Bio-Organic Fertilizer Promotes Pear Yield by Shaping the Rhizosphere Microbiome Composition and Functions

Bio-organic fertilizers (BOF) containing both organic amendments and beneficial microorganisms have been consistently shown to improve soils fertility and yield. However, the exact mechanisms which link amendments and yields remain disputed, and the complexity of bio-organic fertilizers may work in parallel in several ways. BOF may directly improve yield by replenishing soil nutrients or introducing beneficial microbial genes or indirectly by altering the soil microbiome to enrich native beneficial microorganisms. In this work, we aim to disentangle the relative contributions of direct and indirect effects on pear yield. We treated pear trees with either chemical fertilizer or organic fertilizer with/without the plant-beneficial bacterium Bacillus velezensis SQR9. We then assessed, in detail, soil physicochemical and biological properties (metagenome sequencing) as well as pear yield. We then evaluated the relative importance of direct and indirect effects of soil amendments on pear yield. Both organic treatments increased plant yield by up to 20%, with the addition of bacteria tripling the increase driven by organic fertilizer alone. This increase could be linked to alterations in soil physicochemical properties, bacterial community function, and metabolism. Supplementation of organic fertilizer SQR9 increased rhizosphere microbiome richness and functional diversity. Fertilizer-sensitive microbes and functions responded as whole guilds. Pear yield was most positively associated with the Mitsuaria- and Actinoplanes-dominated ecological clusters and with gene clusters involved in ion transport and secondary metabolite biosynthesis. Together, these results suggested that bio-organic fertilizers mainly act indirectly on plant yield by creating soil chemical properties which promote a plant-beneficial microbiome. IMPORTANCE Bio-organic fertilization is a widely used, eco-friendly, sustainable approach to increasing plant productivity in the agriculture and fruit industries. However, it remains unclear whether the promotion of fruit productivity is related to specific changes in microbial inoculants, the resident microbiome, and/or the physicochemical properties of rhizosphere soils. We found that bio-organic fertilizers alter soil chemical properties, thus manipulating specific microbial taxa and functions within the rhizosphere microbiome of pear plants to promote yield. Our work unveils the ecological mechanisms which underlie the beneficial impacts of bio-organic fertilizers on yield promotion in fruit orchards, which may help in the design of more efficient biofertilizers to promote sustainable fruit production.