Plant-specific microbial diversity ensures functional redundancy and ecosystem functioning at the soil-root interface

The co-evolved and specifically composed plant microbiota represents an enormous biodiversity on Earth. However, less is known about functional diversity and whether it correlates with structural diversity. In the present study, both were analyzed by disentangling the microbiota of three medicinal plants at the root-soil interface grown in desert ecosystems under organic farming. Significant differences were observed for structural diversity between all investigated microhabitats (soil, rhizosphere, endorhiza) and plant species (chamomile, marigold, nightshade). Unique genera were identified for each plant species. To explore this plant-driven effect for functional understanding, deepening metagenomics analyses were implemented for rhizosphere samples, which showed the most different composition. However, all rhizosphere microbiomes were characterized by similar functions comprising mainly i) plant nutrition and metabolic interplay (e.g. ion, amino acid, vitamin, lipid, and carbohydrate transport and metabolism, secondary metabolites biosynthesis, transport, and catabolism), ii) plant health (e.g. defense mechanisms, chaperones), and iii) biogeochemical cycling. A lot of signatures support the high activity, which is well known for the root-soil interface. Binning resulted in 298 metagenome-assembled genomes (MAGs); their taxonomy confirmed plant-specific bacteria. Three selected plant-specific MAGs for each plant underlined the metagenome-mined rhizosphere functions, showed multifunctionality and, despite taxonomic differences, functional similarity. Sphingobium, Pseudomonas, and Gemmatirosa multifunctionally contributed to the overall functioning of the rhizosphere; the highest number of 79 encoded rhizospheric core functions was observed for the multifunctionally equipped Sphingobium MAG. The study uncovered functional similarity in structurally different rhizosphere microbiomes and underlines the importance of rhizosphere functioning and diversity for plant and ecosystem health.