Interplay between green-synthesized nanoparticles and plant performance is mediated by the microbial community in the rhizocompartments

Abstract

Numerous green-synthesized nanoparticles are being evaluated for their potential application in soil, yet understanding their influence on plant performance and their rhizocompartments associated microbes is a gap that needs to be addressed. In this study, we investigated how applying iron oxide nanoparticles (control 0, low 25 and high 50 mg/kg) impacted the rhizocompartments associated microbial communities and plant secondary metabolites grown in natural soil microcosm. The transcriptional analysis showed that the majority of artemisinin and flavonoid biosynthetic pathway genes were significantly upregulated in plants with the application of low concentration of green-synthesized iron oxide nanoparticles (FeO.NPs) when compared with control plants, suggesting a fine collaboration between these metabolites’ pathways, as indicated by a remarkable increase in artemisinin content (2-fold), ferulic acid (7.6-fold), luteolin (4.3-fold) and syringic acid (6.2-fold). The response of rhizocompartments microbial communities and associated soil enzymes was investigated using high-throughput sequencing and profiler test kits, respectively. The soil microbial community structure was altered upon FeO.NPs exposure in both low and high treated soils as indicated by multivariate analysis. For instance, bacterial phyla Bacteroidetes and Gemmatimonadetes and fungal phyla Ascomycota demonstrated a significant rise in relative abundance in both the rhizosphere and rhizoplane in low and high treatments relative to the control. Moreover, genera level analysis revealed that Cupriavidus, Vibrionimonas, and Burkholderia displayed higher relative abundance (p < 0.05) in low FeO.NPs concentration while Giaella and Nonomuraea didn't show any noticeable response to FeO.NPs. In terms of fungal genera, Oidiodendron and Cryptococcus showed high relative abundance under low treatment. The altered microbiome profile is possibly associated with soil enzymes, for instance, urease and catalase activities were increased by 1.76 and 1.71-fold, respectively in low FeO.NPs. Thus, this study demonstrates the effects of FeO.NPs gradients on plant secondary metabolites and soil enzyme activities, while contributing new insights into their specific impacts on the microbial community composition in the rhizocompartments of plant root system.