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

Abstract

Abstract 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. Video Abstract

Keywords

• Plant microbiome
• Maize
• Silver nanoparticles
• Rhizosphere
• Metatranscriptome
• Phytopathogens