Competition-induced metabolic switching governs the interaction network in plant microbiome assembly

Abstract

Plants are colonized by characteristic microbiomes that help maintain plant health and function. However, the mechanisms that make these communities assemble in a consistent, repeatable manner remain poorly understood. Here, we show how microbial metabolic strategies for host-derived substrates drive plant microbiome assembly, using a six-member synthetic community that captures the taxonomic diversity of natural duckweed microbiome. Contrary to expectations of metabolic niche partitioning, five of six strains adopt similar metabolic states when colonizing the host alone, consistent with the preferential use of a shared substrate, acetaldehyde. In contrast, during competition with specific community members, these strains consistently switch toward alternative substrates, including sugars and aromatics. Strikingly, this metabolic switching accompanies all negative interspecies interactions observed in the community, indicating that a single class of metabolic response dominates the inhibitory interaction network organizing community structure. By comparison, although metabolite cross-feeding is widespread, its contribution to facilitative interactions depends on the background of resource competition. Together, these findings highlight competition-induced metabolic switching as a primary driver of microbial interaction networks, and provide a cross-scale account of how microbial metabolic strategies underpin the reproducible assembly of plant microbiomes.