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Nanoparticle treatment of maize analyzed through the metatranscriptome: compromised nitrogen cycling, possible phytopathogen selection, and plant hormesis

BACKGROUND: The beneficial use of nanoparticle silver or nanosilver may be confounded when its potent antimicrobial properties impact non-target members of natural microbiomes such as those present in soil or the plant rhizosphere. Agricultural soils are a likely sink for nanosilver due to its prese...

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Autores principales: Sillen, Wouter M. A., Thijs, Sofie, Abbamondi, Gennaro Roberto, De La Torre Roche, Roberto, Weyens, Nele, White, Jason C., Vangronsveld, Jaco
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7488162/
https://www.ncbi.nlm.nih.gov/pubmed/32907632
http://dx.doi.org/10.1186/s40168-020-00904-y
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author Sillen, Wouter M. A.
Thijs, Sofie
Abbamondi, Gennaro Roberto
De La Torre Roche, Roberto
Weyens, Nele
White, Jason C.
Vangronsveld, Jaco
author_facet Sillen, Wouter M. A.
Thijs, Sofie
Abbamondi, Gennaro Roberto
De La Torre Roche, Roberto
Weyens, Nele
White, Jason C.
Vangronsveld, Jaco
author_sort Sillen, Wouter M. A.
collection PubMed
description BACKGROUND: The beneficial use of nanoparticle silver or nanosilver may be confounded when its potent antimicrobial properties impact non-target members of natural microbiomes such as those present in soil or the plant rhizosphere. Agricultural soils are a likely sink for nanosilver due to its presence in agrochemicals and land-applied biosolids, but a complete assessment of nanosilver’s effects on this environment is lacking because the impact on the natural soil microbiome is not known. In a study assessing the use of nanosilver for phytopathogen control with maize, we analyzed the metatranscriptome of the maize rhizosphere and observed multiple unintended effects of exposure to 100 mg kg(−1) nanosilver in soil during a growth period of 117 days. RESULTS: We found several unintended effects of nanosilver which could interfere with agricultural systems in the long term. Firstly, the archaea community was negatively impacted with a more than 30% decrease in relative abundance, and as such, their involvement in nitrogen cycling and specifically, nitrification, was compromised. Secondly, certain potentially phytopathogenic fungal groups showed significantly increased abundances, possibly due to the negative effects of nanosilver on bacteria exerting natural biocontrol against these fungi as indicated by negative interactions in a network analysis. Up to 5-fold increases in relative abundance have been observed for certain possibly phytopathogenic fungal genera. Lastly, nanosilver exposure also caused a direct physiological impact on maize as illustrated by increased transcript abundance of aquaporin and phytohormone genes, overall resulting in a stress level with the potential to yield hormetically stimulated plant root growth. CONCLUSIONS: This study indicates the occurrence of significant unintended effects of nanosilver use on corn, which could turn out to be negative to crop productivity and ecosystem health in the long term. We therefore highlight the need to include the microbiome when assessing the risk associated with nano-enabled agriculture.
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spelling pubmed-74881622020-09-16 Nanoparticle treatment of maize analyzed through the metatranscriptome: compromised nitrogen cycling, possible phytopathogen selection, and plant hormesis Sillen, Wouter M. A. Thijs, Sofie Abbamondi, Gennaro Roberto De La Torre Roche, Roberto Weyens, Nele White, Jason C. Vangronsveld, Jaco Microbiome Research BACKGROUND: The beneficial use of nanoparticle silver or nanosilver may be confounded when its potent antimicrobial properties impact non-target members of natural microbiomes such as those present in soil or the plant rhizosphere. Agricultural soils are a likely sink for nanosilver due to its presence in agrochemicals and land-applied biosolids, but a complete assessment of nanosilver’s effects on this environment is lacking because the impact on the natural soil microbiome is not known. In a study assessing the use of nanosilver for phytopathogen control with maize, we analyzed the metatranscriptome of the maize rhizosphere and observed multiple unintended effects of exposure to 100 mg kg(−1) nanosilver in soil during a growth period of 117 days. RESULTS: We found several unintended effects of nanosilver which could interfere with agricultural systems in the long term. Firstly, the archaea community was negatively impacted with a more than 30% decrease in relative abundance, and as such, their involvement in nitrogen cycling and specifically, nitrification, was compromised. Secondly, certain potentially phytopathogenic fungal groups showed significantly increased abundances, possibly due to the negative effects of nanosilver on bacteria exerting natural biocontrol against these fungi as indicated by negative interactions in a network analysis. Up to 5-fold increases in relative abundance have been observed for certain possibly phytopathogenic fungal genera. Lastly, nanosilver exposure also caused a direct physiological impact on maize as illustrated by increased transcript abundance of aquaporin and phytohormone genes, overall resulting in a stress level with the potential to yield hormetically stimulated plant root growth. CONCLUSIONS: This study indicates the occurrence of significant unintended effects of nanosilver use on corn, which could turn out to be negative to crop productivity and ecosystem health in the long term. We therefore highlight the need to include the microbiome when assessing the risk associated with nano-enabled agriculture. BioMed Central 2020-09-09 /pmc/articles/PMC7488162/ /pubmed/32907632 http://dx.doi.org/10.1186/s40168-020-00904-y Text en © The Author(s) 2020 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/. The Creative Commons Public Domain Dedication waiver (http://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
Sillen, Wouter M. A.
Thijs, Sofie
Abbamondi, Gennaro Roberto
De La Torre Roche, Roberto
Weyens, Nele
White, Jason C.
Vangronsveld, Jaco
Nanoparticle treatment of maize analyzed through the metatranscriptome: compromised nitrogen cycling, possible phytopathogen selection, and plant hormesis
title Nanoparticle treatment of maize analyzed through the metatranscriptome: compromised nitrogen cycling, possible phytopathogen selection, and plant hormesis
title_full Nanoparticle treatment of maize analyzed through the metatranscriptome: compromised nitrogen cycling, possible phytopathogen selection, and plant hormesis
title_fullStr Nanoparticle treatment of maize analyzed through the metatranscriptome: compromised nitrogen cycling, possible phytopathogen selection, and plant hormesis
title_full_unstemmed Nanoparticle treatment of maize analyzed through the metatranscriptome: compromised nitrogen cycling, possible phytopathogen selection, and plant hormesis
title_short Nanoparticle treatment of maize analyzed through the metatranscriptome: compromised nitrogen cycling, possible phytopathogen selection, and plant hormesis
title_sort nanoparticle treatment of maize analyzed through the metatranscriptome: compromised nitrogen cycling, possible phytopathogen selection, and plant hormesis
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7488162/
https://www.ncbi.nlm.nih.gov/pubmed/32907632
http://dx.doi.org/10.1186/s40168-020-00904-y
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