Many bloom-forming dinoflagellates are auxotrophic for essential B-vitamins, yet they proliferate in coastal waters where dissolved vitamin concentrations are often insufficient to sustain bloom biomass. This mismatch suggests that bloom-associated microbiomes may supply limiting vitamins, but the organization and ecological significance of these interactions remain poorly resolved. For blooms of Karenia brevis, a harmful dinoflagellate that requires multiple B-vitamins, the role of microbial partners in contributing vitamin biosynthesis, salvage, and exchange, how these functions are partitioned across the microbiome, or how such interactions affect bloom proliferation and decline are largely unknown.

Here, we integrated metagenomic and metatranscriptomic analyses of laboratory K. brevis cultures with diel-cycle field metatranscriptomes from natural blooms along the western Florida coast. In culture, vitamin pathways were not encoded by single, self-sufficient microbial taxa. Instead, biosynthesis, salvage, transport, and utilization functions were distributed across distinct bacterial ‘guilds’, revealing a division of metabolic labor within the K. brevis microbiome. This partitioning was most pronounced for thiamine, biotin, and cobalamin, with different bacterial guilds specializing in specific vitamin pathways or pathway components. These guilds likely support both K. brevis and other members of the microbiome, forming a metabolically interdependent network rather than a simple one-way exchange between algal host and bacterial vitamin producer. We further examined diel metatranscriptomic data collected from natural K. brevis blooms in the Western Florida Coast to determine whether the vitamin-contributing guilds identified in culture are active in situ. Field data revealed expression of bacterial vitamin biosynthesis, salvage, and transport functions during blooms, supporting the ecological relevance of the distributed guild structure observed in culture. Together, these results indicate that distributed vitamin metabolism is a key organizational feature of the K. brevis microbiome and may help regulate the metabolic interdependencies that influence bloom maintenance, proliferation, and eventual demise.
 

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