Positive interactions between plant-beneficial inoculants and members of the resident soil microbiome improve plant performance under stress

Inoculants containing plant-beneficial microorganisms (BMs) can assist plants in BM recruitment from the soil microbiome. BMs can improve plant growth, especially under stress. We hypothesized that stress disrupts BM recruitment from soil, which can be restored by BM inoculation. We performed drench-inoculation of field-grown maize in two consecutive years with a BM consortium consisting of Bacillus atrophaeus ABi03, Pseudomonas sp. RU47 and Trichoderma harzianium OMG16. Sampling five weeks after inoculation showed that the consortium increased plant biomass and iron uptake in 2020 during severe drought compared to non-inoculated control plants, but not in 2021 with average precipitation. Also, the consortium-dependent modulation of the resident rhizosphere microbiome, based on 16S rRNA gene and ITS amplicon sequencing, depended on the year. Several ASVs classified as Comamonadaceae spp. significantly increased in the rhizosphere due to BMc inoculation in 2020, but not in 2021, and were predictive for iron uptake. This suggests that plant-BMs improved plant growth only during stress exposure due to the recruitment of soil resident BMs. To test this second hypothesis, we compared the 16S rRNA gene of these Comamonadaceae ASVs to a bacterial strain collection from the rhizosphere of maize grown in the same field. The alignment showed that several isolates matched the sequences of ASVs enriched by the consortium inoculation. These isolates were classified as Variovorax spp. and in vitro functional characterization revealed their stress mitigation capacity due to degradation of 1-aminocyclopropane-1-carboxylic acid. In vitro co-cultivation assays showed that the consortium members boosted the biomass of several Variovorax isolates. Moreover, the inoculation of the consortium complemented with Variovorax, as representative of the resident soil microbiome, resulted in higher plant growth under drought in the greenhouse compared to the consortium alone. Consequently, our study indicates that positive interactions between inoculants and the resident microbiome are crucial for plant performance.