Mycorrhizal symbiosis modulates the rhizosphere microbiota to promote rhizobia–legume symbiosis

Abstract

Plants establish symbioses with mutualistic fungi, such as arbuscular mycorrhizal (AM) fungi, and bacteria, such as rhizobia, to exchange key nutrients and thrive. Plants and symbionts have coevolved and represent vital components of terrestrial ecosystems. Plants employ an ancestral AM signaling pathway to establish intracellular symbioses, including the legume–rhizobia symbiosis, in their roots. Nevertheless, the relationship between the AM and rhizobial symbioses in native soil is poorly understood. Here, we examined how these distinct symbioses affect root-associated bacterial communities in Medicago truncatula by performing quantitative microbiota profiling (QMP) of 16S rRNA genes. We found that M. truncatula mutants that cannot establish AM or rhizobia symbiosis have an altered microbial load (quantitative abundance) in the rhizosphere and roots, and in particular that AM symbiosis is required to assemble a normal quantitative root-associated microbiota in native soil. Moreover, quantitative microbial co-abundance network analyses revealed that AM symbiosis affects Rhizobiales hubs among plant microbiota and benefits the plant holobiont. Through QMP of rhizobial rpoB and AM fungal SSU rRNA genes, we revealed a new layer of interaction whereby AM symbiosis promotes rhizobia accumulation in the rhizosphere of M. truncatula. We further showed that AM symbiosis-conditioned microbial communities within the M. truncatula rhizosphere could promote nodulation in different legume plants in native soil. Given that the AM and rhizobial symbioses are critical for crop growth, our findings might inform strategies to improve agricultural management. Moreover, our work sheds light on the co-evolution of these intracellular symbioses during plant adaptation to native soil conditions.