Friends and foes: symbiotic and algicidal bacterial influence on Karenia brevis blooms

Harmful Algal Blooms (HABs) of the toxigenic dinoflagellate Karenia brevis (KB) are pivotal in structuring the ecosystem of the Gulf of Mexico (GoM), decimating coastal ecology, local economies, and human health. Bacterial communities associated with toxigenic phytoplankton species play an important role in influencing toxin production in the laboratory, supplying essential factors to phytoplankton and even killing blooming species. However, our knowledge of the prevalence of these mechanisms during HAB events is limited, especially for KB blooms. Here, we introduced native microbial communities from the GoM, collected during two phases of a Karenia bloom, into KB laboratory cultures. Using bacterial isolation, physiological experiments, and shotgun metagenomic sequencing, we identified both putative enhancers and mitigators of KB blooms. Metagenome-assembled genomes from the Roseobacter clade showed strong correlations with KB populations during HABs, akin to symbionts. A bacterial isolate from this group of metagenome-assembled genomes, Mameliella alba, alleviated vitamin limitations of KB by providing it with vitamins B₁, B₇ and B₁₂. Conversely, bacterial isolates belonging to Bacteroidetes and Gammaproteobacteria, Croceibacter atlanticus, and Pseudoalteromonas spongiae, respectively, exhibited strong algicidal properties against KB. We identified a serine protease homolog in P. spongiae that putatively drives the algicidal activity in this isolate. While the algicidal mechanism in C. atlanticus is unknown, we demonstrated the efficiency of C. atlanticus to mitigate KB growth in blooms from the GoM. Our results highlight the importance of specific bacteria in influencing the dynamics of HABs and suggest strategies for future HAB management.