Assembly and ecological function of the root microbiome across angiosperm plant species

Abstract

Across plants and animals, host-associated microbial communities play fundamental roles in host nutrition, development, and immunity. The factors that shape host-microbiome interactions are poorly understood, yet essential for understanding the evolution and ecology of these symbioses. Plant roots assemble two distinct microbial compartments from surrounding soil: the rhizosphere (microbes surrounding roots) and the endosphere (microbes within roots). Root-associated microbes were key for the evolution of land plants and underlie fundamental ecosystem processes. However, it is largely unknown how plant evolution has shaped root microbial communities, and in turn, how these microbes affect plant ecology, such as the ability to mitigate biotic and abiotic stressors. Here we show that variation among 30 angiosperm species, which have diverged for up to 140 million years, affects root bacterial diversity and composition. Greater similarity in root microbiomes between hosts leads to negative effects on plant performance through soil feedback, with specific microbial taxa in the endosphere and rhizosphere potentially affecting competitive interactions among plant species. Drought also shifts the composition of root microbiomes, most notably by increasing the relative abundance of the Actinobacteria. However, this drought response varies across host plant species, and host-specific changes in the relative abundance of endosphere Streptomyces are associated with host drought tolerance. Our results emphasize the causes of variation in root microbiomes and their ecological importance for plant performance in response to biotic and abiotic stressors.

Keywords: host microbial ecology; plant drought; plant microbiome; plant–soil feedback; root microbiome.

Fig. 1.

The diversity and composition of endosphere and rhizosphere compartments across plant species. (A) The endosphere exhibited less than one-quarter of the diversity found in the rhizosphere [F_{(1, 56)} = 64.62_, P_FDR < 0.001, P-value adjusted using the FDR]. (B) The abundance of bacterial phyla were significantly affected (GLM: P_FDR < 0.05) by compartment (black star) and host plant species (green star, endosphere; yellow star, rhizosphere). (C) Endosphere diversity exhibited greater variation across host plants than rhizosphere diversity (χ² = 17.72, P_FDR < 0.001). Endosphere diversity was also correlated with the underlying plant phylogeny, while rhizosphere diversity was not. (D) Plant species varied more in the composition of their endosphere versus rhizosphere compartments (χ² = 20.06, P_FDR < 0.001). Mantel tests revealed a significant correlation between endosphere (but not rhizosphere) compositional similarity and phylogenetic relatedness.

Fig. 2.

Root microbial composition is related to PSF. (A) PSF occurs when the soil microbes recruited by one plant influence the growth of other plants. Positive values indicate that a focal species performed better in soil conditioned by a heterospecific plant relative to a conspecific plant, whereas negative values indicate the opposite. (B) Plants exhibit enhanced growth when inoculated with soil conditioned by a heterospecific species with dissimilar endosphere (measured as weighted UniFrac distance) and (C) rhizosphere compartments (measured as unweighted UniFrac distance).

Fig. 3.

Differential abundance of root bacterial taxa and PSF. Host plant species exhibit differential abundance for numerous root bacterial taxa in either the endosphere or rhizosphere, including: (A) an endosphere Streptomyces ASV and (B) the genus Pseudoxanthomonas, found in the rhizosphere (GLM: P_FDR < 0.05). We estimated the log₂ fold-change of differentially abundant root bacterial taxa among all unique pairs of focal (starred taxa on the host plant phylogeny) and soil-conditioning host plant species and correlated this with their measured PSF. Negative log₂ fold-changes indicate a higher taxon abundance in soil-conditioning host plant species, while positive values indicate a higher taxon abundance in focal host plant species. (C) The differential abundance of the endosphere Streptomyces ASV between focal and soil-conditioning host plant species was positively related to their PSF. (D) However, the differential abundance of rhizosphere Pseudoxanthomonas between focal and soil-conditioning host plant species was negatively related to their PSF. (E and F) PSF between host plant species was significantly associated with the differential abundance of 66 endosphere taxa and 33 rhizosphere taxa. (E) In the endosphere, we observed a high proportion (35%) of PSF-related taxa exhibiting the association depicted in C (green lines illustrate significant trend lines between differential abundance of endosphere taxa and PSF at P_FDR < 0.05). (F) While in the rhizosphere, a greater proportion (88%) of taxa exhibited the association depicted in D (yellow lines illustrate significant trend lines between rhizosphere taxa and PSF at P_FDR < 0.05). See Dataset S2 for a full list of PSF-related taxa.

Fig. 4.

The effects of drought on root microbial communities. (A) The drought treatment (denoted by T) caused small reductions in the diversity of the endosphere and rhizosphere compartments (denoted by C), and (B) had large effects on the relative abundance of major bacterial phyla; starred phyla were significantly affected (GLM: P_FDR < 0.05) by drought (green, endosphere; orange, rhizosphere). (C) Drought also had strong effects on the overall composition of the endosphere and rhizosphere microbiomes, although endosphere compartments exhibited a greater response. (Inset) Plants under drought experienced fourfold lower soil moisture than well-watered plants.

Fig. 5.

The relationship between drought tolerance and Streptomycetaceae. (A) On average, the drought treatment (denoted by T) caused a 35% reduction in biomass compared with well-watered conditions [F_{(1, 44)} = 17.37, P < 0.001], and plant species (denoted by S) varied significantly in their response to drought (represented by dots connected by individual lines). (B) Drought caused a sixfold increase in the mean relative abundance of endosphere Streptomycetaceae (Actinobacteria), but this effect varied among plant species. (C) Plant species with greater relative increases in an endosphere Streptomyces ASV under drought conditions had greater drought tolerance. See Dataset S4 for a full list of drought-related taxa.