Microcystin influence on soil-plant microbiota: unraveling microbiota modulations and assembly processes in the rhizosphere of Vicia faba

Abstract

Microcystins (MCs) are frequently detected in cyanobacterial bloom-impacted waterbodies and introduced into agroecosystems via irrigation water. They are widely known as phytotoxic cyanotoxins, which impair the growth and physiological functions of crop plants. However, their impact on the plant-associated microbiota is scarcely tackled and poorly understood. Therefore, we aimed to investigate the effect of MCs on microbiota-inhabiting bulk soil (BS), root adhering soil (RAS), and root tissue (RT) of Vicia faba when exposed to 100 μg L−1 MCs in a greenhouse pot experiment. Under MC exposure, the structure, co-occurrence network, and assembly processes of the bacterial microbiota were modulated with the greatest impact on RT-inhabiting bacteria, followed by BS and, to a lesser extent, RAS. The analyses revealed a significant decrease in the abundances of several Actinobacteriota-related taxa within the RT microbiota, including the most abundant and known genus of Streptomyces. Furthermore, MCs significantly increased the abundance of methylotrophic bacteria (Methylobacillus, Methylotenera) and other Proteobacteria-affiliated genera (e.g., Paucibacter), which are supposed to degrade MCs. The co-occurrence network of the bacterial community in the presence of MCs was less complex than the control network. In MC-exposed RT, the turnover in community composition was more strongly driven by deterministic processes, as proven by the beta-nearest taxon index. Whereas in MC-treated BS and RAS, both deterministic and stochastic processes can influence community assembly to some extent, with a relative dominance of deterministic processes. Altogether, these results suggest that MCs may reshape the structure of the microbiota in the soil-plant system by reducing bacterial taxa with potential phytobeneficial traits and increasing other taxa with the potential capacity to degrade MCs.