Cargando…

Carbendazim shapes microbiome and enhances resistome in the earthworm gut

BACKGROUND: It is worrisome that several pollutants can enhance the abundance of antibiotic resistance genes (ARGs) in the environment, including agricultural fungicides. As an important bioindicator for environmental risk assessment, earthworm is still a neglected focus that the effects of the fung...

Descripción completa

Detalles Bibliográficos
Autores principales: Song, Jiajin, Li, Tongxin, Zheng, Zhiruo, Fu, Wenjie, Long, Zhengnan, Shi, Nan, Han, Yuling, Zhang, Luqing, Yu, Yunlong, Fang, Hua
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9014604/
https://www.ncbi.nlm.nih.gov/pubmed/35436900
http://dx.doi.org/10.1186/s40168-022-01261-8
_version_ 1784688219404632064
author Song, Jiajin
Li, Tongxin
Zheng, Zhiruo
Fu, Wenjie
Long, Zhengnan
Shi, Nan
Han, Yuling
Zhang, Luqing
Yu, Yunlong
Fang, Hua
author_facet Song, Jiajin
Li, Tongxin
Zheng, Zhiruo
Fu, Wenjie
Long, Zhengnan
Shi, Nan
Han, Yuling
Zhang, Luqing
Yu, Yunlong
Fang, Hua
author_sort Song, Jiajin
collection PubMed
description BACKGROUND: It is worrisome that several pollutants can enhance the abundance of antibiotic resistance genes (ARGs) in the environment, including agricultural fungicides. As an important bioindicator for environmental risk assessment, earthworm is still a neglected focus that the effects of the fungicide carbendazim (CBD) residues on the gut microbiome and resistome are largely unknown. In this study, Eisenia fetida was selected to investigate the effects of CBD in the soil-earthworm systems using shotgun metagenomics and qPCR methods. RESULTS: CBD could significantly perturb bacterial community and enrich specific bacteria mainly belonging to the phylum Actinobacteria. More importantly, CBD could serve as a co-selective agent to elevate the abundance and diversity of ARGs, particularly for some specific types (e.g., multidrug, glycopeptide, tetracycline, and rifamycin resistance genes) in the earthworm gut. Additionally, host tracking analysis suggested that ARGs were mainly carried in some genera of the phyla Actinobacteria and Proteobacteria. Meanwhile, the level of ARGs was positively relevant to the abundance of mobile genetic elements (MGEs) and some representative co-occurrence patterns of ARGs and MGEs (e.g., cmx-transposase and sul1-integrase) were further found on the metagenome-assembled contigs in the CBD treatments. CONCLUSIONS: It can be concluded that the enhancement effect of CBD on the resistome in the earthworm gut may be attributed to its stress on the gut microbiome and facilitation on the ARGs dissemination mediated by MGEs, which may provide a novel insight into the neglected ecotoxicological risk of the widely used agrochemicals on the gut resistome of earthworm dwelling in soil. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-022-01261-8.
format Online
Article
Text
id pubmed-9014604
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-90146042022-04-19 Carbendazim shapes microbiome and enhances resistome in the earthworm gut Song, Jiajin Li, Tongxin Zheng, Zhiruo Fu, Wenjie Long, Zhengnan Shi, Nan Han, Yuling Zhang, Luqing Yu, Yunlong Fang, Hua Microbiome Research BACKGROUND: It is worrisome that several pollutants can enhance the abundance of antibiotic resistance genes (ARGs) in the environment, including agricultural fungicides. As an important bioindicator for environmental risk assessment, earthworm is still a neglected focus that the effects of the fungicide carbendazim (CBD) residues on the gut microbiome and resistome are largely unknown. In this study, Eisenia fetida was selected to investigate the effects of CBD in the soil-earthworm systems using shotgun metagenomics and qPCR methods. RESULTS: CBD could significantly perturb bacterial community and enrich specific bacteria mainly belonging to the phylum Actinobacteria. More importantly, CBD could serve as a co-selective agent to elevate the abundance and diversity of ARGs, particularly for some specific types (e.g., multidrug, glycopeptide, tetracycline, and rifamycin resistance genes) in the earthworm gut. Additionally, host tracking analysis suggested that ARGs were mainly carried in some genera of the phyla Actinobacteria and Proteobacteria. Meanwhile, the level of ARGs was positively relevant to the abundance of mobile genetic elements (MGEs) and some representative co-occurrence patterns of ARGs and MGEs (e.g., cmx-transposase and sul1-integrase) were further found on the metagenome-assembled contigs in the CBD treatments. CONCLUSIONS: It can be concluded that the enhancement effect of CBD on the resistome in the earthworm gut may be attributed to its stress on the gut microbiome and facilitation on the ARGs dissemination mediated by MGEs, which may provide a novel insight into the neglected ecotoxicological risk of the widely used agrochemicals on the gut resistome of earthworm dwelling in soil. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-022-01261-8. BioMed Central 2022-04-18 /pmc/articles/PMC9014604/ /pubmed/35436900 http://dx.doi.org/10.1186/s40168-022-01261-8 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
Song, Jiajin
Li, Tongxin
Zheng, Zhiruo
Fu, Wenjie
Long, Zhengnan
Shi, Nan
Han, Yuling
Zhang, Luqing
Yu, Yunlong
Fang, Hua
Carbendazim shapes microbiome and enhances resistome in the earthworm gut
title Carbendazim shapes microbiome and enhances resistome in the earthworm gut
title_full Carbendazim shapes microbiome and enhances resistome in the earthworm gut
title_fullStr Carbendazim shapes microbiome and enhances resistome in the earthworm gut
title_full_unstemmed Carbendazim shapes microbiome and enhances resistome in the earthworm gut
title_short Carbendazim shapes microbiome and enhances resistome in the earthworm gut
title_sort carbendazim shapes microbiome and enhances resistome in the earthworm gut
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9014604/
https://www.ncbi.nlm.nih.gov/pubmed/35436900
http://dx.doi.org/10.1186/s40168-022-01261-8
work_keys_str_mv AT songjiajin carbendazimshapesmicrobiomeandenhancesresistomeintheearthwormgut
AT litongxin carbendazimshapesmicrobiomeandenhancesresistomeintheearthwormgut
AT zhengzhiruo carbendazimshapesmicrobiomeandenhancesresistomeintheearthwormgut
AT fuwenjie carbendazimshapesmicrobiomeandenhancesresistomeintheearthwormgut
AT longzhengnan carbendazimshapesmicrobiomeandenhancesresistomeintheearthwormgut
AT shinan carbendazimshapesmicrobiomeandenhancesresistomeintheearthwormgut
AT hanyuling carbendazimshapesmicrobiomeandenhancesresistomeintheearthwormgut
AT zhangluqing carbendazimshapesmicrobiomeandenhancesresistomeintheearthwormgut
AT yuyunlong carbendazimshapesmicrobiomeandenhancesresistomeintheearthwormgut
AT fanghua carbendazimshapesmicrobiomeandenhancesresistomeintheearthwormgut