An Integrative Genomic and Transcriptomic Analysis Reveals the Divergent Molecular Strategies Driving Mutualism and Pathogenesis in a Dinoflagellate Phycosphere

The dinoflagellate phycosphere hosts mutualistic and algicidal bacteria, but how the algal host integrates these opposing microbial signals is unclear. We used comparative genomics and dual RNA-seq to study Karenia mikimotoi in co-culture with its symbiotic and algicidal bacteria. Genomes revealed distinct potentials: the symbiont is equipped for nutrient exchange, while the algicide possesses a T6SS (Type VI Secretion System) and siderophore synthesis pathways. Dual RNA-seq revealed divergent host strategies. The symbiont induced a defence priming state, upregulating photosynthesis and antioxidant genes. Conversely, the algicide induced systemic metabolic failure. This collapse was driven by the pathogen's active suppression of algal glutathione reductase gene transcription, leading to oxidative stress and a shutdown of central metabolism, including glycolysis and TCA (tricarboxylic acid). The pathogen concurrently activated its T6SS, secreted proteases, and iron-scavenging systems. This study not only reveals the molecular blueprints for algal-bacterial symbiosis and pathogenesis, but it also challenges the conventional perception of these interactions as simplistic models of nutrient provisioning or toxin-mediated assault. It provides a new molecular framework, revealing these interactions as dynamic processes dictated by divergent transcriptomic responses of the host to either initiate a reinforced growth program or execute a systemic metabolic and defensive collapse.