Are Nanoparticles a Threat to Mycorrhizal and Rhizobial Symbioses? A Critical Review

Soil microorganisms can be exposed to, and affected by, nanoparticles (NPs) that are either purposely released into the environment (e.g., nanoagrochemicals and NP-containing amendments) or reach soil as nanomaterial contaminants. It is crucial to evaluate the potential impact of NPs on key plant-microbe symbioses such as mycorrhizas and rhizobia, which are vital for health, functioning and sustainability of both natural and agricultural ecosystems. Our critical review of the literature indicates that NPs may have neutral, negative, or positive effects on development of mycorrhizal and rhizobial symbioses. The net effect of NPs on mycorrhizal development is driven by various factors including NPs type, speciation, size, concentration, fungal species, and soil physicochemical properties. As expected for potentially toxic substances, NPs concentration was found to be the most critical factor determining the toxicity of NPs against mycorrhizas, as even less toxic NPs such as ZnO NPs can be inhibitory at high concentrations, and highly toxic NPs such as Ag NPs can be stimulatory at low concentrations. Likewise, rhizobia show differential responses to NPs depending on the NPs concentration and the properties of NPs, rhizobia, and growth substrate, however, most rhizobial studies have been conducted in soil-less media, and the documented effects cannot be simply interpreted within soil systems in which complex interactions occur. Overall, most studies indicating adverse effects of NPs on mycorrhizas and rhizobia have been performed using either unrealistically high NP concentrations that are unlikely to occur in soil, or simple soil-less media (e.g., hydroponic cultures) that provide limited information about the processes occurring in the real environment/agrosystems. To safeguard these ecologically paramount associations, along with other ecotoxicological considerations, large-scale application of NPs in farming systems should be preceded by long-term field trials and requires an appropriate application rate and comprehensive (preferably case-specific) assessment of the context parameters i.e., the properties of NPs, microbial symbionts, and soil. Directions and priorities for future research are proposed based on the gaps and experimental restrictions identified.