Soil nutrition-dependent dynamics of the root-associated microbiome in paddy rice

Plants accommodate diverse microbial communities, known as the microbiome, which can change dynamically during plant adaptation to varying environmental conditions. However, the mechanisms driving these changes, particularly in crops adapting to the field conditions, remain poorly understood. Here, we investigate the root-associated microbiome of rice (Oryza sativa L.) across four consecutive cultivation seasons in a high-yield, non-fertilized, and pesticide-free paddy field, compared to a neighboring fertilized and pesticide-treated field. Using 16S rRNA amplicon and meta-genome sequencing, we analyzed three Japonica cultivars-Nipponbare, Hinohikari, and Kinmaze. Our findings reveal that microbial community structures shift and separate based on soil fertilization status and plant developmental stages, while the effects of cultivar variation are less significant. Notably, nitrogen-fixing bacteria such as Telmatospirillum, Bradyrhizobium and Rhizomicrobium were over-represented in rice growth in the non-fertilized field, implying that the assembly of these microbes supports rice adaptation to nutrient-deficient environments. Furthermore, a machine learning model trained on the microbiome data successfully predicted soil nutrition status across different years and rice cultivars, highlighting the potential of root microbiome analysis in forecasting soil and plant nutrition. Additionally, we observed significant changes in the root microbiome structures of ccamk mutants, which lack a master regulator of mycorrhizal and rhizobial symbioses, under laboratory conditions but not in the field. This indicates a condition-dependent role for CCaMK in establishing microbiomes in paddy rice.