Algal symbiosis adaptively restructures the cnidarian microbiome to enhance holobiont metabolism

Abstract Microbiomes are integral to the function and resilience of cnidarian holobionts, yet the spatial and functional integration of microbial communities within host tissues remains poorly understood. Here, we show that symbiosis with photosynthetic dinoflagellates induces adaptive, tissue-specific restructuring of the microbiome in the cnidarian model Aiptasia, fundamentally enhancing holobiont nitrogen assimilation and metabolic flexibility. Using laser microdissection, tissue-resolved metatranscriptomics, gnotobiotic hosts, and stable isotope tracing, we reveal that symbiosis profoundly restructures microbial communities across the epidermis and gastrodermis, enriching for taxa and pathways that support nitrogen assimilation in photosynthetically active tissues. Expression of microbial nitrite reductase is strongly upregulated in the symbiotic gastrodermis, and 15 N-tracer experiments demonstrate that bacterial assimilation of nitrite synergizes with algal symbionts to fuel the biosynthesis of essential amino acids. These findings show that symbiosis drives spatially compartmentalized microbiome adaptation within animal tissues, aligning microbial metabolism with host-algal nutrient exchanges to enhance holobiont functioning.