The seed microbial community constitutes an initial inoculum for plant microbiota assembly. Still, the persistence of seed microbiota when seeds encounter soil during plant emergence and early growth is barely documented. We characterized the encounter event of seed and soil microbiota and how it structured seedling bacterial and fungal communities by using amplicon sequencing. We performed eight contrasting encounter events to identify drivers influencing seedling microbiota assembly. To do so, four contrasting seed lots of two Brassica napus genotypes were sown in two soils whose microbial diversity levels were manipulated by serial dilution and recolonization. Seedling root and stem microbiota were influenced by soil but not by initial seed microbiota composition or by plant genotype. A strong selection on the seed and soil communities occurred during microbiota assembly, with only 8% to 32% of soil taxa and 0.8% to 1.4% of seed-borne taxa colonizing seedlings. The recruitment of seedling microbiota came mainly from soil (35% to 72% of diversity) and not from seeds (0.3% to 15%). Soil microbiota transmission success was higher for the bacterial community than for the fungal community. Interestingly, seedling microbiota was primarily composed of initially rare taxa (from seed, soil, or unknown origin) and intermediate-abundance soil taxa. IMPORTANCE Seed microbiota can have a crucial role for crop installation by modulating dormancy, germination, seedling development, and recruitment of plant symbionts. Little knowledge is available on the fraction of the plant microbiota that is acquired through seeds. We characterize the encounter between seed and soil communities and how they colonize the seedling together. Transmission success and seedling community assemblage can be influenced by the variation of initial microbial pools, i.e., plant genotype and cropping year for seeds and diversity level for soils. Despite a supposed resident advantage of the seed microbiota, we show that transmission success is in favor of the soil microbiota. Our results also suggest that successful plant-microbiome engineering based on native seed or soil microbiota must include rare taxa.
Keywords: Brassica napus; microbial ecology; microbiota; plant microbiota; root; seed; soil; soil microbiology; stem; transmission.