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

Wouter M A Sillen,Sofie Thijs,Jaco Vangronsveld,Gennaro Roberto Abbamondi,Roberto De La Torre Roche,Jason C White,Nele Weyens

doi:10.1186/s40168-020-00904-y

Abstract

BackgroundThe 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.ResultsWe 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.ConclusionsThis 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.8o2Ktf3WjN9uvowsG6Jw_6Video

Highlights

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
(c) fungi; and Principal coordinates analyses (PCoA) plot based on Bray-Curtis dissimilarities for (d) archaea, (e) bacteria, and (f) fungi for maize rhizosphere soil communities with or without exposure to 100 mg kg−1 silver nanoparticles (20 nm) in soil, based on the metatranscriptome
Using the extensive information, the rhizosphere metatranscriptome has to offer, we show that soil borne nanosilver has various unintended effects on maize and its rhizosphere microbiome

Summary

Introduction

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. The diverse and highly complex interplay of biotic and abiotic factors in environments such as soil serve as a major confounding factor to efforts designed to understand the potential negative or positive impacts associated with nanomaterials and nano-enabled products. The rhizosphere or soil root-zone is a prime example of such a complex environment Both prokaryotic and eukaryotic microorganisms reside in root-affected soil, and these groups of microbes can interact directly or indirectly with each other or with the plant in ways that may be beneficial, antagonistic, or neutral [1,2,3]. Given the importance of the rhizosphere to both agriculture and important ecosystem services such as nutrient cycling (e.g., nitrogen fixation), a thorough understanding of the range of potential impacts of nanomaterial exposure in this complex environment is of critical importance [4]

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