Combinatorial Community Coalescence Reveals a Compositional Continuum Shaped By Source Legacy and Shared Rhizosphere Constraints

Abstract

The rhizosphere microbiome plays fundamental roles in plant health and productivity, yet the ecological rules governing microbiome assembly remain poorly understood. Here, we investigated early rhizosphere community assembly in tomato using a replicated combinatorial community coalescence framework, in which seven distinct natural bacterial communities were inoculated individually and in all possible pairwise and triplet combinations. Single-inoculum communities clustered according to inoculum identity, indicating substantial source-community legacy in assembly trajectories. Pairwise coalescence outcomes were directional and context-dependent, and changes in dominant ASV abundances varied among source combinations. Nevertheless, when all communities were analyzed jointly, samples formed a continuous compositional landscape with no clear evidence of discrete community states. Despite major differences among source communities, the resulting rhizosphere communities exhibited a recurrent uneven rank–abundance structure, with two ASVs accounting for 50% of total abundance and a median of nineteen ASVs per community accounting for 90%. Assembly was dominated by a small number of Pseudomonas ASVs, although some communities developed alternative dominant configurations. Increasing inoculum complexity was associated with progressively greater proximity to a balanced leave-one-treatment-out compositional reference and did not increase replicate-to-replicate compositional variability. Together, these results are most consistent with source-community legacy and shared rhizosphere constraints acting simultaneously. Source identity and coalescing-partner context influenced individual assembly outcomes, while common rhizosphere conditions constrained communities to a continuous compositional region and promoted recurrent taxon dominance and abundance organization.