence and proliferation of antibiotic resistance genes (ARGs). Yet, little is known the underlying mechanism by which soil salinity and alkalinity affect antibiotic resistance evolution. Here we investigated the ARGs variation in soil salinity and alkalinity environments created by different fertilization, and explored the biological mechanisms that salinity and alkalinity alter the evolutionary paradigm of antibiotic resistance. The results showed the soil treated by organic fertilizer exhibited a low salinity, neutral level (TSD 239.20 μS/cm, pH 7.17). The ARG abundance in the OF treatment was the highest, keeping an average of 67.83 TPM. Beside the effect of direct input of organic fertilizer at the beginning, it was important to note that, ARGs abundance during planting showed significant correlations with pH and electric conductivity. We observed that changes in microbial survival strategies under different salinity and alkalinity conditions further affected ARG hosts abundance. Indoor experiments demonstrated that there was a survival trade-off between the growth of resistant bacteria and the evolution of antibiotic resistance in salinity and alkalinity environments. Meta-genomic and Meta-transcriptomic analysis consistently demonstrated bacterial antibiotic resistance was primarily associated with pyruvate, energy and lipid metabolic pathways. The functional gene related to salinity and alkalinity, like cysH, cysK, plsB and plsC showed negative correlations with MDR. Prokaryotic transcription assays validated these relations. This study well explains the prevalence of soil ARGs after different fertilization regimes and will give a deeper understanding for the effect of soil salinity and alkalinity on antibiotic resistance evolution.
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spelling doaj-art-92a2497a770e4195abcb4f2bf3e2db7d2025-01-24T04:44:13ZengElsevierEnvironment International0160-41202025-01-01195109247Decoding the trajectory of antibiotic resistance genes in saline and alkaline soils: Insights from different fertilization regimesDandan Zhang0Jie Li1Guilong Zhang2Yan Xu3Agro-Environmental Protection Institute, Ministry of Agriculture and Rural Affairs, Key Laboratory of Original Agro-Environmental Pollution Prevention and Control, MARA, Tianjin and Tianjin Key Laboratory of Agro-Environment and Agro-Product Safety, Tianjin 300191, ChinaAgro-Environmental Protection Institute, Ministry of Agriculture and Rural Affairs, Key Laboratory of Original Agro-Environmental Pollution Prevention and Control, MARA, Tianjin and Tianjin Key Laboratory of Agro-Environment and Agro-Product Safety, Tianjin 300191, ChinaAgro-Environmental Protection Institute, Ministry of Agriculture and Rural Affairs, Key Laboratory of Original Agro-Environmental Pollution Prevention and Control, MARA, Tianjin and Tianjin Key Laboratory of Agro-Environment and Agro-Product Safety, Tianjin 300191, China; Agro-Environmental Protection Institute, Ministry of Agriculture and Rural Affairs, Qingyun Comprehensive Test Base, Dezhou 253000, ChinaAgro-Environmental Protection Institute, Ministry of Agriculture and Rural Affairs, Key Laboratory of Original Agro-Environmental Pollution Prevention and Control, MARA, Tianjin and Tianjin Key Laboratory of Agro-Environment and Agro-Product Safety, Tianjin 300191, China; Corresponding author.The soil salinity and alkalinity play an important role in the occurrence and proliferation of antibiotic resistance genes (ARGs). Yet, little is known the underlying mechanism by which soil salinity and alkalinity affect antibiotic resistance evolution. Here we investigated the ARGs variation in soil salinity and alkalinity environments created by different fertilization, and explored the biological mechanisms that salinity and alkalinity alter the evolutionary paradigm of antibiotic resistance. The results showed the soil treated by organic fertilizer exhibited a low salinity, neutral level (TSD 239.20 μS/cm, pH 7.17). The ARG abundance in the OF treatment was the highest, keeping an average of 67.83 TPM. Beside the effect of direct input of organic fertilizer at the beginning, it was important to note that, ARGs abundance during planting showed significant correlations with pH and electric conductivity. We observed that changes in microbial survival strategies under different salinity and alkalinity conditions further affected ARG hosts abundance. Indoor experiments demonstrated that there was a survival trade-off between the growth of resistant bacteria and the evolution of antibiotic resistance in salinity and alkalinity environments. Meta-genomic and Meta-transcriptomic analysis consistently demonstrated bacterial antibiotic resistance was primarily associated with pyruvate, energy and lipid metabolic pathways. The functional gene related to salinity and alkalinity, like cysH, cysK, plsB and plsC showed negative correlations with MDR. Prokaryotic transcription assays validated these relations. This study well explains the prevalence of soil ARGs after different fertilization regimes and will give a deeper understanding for the effect of soil salinity and alkalinity on antibiotic resistance evolution.http://www.sciencedirect.com/science/article/pii/S0160412024008341SoilFertilization regimeSalinity-alkalinityAntibiotic resistance genesEvolutionMicrobial metabolism
spellingShingle Dandan Zhang
Jie Li
Guilong Zhang
Yan Xu
Decoding the trajectory of antibiotic resistance genes in saline and alkaline soils: Insights from different fertilization regimes
Environment International
Soil
Fertilization regime
Salinity-alkalinity
Antibiotic resistance genes
Evolution
Microbial metabolism
title Decoding the trajectory of antibiotic resistance genes in saline and alkaline soils: Insights from different fertilization regimes
title_full Decoding the trajectory of antibiotic resistance genes in saline and alkaline soils: Insights from different fertilization regimes
title_fullStr Decoding the trajectory of antibiotic resistance genes in saline and alkaline soils: Insights from different fertilization regimes
title_full_unstemmed Decoding the trajectory of antibiotic resistance genes in saline and alkaline soils: Insights from different fertilization regimes
title_short Decoding the trajectory of antibiotic resistance genes in saline and alkaline soils: Insights from different fertilization regimes
title_sort decoding the trajectory of antibiotic resistance genes in saline and alkaline soils insights from different fertilization regimes
topic Soil
Fertilization regime
Salinity-alkalinity
Antibiotic resistance genes
Evolution
Microbial metabolism
url http://www.sciencedirect.com/science/article/pii/S0160412024008341
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AT jieli decodingthetrajectoryofantibioticresistancegenesinsalineandalkalinesoilsinsightsfromdifferentfertilizationregimes
AT guilongzhang decodingthetrajectoryofantibioticresistancegenesinsalineandalkalinesoilsinsightsfromdifferentfertilizationregimes
AT yanxu decodingthetrajectoryofantibioticresistancegenesinsalineandalkalinesoilsinsightsfromdifferentfertilizationregimes