Microbial interkingdom interactions in roots promote Arabidopsis survival

Abstract

17Roots of healthy plants are inhabited by soil-derived bacteria, fungi, and oomycetes that have 18 evolved independently in distinct kingdoms of life. How these microorganisms interact and to 19 what extent those interactions affect plant health are poorly understood. We examined root-20 associated microbial communities from three Arabidopsis thaliana populations and detected 21 mostly negative correlations between bacteria and filamentous microbial eukaryotes. We 22 established microbial culture collections for reconstitution experiments using germ-free A. 23 thaliana. In plants inoculated with mono-or multi-kingdom synthetic microbial consortia, we 24 observed a profound impact of the bacterial root microbiota on fungal and oomycetal 25 2 community structure and diversity. We demonstrate that the bacterial microbiota is essential 26 for plant survival and protection against root-derived filamentous eukaryotes. Deconvolution 27 of 2,862 binary bacterial-fungal interactions ex situ, combined with community perturbation 28 experiments in planta, indicate that biocontrol activity of bacterial root commensals is a 29 redundant trait that maintains microbial interkingdom balance for plant health. 30 31 reconstitution experiments, we provide community-level evidence that negative interactions 51 between prokaryotic and eukaryotic root microbiota members are critical for plant host 52 survival and maintenance of host-microbiota balance. 53 54 Results 55Root-associated microbial assemblages. We collected A. thaliana plants from natural 56 populations at two neighbouring sites in Germany (Geyen and Pulheim; 5 km apart) and a 57 more distant location in France (Saint-Dié; ~300 km away) ( Figure S1; Table S1). For each 58 population, four replicates, each consisting of four pooled A. thaliana individuals were 59 prepared, together with corresponding bulk soils. Root samples were fractionated into 60 episphere and endosphere compartments, enriching for microbes residing on the root surface 61 or inside roots, respectively ( Figure S2). We characterized the multi-kingdom microbial 62 consortia along the soil-root continuum by simultaneous DNA amplicon sequencing of the 63 bacterial 16S rRNA gene and fungal as well as oomycetal Internal Transcribed Spacer (ITS) 64 regions (Agler et al. 2016) ( Table S2). Alpha diversity indices (within-sample diversity) 65 indicated a gradual decrease of microbial diversity from bulk soil to the root endosphere 66 (Kruskal-Wallis test, p<0.01; Figure S3). Profiles of microbial class abundance between 67 sample-types ( Figure 1A) and Operational Taxonomic Unit (OTU) enrichment tests 68 conducted using a linear model between soil, root episphere and root endosphere samples 69 (p<0.05, Figure 1B) identified 96 bacterial, 24 fungal and one oomycetal OTU that are 70 consistently enriched in plant roots across all three sites. This, together with the reduced alpha 71 diversity, points to a gating role of the root surface for entry into the root interior for each of 72 the three microbial kingdoms ...

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