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

Periodic Reporting for period 2 - MICRORULES (Structural and Functional Architectures of Multi-Kingdom Microbial Consortia Colonizing Plant Roots)

Reporting period: 2019-03-01 to 2020-08-31

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) 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 .

We tested whether roots of healthy A. thaliana and sympatric grasses growing in various soils and climatic environments can establish stable associations with bacterial and filamentous eukaryotic communities across a latitudinal gradient in Europe. We sampled natural A. thaliana populations at the flowering stage at 17 sites along a latitudinal gradient in Europe in three consecutive years (2016, 2017 and 2018). We harvested bulk soil (soil), rhizosphere (RS), rhizoplane (RP), and root endosphere (root) compartments of A. thaliana and sympatric grasses at four sites in Sweden, six in Germany, three in France, one in Italy, and three in Spain, each having distinct environmental and soil characteristics.

Major conclusions:
- Strong geographic structuring of the soil microbiota, but not of the root microbiota.
- Few similar core taxa disproportionately colonize roots across geographically distant sites.
- Composition of the root microbiota is barely affected by host genotype, but altered by location and soil origin
- Differences in climate between sites is a primary force explaining temporal and spatial variation in root-associated filamentous eukaryotic communities.

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.

Roots of healthy plants are inhabited by soil-derived bacteria, fungi, and oomycetes that have evolved independently in distinct kingdoms of life. How these microorganisms interact and to what extent those interactions affect plant health are poorly understood. We established microbial culture collections for reconstitution experiments using germ-free A. thaliana.

Major conclusions:
- Roots of healthy plants are colonized by multi-kingdom microbial consortia.
- Bacterial Root Commensals shape fungal and oomycetal community structure
- Bacterial Root Commensals protect plants against fungi and oomycetes
- Biocontrol activity of Bacterial Root Commensals is a redundant trait and essential for plant survival


3) Generate extensive microbial genome resources for in-depth metatranscriptome studies of multi-kingdom synthetic communities on germ-free plants.

We have already generated collections of root-associated microbes, especially fungi (588 fungal strains) and a large-scale fungal genome sequencing project has been initiated in collaboration with the JGI (USA) and Dr. Francis Martin (INRA Nancy). Comparative genome analysis with saprotrophic, mycorrhizal, and pathogenic fungi is ongoing and will provide new insights into the conserved signatures associated with endophytism. We have already reconstituted the multi-kingdom microbial consortia of Arabidopsis roots and performed high-resolution metatranscriptome profiling of such synthetic microbial communities during root colonization on germ-free plants.

These two projects are developing fast and I anticipate two major publications that will be submitted beginning of 2021.


4) Dissect the molecular bases of multitrophic plant-microbe interactions and the cascading consequences on plant health.

A PhD student (Felix Getzke) has been recently recruited to tackle this research question.
- Our continental-scale survey of the A. thaliana root microbiota, which provides important clues regarding variation and stability of the root microbiota across European sites, has been recently published in the prestigious journal Nature Ecology and Evolution (Thiergart, Duran et al. 2020). The work has been highlighted by a press release (https://www.mpipz.mpg.de/5009634/pr_hacquard_2019) as well as in an informal invited ‘Behind the Paper’ piece by co-first author Paloma Durán (https://natureecoevocommunity.nature.com/channels/521-behind-the-paper/posts/57743-the-wild-side-of-arabidopsis-thaliana-and-its-associated-root-microbiota). The article has been recommended at F1000Prime (https://f1000.com/prime/737160827).

- Another major publication has been published in the multidisciplinary journal Cell, underlying the novelty and originality of the ERC research project (Duran, Thiergart et al. Cell, 2018). Our article has been promoted with a Cell cover image. A press release has been written to disperse the important conclusions of the paper (https://www.mpipz.mpg.de/4713649/pr_hacquard_2018_11) a commentary has been written by our colleagues (https://www.sciencedirect.com/science/article/pii/S167420521930022X?via%3Dihub), and the article has been recommended at F1000Prime (https://f1000.com/prime/734323252).

- We also wrote three review articles: 1) microbial interactions within the plant holobiont (Hassani et al. Microbiome, 2018) that has been already accessed > 15,000 times and is highly cited > 140 citations in < 2 year. 2) Microbiota-mediated disease resistance in plants (Vannier et al. 2019, cited 16 times in 9 months). 3) Bacteria-fungal balance and host health (Getzke et al. 2019) that has just been published end of last year. Therefore, the role of microbe-microbe interactions for community assembly/dynamics and host health is becoming a topic of high interest and our work is contributing to this emerging research field thanks to the support of ERC.