Enhanced plant growth in the presence of earthworms correlates with changes in soil microbiota but not nutrient availability

•Earthworms enhanced wheat growth under watered and drought conditions.•Soil extractions indicated no impact of earthworms on nutrient availability.•Earthworm-treatment microbiomes had fewer pathogens and more beneficial microbes.•Increase plant growth in earthworm treatments was due to changes in the microbiome. Earthworms enhance plant growth but the precise mechanism by which this occurs is not known. An understanding of the mechanism could potentially support changes in agricultural management reducing fertiliser usage and therefore costs and the carbon footprint of agriculture. We conducted a factorial experiment in which 5 strains of wheat were grown in the presence and absence of earthworms under regular watering and droughted conditions. The different wheat strains all responded in a similar fashion. Plant biomass was greater in the presence of earthworms and under regular watering. The presence of earthworms reduced the impact of drought on plant biomass and also slowed down the rate of drying of the droughted soils. Plant nutrient content (N, P, Si) showed no consistent pattern with treatments but plant total N, P and Si mirrored plant biomass and decreased in the order earthworm-present watered > earthworm-present droughted > earthworm-absent watered > earthworm-absent droughted. Nutrient availability in the soil, as assessed by chemical extractions showed no consistent pattern with treatments. Differential gene expression of plants was greater between watering treatments than between earthworm treatments. Genes that were differentially expressed between the earthworm treatments predominantly related to plant defences, abiotic stress and control of plant growth though a couple were linked to both nitrogen cycling and stress responses. The soil microbiome of the earthworm-present treatments was more associated with nutrient-rich environments, the promotion of plant growth and the suppression of plant pathogens whilst that of the earthworm-absent treatments included a variety of plant pathogens. Our data are consistent with enhanced plant growth being due to changes in the microbiome brought about by earthworm processing of the soil rather than changes in nutrient availability directly due to earthworm activity.