Rhizosphere Microbial Response to Multiple Metal(loid)s in Different Contaminated Arable Soils Indicates Crop-Specific Metal-Microbe Interactions

The rhizosphere is the “hub” for plant-microbe interactions and an active region for exchange of nutrients and energy between soil and plants. In arable soils contaminated by mining activities, the rhizosphere may be an important barrier resisting metal uptake. Therefore, the responses of the rhizosphere microbiota to metal contamination involve important biogeochemical processes, which can affect metal bioavailability and thus impact food safety. However, understanding these processes remains a challenge. The current study illustrates that metal-microbe interactions may be crop specific and some less-addressed metals, such as V and Cr, may play important roles in shaping bacterial communities. The current study provides new insights into metal-microbe interactions and contributes to future implementation and monitoring efforts in contaminated arable soils. ABSTRACT In this study, we sampled rhizosphere soils from seven different agricultural fields adjacent to mining areas and cultivated with different crops (corn, rice, or soybean), to study the interactions among the innate microbiota, soil chemical properties, plants, and metal contamination. The rhizosphere bacterial communities were characterized by Illumina sequencing of the 16S rRNA genes, and their interactions with the local environments, including biotic and abiotic factors, were analyzed. Overall, these soils were heavily contaminated with multiple metal(loid)s, including V, Cr, Cu, Sb, Pb, Cd, and As. The interactions between environmental parameters and microbial communities were identified using multivariate regression tree analysis, canonical correspondence analysis, and network analysis. Notably, metal-microbe interactions were observed to be crop specific. The rhizosphere communities were strongly correlated with V and Cr levels, although these sites were contaminated from Sb and Zn/Pb mining, suggesting that these two less-addressed metals may play important roles in shaping the rhizosphere microbiota. Members of Gaiellaceae cooccurred with other bacterial taxa (biotic interactions) and several metal(loid)s, suggesting potential metal(loid) resistance or cycling involving this less-well-known taxon. IMPORTANCE The rhizosphere is the “hub” for plant-microbe interactions and an active region for exchange of nutrients and energy between soil and plants. In arable soils contaminated by mining activities, the rhizosphere may be an important barrier resisting metal uptake. Therefore, the responses of the rhizosphere microbiota to metal contamination involve important biogeochemical processes, which can affect metal bioavailability and thus impact food safety. However, understanding these processes remains a challenge. The current study illustrates that metal-microbe interactions may be crop specific and some less-addressed metals, such as V and Cr, may play important roles in shaping bacterial communities. The current study provides new insights into metal-microbe interactions and contributes to future implementation and monitoring efforts in contaminated arable soils.