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Endophytic microbiomes of healthy seed form a symbiotic relationship with their host. Seed and environment are sources of microbes that colonize the developing plant; however, the influence of each remains unclear. Here, using irradiation combined with surface sterilization to generate near-axenic seed with disrupted and reduced microbiomes, we contrasted the colonization potential of seed and soil microbiomes. We hypothesized that the seed microbiome would be the primary colonizer of the plant endophytic compartments. Our experimental design comprised four treatments, using soybean as a model plant: (i) nearly axenic seed growing in a sterile environment, (ii) nonaxenic seed inoculated with a microbial soil extract, (iii) nearly axenic seed inoculated with a microbial seed extract, and (iv) nearly axenic seed inoculated with a microbial soil extract. After 14 days of growth, plants were harvested, and DNA was extracted from the shoot, roots, and rhizosphere and subjected to 16S ribosomal RNA gene amplicon sequencing, quantitative PCR quantification of the total community, and functional genes involved in the N cycle. Community dynamics were similar for most treatments within their respective compartments, except for the soil treatment, where rhizosphere and root microbiomes differed from other treatments, suggesting that the soil microbiome colonizes the belowground compartment efficiently only when the seed microbiome is severely disrupted. For the shoot, all treatments resembled the seed microbiome treatment, suggesting that the seedborne bacteria colonize the aboveground compartment preferentially. Our results highlight the primacy of the seed microbiome over the soils during early colonization, putting seed microbes as potential candidates of microbiome engineering efforts.

Soybean Microbiome Recovery After Disruption is Modulated by the Seed and Not the Soil Microbiome