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Structural and Functional Architectures of Multi-Kingdom Microbial Consortia Colonizing Plant Roots

Periodic Reporting for period 3 - MICRORULES (Structural and Functional Architectures of Multi-Kingdom Microbial Consortia Colonizing Plant Roots)

Reporting period: 2020-09-01 to 2022-02-28

In roots of healthy plants, bacteria, fungi and oomycetes coexist and interact, forming physically and metabolically interdependent consortia that harbor distinct properties compared to their single components. The importance of microbe-microbe interactions for structuring and stabilizing plant-associated microbial communities has been so far neglected and is a central aspect of the project. One promising experimental approach for understanding organizational principles and functional capabilities of root-associated microbial communities is to reconstitute high-complexity microbial communities in laboratory settings to test general ecological principles that would be otherwise impossible to address by field experiments.

The objectives are:
1) Characterize the structure of the A. thaliana root microbiota (bacteria, fungi and oomycetes) at a continental scale and identify the major driving forces governing establishment of complex microbial consortia on plant roots .
2) Obtain deeper insights into the fundamental mechanisms underlying the structure and the functions of complex root-associated microbial communities by i) establishing reference microbial culture collections and ii) reconstructing the root microbiota using synthetic microbial consortia and germ-free plants.
3) Generate extensive microbial genome resources for in-depth metatranscriptome studies of multi-kingdom synthetic communities on germ-free plants and initiate the transition from binary plant-microbe to community-level molecular investigations.
4) Dissect the molecular bases of multitrophic plant-microbe interactions and the cascading consequences on plant health.
1) Our continental-scale survey of the A. thaliana root microbiome revealed that roots of healthy plants are colonized by multi-kingdom microbial consortia (bacteria, fungi, oomycetes). A strong geographic structuring was observed for the soil microbiota, but not for the root microbiota. This was consistent with our observation that these plants from diverse European habitats often associate with the same small group of highly abundant microbes. Notably, differences in climate between sites was a primary force explaining variation in root-associated filamentous eukaryotic communities, whereas difference in soil conditions better explained bacterial community variation (Thiergart et al. 2020).

2) Using synthetic microbial communities and microbiota reconstitution experiments in gnotobiotic plant systems, we showed that bacterial root commensals shape fungal and oomycete community composition and protect plants against fungi and oomycetes (Duran et al. 2018). We further demonstrated that protective activities of bacterial root commensals act in concert with host immune outputs (tryptophan branch) to prevent fungal dysbiosis in roots (Wolinska et al. 2021). In addition to the role of microbe-microbe-host interactions for plant health, these reconstitution experiments also revealed that plant responses to microbial root commensals and light were interconnected along a microbiota–root–shoot axis to boost plant growth at the expense of defense under low light. An important finding was that microbiota-induced growth under low light depends on microbiota composition and requires the host transcriptional regulator MYC2 (Hou et al. 2021).

3) Using comparative fungal genomics, we discovered that root mycobiota members evolved from ancestors with diverse lifestyles and retained large repertoires of plant cell wall-degrading enzymes. Notably, fungi belonging to the A. thaliana core mycobiome were detrimental in mono-association experiments with the host, which was associated with highly diverse repertoires of enzymes degrading the plant cell wall component pectin. Notably, over-expression of a pectinase gene in a fungal genetic background lacking this gene family not only resulted in increased root colonization but also in altered effect on plant growth compared to the parental line (Mesny et al. 2021). Using bacterial and fungal genomes, we also developped genome-resolved metatranscriptomic approaches to identified conserved bacterial function induced upon host contact. We recently validated the role of the bacterial TypA gene for root colonization (Vannier, in preparation)

4) Molecular basis of multitrophic plant-microbe interactions: The work is ongoing but has been slightly delayed do to the pandemic.
The results published to date have been important and have contributed to move the plant microbiota research field forward.

1) Our observation that plants from diverse European habitats associate with the same small group of highly abundant microorganisms provides a basis for future rational design of low-complexity synthetic microbial communities (Thiergart et al., Nature Ecology & Evolution 2020).

2) A second major output was the discovery that the innate immune system of plants is insufficient to protect them from filamentous eukaryotes and that bactrerial root commensals provide an additional layer of protection, which is need for plant survival in natural soil. The results shed new light into the fact that microbe-microbe interactions are at least as important as host-microbe interactions to prevent dysbiosis in the root endosphere (Duran et al. Cell, 2018, Wolinska et al, PNAS, 2021). We also accidentally discovered a remarkable bi-directional signalling mechanism connecting chemical energy state in leaves and microbial assemblages in roots that promotes microbiota-induced growth or defence depending on the light condition. Our results, reminiscent of the microbiota-gut-brain axis described in animals, have important applications for utilizing belowground microbes to modulate aboveground stress responses in plants (Hou et al., Nature Plants, 2021).

3) Finally, we recently identified fungal genetic determinants that explain why core fungi from the root mycobiome can robustly colonize roots and cause disease more efficiently than others. our results revealed that fungal enzymes degrading root tissues are key determinants shaping root mycobiome composition and modulating plant health (Mesny et al. Nature communications, 2021).

We also wrote several review articles to promote the major findings linked to microbe-microbe interactions (Hassani et al., Microbiome, 2018; Mataigne et al. Frontiers in Microbiology, 2021), microbiota-mediated disease resistance in plants (Vannier et al., PLoS Pathogens, 2019, Getzke et al. COIM 2019), and the microbiota-root-shoot axis (Hou et al., COiPB, 2021). The role of microbe-microbe interactions and microbiota-root-shoot circuits in shaping plant health are emerging as important topics in the field.
ERC project summary