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Natural selenium stress influences the changes of antibiotic resistome in seleniferous forest soils

BACKGROUND: Metal(loid)s can promote the spread and enrichment of antibiotic resistance genes (ARGs) in the environment through a co-selection effect. However, it remains unclear whether exposure of microorganisms to varying concentrations of selenium (Se), an essential but potentially deleterious m...

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Autores principales: Wang, Fang-Fang, Liu, Guo-Ping, Zhang, Fan, Li, Zong-Ming, Yang, Xiao-Lin, Yang, Chao-Dong, Shen, Jian-Lin, He, Ji-Zheng, Li, B. Larry, Zeng, Jian-Guo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9107767/
https://www.ncbi.nlm.nih.gov/pubmed/35570296
http://dx.doi.org/10.1186/s40793-022-00419-z
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author Wang, Fang-Fang
Liu, Guo-Ping
Zhang, Fan
Li, Zong-Ming
Yang, Xiao-Lin
Yang, Chao-Dong
Shen, Jian-Lin
He, Ji-Zheng
Li, B. Larry
Zeng, Jian-Guo
author_facet Wang, Fang-Fang
Liu, Guo-Ping
Zhang, Fan
Li, Zong-Ming
Yang, Xiao-Lin
Yang, Chao-Dong
Shen, Jian-Lin
He, Ji-Zheng
Li, B. Larry
Zeng, Jian-Guo
author_sort Wang, Fang-Fang
collection PubMed
description BACKGROUND: Metal(loid)s can promote the spread and enrichment of antibiotic resistance genes (ARGs) in the environment through a co-selection effect. However, it remains unclear whether exposure of microorganisms to varying concentrations of selenium (Se), an essential but potentially deleterious metal(loid) to living organisms, can influence the migration and distribution of ARGs in forest soils. RESULTS: Precisely 235 ARGs conferring resistance to seven classes of antibiotics were detected along a Se gradient (0.06–20.65 mg kg(−1)) across 24 forest soils. (flor)/(chlor)/(am)phenicol resistance genes were the most abundant in all samples. The total abundance of ARGs first increased and then decreased with an elevated available Se content threshold of 0.034 mg kg(−1) (P = 2E−05). A structural equation model revealed that the dominant mechanism through which Se indirectly influences the vertical migration of ARGs is by regulating the abundance of the bacterial community. In addition, the methylation of Se (mediated by tehB) and the repairing of DNA damages (mediated by ruvB and recG) were the dominant mechanisms involved in Se resistance in the forest soils. The co-occurrence network analysis revealed a significant correlated cluster between Se-resistance genes, MGEs and ARGs, suggesting the co-transfer potential. Lelliottia amnigena YTB01 isolated from the soil was able to tolerate 50 μg mL(−1) ampicillin and 1000 mg kg(−1) sodium selenite, and harbored both Se resistant genes and ARGs in the genome. CONCLUSIONS: Our study demonstrated that the spread and enrichment of ARGs are enhanced under moderate Se pressure but inhibited under severe Se pressure in the forest soil (threshold at 0.034 mg kg(−1) available Se content). The data generated in this pilot study points to the potential health risk associated with Se contamination and its associated influence on ARGs distribution in soil. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40793-022-00419-z.
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spelling pubmed-91077672022-05-16 Natural selenium stress influences the changes of antibiotic resistome in seleniferous forest soils Wang, Fang-Fang Liu, Guo-Ping Zhang, Fan Li, Zong-Ming Yang, Xiao-Lin Yang, Chao-Dong Shen, Jian-Lin He, Ji-Zheng Li, B. Larry Zeng, Jian-Guo Environ Microbiome Research Article BACKGROUND: Metal(loid)s can promote the spread and enrichment of antibiotic resistance genes (ARGs) in the environment through a co-selection effect. However, it remains unclear whether exposure of microorganisms to varying concentrations of selenium (Se), an essential but potentially deleterious metal(loid) to living organisms, can influence the migration and distribution of ARGs in forest soils. RESULTS: Precisely 235 ARGs conferring resistance to seven classes of antibiotics were detected along a Se gradient (0.06–20.65 mg kg(−1)) across 24 forest soils. (flor)/(chlor)/(am)phenicol resistance genes were the most abundant in all samples. The total abundance of ARGs first increased and then decreased with an elevated available Se content threshold of 0.034 mg kg(−1) (P = 2E−05). A structural equation model revealed that the dominant mechanism through which Se indirectly influences the vertical migration of ARGs is by regulating the abundance of the bacterial community. In addition, the methylation of Se (mediated by tehB) and the repairing of DNA damages (mediated by ruvB and recG) were the dominant mechanisms involved in Se resistance in the forest soils. The co-occurrence network analysis revealed a significant correlated cluster between Se-resistance genes, MGEs and ARGs, suggesting the co-transfer potential. Lelliottia amnigena YTB01 isolated from the soil was able to tolerate 50 μg mL(−1) ampicillin and 1000 mg kg(−1) sodium selenite, and harbored both Se resistant genes and ARGs in the genome. CONCLUSIONS: Our study demonstrated that the spread and enrichment of ARGs are enhanced under moderate Se pressure but inhibited under severe Se pressure in the forest soil (threshold at 0.034 mg kg(−1) available Se content). The data generated in this pilot study points to the potential health risk associated with Se contamination and its associated influence on ARGs distribution in soil. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40793-022-00419-z. BioMed Central 2022-05-15 /pmc/articles/PMC9107767/ /pubmed/35570296 http://dx.doi.org/10.1186/s40793-022-00419-z Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Wang, Fang-Fang
Liu, Guo-Ping
Zhang, Fan
Li, Zong-Ming
Yang, Xiao-Lin
Yang, Chao-Dong
Shen, Jian-Lin
He, Ji-Zheng
Li, B. Larry
Zeng, Jian-Guo
Natural selenium stress influences the changes of antibiotic resistome in seleniferous forest soils
title Natural selenium stress influences the changes of antibiotic resistome in seleniferous forest soils
title_full Natural selenium stress influences the changes of antibiotic resistome in seleniferous forest soils
title_fullStr Natural selenium stress influences the changes of antibiotic resistome in seleniferous forest soils
title_full_unstemmed Natural selenium stress influences the changes of antibiotic resistome in seleniferous forest soils
title_short Natural selenium stress influences the changes of antibiotic resistome in seleniferous forest soils
title_sort natural selenium stress influences the changes of antibiotic resistome in seleniferous forest soils
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9107767/
https://www.ncbi.nlm.nih.gov/pubmed/35570296
http://dx.doi.org/10.1186/s40793-022-00419-z
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