SummaryRoots 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 examined root-associated microbial communities from three Arabidopsis thaliana populations and detected mostly negative correlations between bacteria and filamentous microbial eukaryotes. We established microbial culture collections for reconstitution experiments using germ-free A. thaliana. In plants inoculated with mono- or multi-kingdom synthetic microbial consortia, we observed a profound impact of the bacterial root microbiota on fungal and oomycetal community structure and diversity. We demonstrate that the bacterial microbiota is essential for plant survival and protection against root-derived filamentous eukaryotes. Deconvolution of 2,862 binary bacterial-fungal interactions ex situ, combined with community perturbation experiments in planta, indicate that biocontrol activity of bacterial root commensals is a redundant trait that maintains microbial interkingdom balance for plant health.

The mechanisms that underlie the origin of major prokaryotic groups are poorly understood. In principle, the origin of both species and higher taxa among prokaryotes should entail similar mechanisms — ecological interactions with the environment paired with natural genetic variation involving lineage-specific gene innovations and lineage-specific gene acquisitions1,2,3,4. To investigate the origin of higher taxa in archaea, we have determined gene distributions and gene phylogenies for the 267,568 protein coding genes of 134 sequenced archaeal genomes in the context of their homologs from 1,847 reference bacterial genomes. Archaea-specific gene families define 13 traditionally recognized archaeal higher taxa in our sample. Here we report that the origins of these 13 groups unexpectedly correspond to 2,264 group-specific gene acquisitions from bacteria. Interdomain gene transfer is highly asymmetric, transfers from bacteria to archaea are more than 5-fold more frequent than vice versa. Gene transfers identified at major evolutionary transitions among prokaryotes specifically implicate gene acquisitions for metabolic functions from bacteria as key innovations in the origin of higher archaeal taxa.

Life is the harnessing of chemical energy in such a way that the energy-harnessing device makes a copy of itself. This paper outlines an energetically feasible path from a particular inorganic setting for the origin of life to the first free-living cells. The sources of energy available to early organic synthesis, early evolving systems and early cells stand in the foreground, as do the possible mechanisms of their conversion into harnessable chemical energy for synthetic reactions. With regard to the possible temporal sequence of events, we focus on: (i) alkaline hydrothermal vents as the far-from-equilibrium setting, (ii) the Wood–Ljungdahl (acetyl-CoA) pathway as the route that could have underpinned carbon assimilation for these processes, (iii) biochemical divergence, within the naturally formed inorganic compartments at a hydrothermal mound, of geochemically confined replicating entities with a complexity below that of free-living prokaryotes, and (iv) acetogenesis and methanogenesis as the ancestral forms of carbon and energy metabolism in the first free-living ancestors of the eubacteria and archaebacteria, respectively. In terms of the main evolutionary transitions in early bioenergetic evolution, we focus on: (i) thioester-dependent substrate-level phosphorylations, (ii) harnessing of naturally existing proton gradients at the vent–ocean interface via the ATP synthase, (iii) harnessing of Na+ gradients generated by H+/Na+ antiporters, (iv) flavin-based bifurcation-dependent gradient generation, and finally (v) quinone-based (and Q-cycle-dependent) proton gradient generation. Of those five transitions, the first four are posited to have taken place at the vent. Ultimately, all of these bioenergetic processes depend, even today, upon CO2 reduction with low-potential ferredoxin (Fd), generated either chemosynthetically or photosynthetically, suggesting a reaction of the type ‘reduced iron → reduced carbon’ at the beginning of bioenergetic evolution.

Factors that drive continental-scale variation in root microbiota and plant adaptation are poorly understood. We monitored root-associated microbial communities in Arabidopsis thaliana and cooccurring grasses at 17 European sites across three years. Analysis of 5,625 microbial community profiles demonstrated strong geographic structuring of the soil biome, but not of the root microbiota.Remarkable similarity in bacterial community composition in roots of A. thaliana and grasses was explained by the presence of a few diverse and geographically widespread taxa that disproportionately colonize roots across sites. In a reciprocal transplant between two A. thaliana populations in Sweden and Italy, we uncoupled soil from location effects and tested their respective contributions to root . CC-BY-NC-ND 4.

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 ...