Stochastic and deterministic processes shape bioenergy crop microbiomes along a vertical soil niche.

Sustainable biofuel cropping systems aim to address climate change while meeting energy needs. Understanding how soil and plant-associated microbes respond to these different cropping systems is key to promoting agriculture sustainability and evaluating changes in ecosystem functions. Here, we leverage a long-term biofuel cropping system field experiment to dissect soil and root microbiome changes across a soil-depth gradient in poplar, restored prairie and switchgrass to understand their effects on the microbial communities. High throughput amplicon sequencing of the fungal internal transcribed spacer (ITS) and prokaryotic 16S DNA regions showed a common trend of root and soil microbial community richness decreasing and evenness increasing with depth. Ecological niche (root vs. soil) had the strongest effect on community structure, followed by depth, then crop. Stochastic processes dominated the structuring of fungal communities in deeper soil layers while operational taxonomic units (OTUs) in surface soil layers were more likely to co-occur and to be enriched by plant hosts. Prokaryotic communities were dispersal limited at deeper depths. Microbial networks showed a higher density, connectedness, average degree and module size in deeper soils. We observed a decrease in fungal-fungal links and an increase of bacteria-bacteria links with increasing depth in all crops, particularly in the root microbiome.

Soil Origin and Plant Genotype Modulate Switchgrass Aboveground Productivity and Root Microbiome Assembly.

Switchgrass (Panicum virgatum) is a model perennial grass for bioenergy production that can be productive in agricultural lands that are not suitable for food production. There is growing interest in whether its associated microbiome may be adaptive in low- or no-input cultivation systems. However, the relative impact of plant genotype and soil factors on plant microbiome and biomass are a challenge to decouple. To address this, a common garden greenhouse experiment was carried out using six common switchgrass genotypes, which were each grown in four different marginal soils collected from long-term bioenergy research sites in Michigan and Wisconsin. We characterized the fungal and bacterial root communities with high-throughput amplicon sequencing of the ITS and 16S rDNA markers, and collected phenological plant traits during plant growth, as well as soil chemical traits. At harvest, we measured the total plant aerial dry biomass. Significant differences in richness and Shannon diversity across soils but not between plant genotypes were found. Generalized linear models showed an interaction between soil and genotype for fungal richness but not for bacterial richness. Community structure was also strongly shaped by soil origin and soil origin × plant genotype interactions. Overall, plant genotype effects were significant but low. Random Forest models indicate that important factors impacting switchgrass biomass included NO3-, Ca2+, PO43-, and microbial biodiversity. We identified 54 fungal and 52 bacterial predictors of plant aerial biomass, which included several operational taxonomic units belonging to Glomeraceae and Rhizobiaceae, fungal and bacterial lineages that are involved in provisioning nutrients to plants. IMPORTANCE Greenhouse gas reduction, carbon sequestration, and environmental remediation are top research themes within the U.S. Department of Energy funded bioenergy research centers. The utilization of unproductive agricultural land for bioenergy crop production is one of the most promising directions to achieve these goals. Switchgrass is a model biofuel system: it is adapted to a wide variety of geographical regions in North America, it is protective of soil and water resources, and it can be productive in low-fertility soils, but its profitability depends greatly on the biomass yield. Beneficial microbes have known roles in modulating plant biomass production but their interaction with soil geography, and switchgrass cultivars were not thoroughly studied. This study aims to fill important knowledge gaps and to serve as a foundation for switchgrass biomass promotion through microbe selection with an ultimate goal of facilitating sustainable bioenergy crop production.