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Structure, function and evolution of bacterial root microbiota

Final Report Summary - ROOTMICROBIOTA (Structure, function and evolution of bacterial root microbiota)

The plant-associated bacterial microbiota is characterized by the co-occurrence of three main phyla across divergent hosts, including Proteobacteria, Actinobacteria, and Bacteroidetes, as well as Firmicutes in some soil types. The highly diverse but stable soil biome functions as the inoculum source for the root microbiota, from which a fraction of microbes successfully colonize the root. One likely signal for root colonization by soil bacteria is photoassimilate-derived organic carbon that is released into the rhizosphere as root exudates, given that low-molecular-weight carbon is rate-limiting for bacterial growth in unplanted soil substrate, and that addition of such carbon compounds to soil results in community shifts resembling those during root microbiota formation.
Comparative analysis of the bacterial root microbiota with the model plant Arabidopsis thaliana and several A. thaliana relatives revealed a quantitative divergence of bacterial community profiles and host phylogenetic signals. This indicates potential host-species specific adaptation of the root-associated bacterial assemblages. Parts of the root microbiota modulate flowering time, whereas, after microbiota acquisition during vegetative growth, the established root-associated bacterial assemblage is structurally robust to perturbations caused by flowering and drastic changes in plant stature.
Legumes are known as pioneer plants colonizing marginal soils, and as enhancers of the nutritional status in cultivated soils. This beneficial activity has been explained by their capacity to engage in symbiotic relationship with nitrogen-fixing rhizobia. Genetic disruption of the nodulation pathway in the model legume Lotus japonicus resulted in depletion of six bacterial orders from the root compartment, including the two most abundant orders identified, Flavobacteriales and Burkholderiales. Thus, nitrogen-fixing rhizobia acts as a bacterial hub in Lotus roots for the assembly of a taxonomically diverse bacterial root microbiota.
Understanding the organizational principles and functional capabilities of complex microbial communities that colonize plant roots demands a holistic deconstruction and reconstitution of the plant microbiota under controlled laboratory conditions. We have established Arabidopsis thaliana leaf- and root-derived microbiota culture collections representing the majority of bacterial species that are reproducibly detectable by culture-independent community sequencing. We found an extensive taxonomic overlap between the leaf and root microbiota. Using defined bacterial communities and a gnotobiotic Arabidopsis plant system, we have shown that the bacterial isolates form assemblies resembling natural microbiota on their cognate host organs, but are also capable of ectopic leaf or root colonization. High-quality genome drafts of > 400 microbiota members revealed a large overlap of genome-encoded functional capabilities between leaf- and root-derived bacteria with few significant differences at the level of individual functional categories. The culture collections of the A. thaliana bacterial microbiota, together with their genomes, represent an important future resource for the wider research community working on phytobiomes.
This project also enabled us to identify an A. thaliana fungal endophyte, beneficial Colletotrichum tofieldiae, which appears to partly compensate for the loss of mycorrhiza symbiosis in this plant species. Although most characterized species of the fungal genus Colletotrichum are destructive pathogens, C. tofieldiae (Ct) is an endemic beneficial endophyte in natural Arabidopsis thaliana populations in central Spain. Colonization by Ct initiates in roots but can also spread systemically into shoots. Ct transfers the macronutrient phosphorus to shoots, promotes plant growth, and increases fertility only under phosphorus-deficient conditions, a nutrient status that might have facilitated the transition from pathogenic to beneficial lifestyles. The host’s phosphate starvation response (PSR) system controls Ct root colonization and is needed for plant growth promotion (PGP). PGP also requires PEN2-dependent indole glucosinolate metabolism, a component of innate immune responses, indicating a functional link between innate immunity and the PSR system during beneficial interactions with Ct.