Soil microbiomes play an important role in the services and functioning of terrestrial ecosystems. However, little is known of their vertical responses to restoration process and their contributions to soil nutrient cycling in the subsurface profiles. Here, we investigated the community assembly of soil bacteria, archaea, and fungi along vertical (i.e., soil depths of 0–300 cm) and horizontal (i.e., distance from trees of 30–90 cm) profiles in a chronosequence of reforestation sites that represent over 30 years of restoration. In the superficial layers (0–80 cm), bacterial and fungal diversity decreased, whereas archaeal diversity increased with increasing soil depth. As reforestation proceeded over time, the vertical spatial variation in bacterial communities decreased, while that in archaeal and fungal communities increased. Vertical distributions of the soil microbiomes were more related to the variation in soil properties, while their horizontal distributions may be driven by a gradient effect of roots extending from the tree. Bacterial and archaeal beta-diversity were strongly related to multi-nutrient cycling in the soil, respectively, playing major roles in deep and superficial layers. Taken together, these results reveal a new perspective on the vertical and horizontal spatial variation in soil microbiomes at the fine scale of single trees. Distinct response patterns underpinned the contributions of soil bacteria, archaea, and fungi as a function of subsurface nutrient cycling during the reforestation of ex-arable land.

Background: Plant health and growth are negatively affected by pathogen invasion; however, plants can dynamically modulate their rhizosphere microbiome and adapt to such biotic stresses. Although plant-recruited protective microbes can be assembled into synthetic communities for application in the control of plant disease, rhizosphere microbial communities commonly contain some taxa at low abundance. The roles of low-abundance microbes in synthetic communities remain unclear; it is also unclear whether all the microbes enriched by plants can enhance host adaptation to the environment. Here, we assembled a synthetic community with a disease resistance function based on differential analysis of root-associated bacterial community composition. We further simplified the synthetic community and investigated the roles of low-abundance bacteria in the control of Astragalus mongholicus root rot disease by a simple synthetic community. Results: Fusarium oxysporum infection reduced bacterial Shannon diversity and significantly affected the bacterial community composition in the rhizosphere and roots of Astragalus mongholicus. Under fungal pathogen challenge, Astragalus mongholicus recruited some beneficial bacteria such as Stenotrophomonas, Achromobacter, Pseudomonas, and Flavobacterium to the rhizosphere and roots. We constructed a disease-resistant bacterial community containing 10 high- and three low-abundance bacteria enriched in diseased roots. After the joint selection of plants and pathogens, the complex synthetic community was further simplified into a four-species community composed of three high-abundance bacteria (Stenotrophomonas sp., Rhizobium sp., Ochrobactrum sp.) and one low-abundance bacterium (Advenella sp.). Notably, a simple community containing these four strains and a thirteen-species community had similar effects on the control root rot disease. Furthermore, the simple community protected plants via a synergistic effect of highly abundant bacteria inhibiting fungal pathogen growth and less abundant bacteria activating plant-induced systemic resistance. Conclusions: Our findings suggest that bacteria with low abundance play an important role in synthetic communities and that only a few bacterial taxa enriched in diseased roots are associated with disease resistance. Therefore, the construction and simplification of synthetic communities found in the present study could be a strategy employed by plants to adapt to environmental stress.

Background: The rhizosphere microbiome, which is shaped by host genotypes, root exudates, and plant domestication, is crucial for sustaining agricultural plant growth. Despite its importance, how plant domestication builds up specific rhizosphere microbiomes and metabolic functions, as well as the importance of these affected rhizobiomes and relevant root exudates in maintaining plant growth, is not well understood. Here, we firstly investigated the rhizosphere bacterial and fungal communities of domestication and wild accessions of tetraploid wheat using amplicon sequencing (16S and ITS) after 9 years of domestication process at the main production sites in China. We then explored the ecological roles of root exudation in shaping rhizosphere microbiome functions by integrating metagenomics and metabolic genomics approaches. Furthermore, we established evident linkages between root morphology traits and keystone taxa based on microbial culture and plant inoculation experiments. Results: Our results suggested that plant rhizosphere microbiomes were co-shaped by both host genotypes and domestication status. The wheat genomes contributed more variation in the microbial diversity and composition of rhizosphere bacterial communities than fungal communities, whereas plant domestication status exerted much stronger influences on the fungal communities. In terms of microbial interkingdom association networks, domestication destabilized microbial network and depleted the abundance of keystone fungal taxa. Moreover, we found that domestication shifted the rhizosphere microbiome from slow growing and fungi dominated to fast growing and bacteria dominated, thereby resulting in a shift from fungi-dominated membership with enrichment of carbon fixation genes to bacteria-dominated membership with enrichment of carbon degradation genes. Metagenomics analyses further indicated that wild cultivars of wheat possess higher microbial function diversity than domesticated cultivars. Notably, we found that wild cultivar is able to harness rhizosphere microorganism carrying N transformation (i.e., nitrification, denitrification) and P mineralization pathway, whereas rhizobiomes carrying inorganic N fixation, organic N ammonification, and inorganic P solubilization genes are recruited by the releasing of root exudates from domesticated wheat. More importantly, our metabolite-wide association study indicated that the contrasting functional roles of root exudates and the harnessed keystone microbial taxa with different nutrient acquisition strategies jointly determined the aboveground plant phenotypes. Furthermore, we observed that although domesticated and wild wheats recruited distinct microbial taxa and relevant functions, domestication-induced recruitment of keystone taxa led to a consistent growth regulation of root regardless of wheat domestication status. Conclusions: Our results indicate that plant domestication profoundly influences rhizosphere microbiome assembly and metabolic functions and provide evidence that host plants are able to harness a differentiated ecological role of root-associated keystone microbiomes through the release of root exudates to sustain belowground multi-nutrient cycles and plant growth. These findings provide valuable insights into the mechanisms underlying plant-microbiome interactions and how to harness the rhizosphere microbiome for crop improvement in sustainable agriculture.

Revealing the roles of biotic factors in driving community assembly, which is crucial for the understanding of biodiversity and ecosystem functions, is a fundamental but infrequently investigated subject in microbial ecology. Here, combining a cross‐biome observational study with an experimental microcosm study, we provided evidence to reveal the major roles of biotic factors (i.e., soil fungi and cross‐kingdom species associations) in determining soil bacterial biogeography and community assembly in complex terrestrial ecosystems of the arid regions of northwest China. The results showed that the soil fungal richness mediates the balance of assembly processes of bacterial communities, and stochastic assembly processes decreased with increasing fungal richness. Our results further suggest that the predicted increase in aridity conditions due to climate change will reduce bacterial α‐diversity, particularly in desert soils and subsurface layer, and induce more negative species associations. Together, our study represents a significant advance in linking soil fungi to the mechanisms underlying bacterial biogeographic patterns and community assembly in arid ecosystems under climate aridity and land‐use change scenarios.