Bacterial generalists and fungal specialists play important roles in maintaining community stability and regulating microbial diversity of the algae-associated microbiome throughout the growth cycle of Alexandrium pacificum.

Abstract

The algae-associated microbiome represents a consortium that has been chronically domesticated by specific algae, maintaining a close relationship with the host population. Although the microbes associated with dinoflagellates have garnered significant attention in recent years, the interactions and contributions of microbial generalists and specialists through the growth cycle of a bloom-forming dinoflagellate remain largely unexplored. Herein, the ecological and evolutionary characteristics of free-living generalists and specialists within bacterial and fungal communities were investigated during the growth process of Alexandrium pacificum cultured in the laboratory for years without antibiotic treatment. From an ecological perspective, bacterial generalists and fungal specialists dominated the community, indicating different microbial niche patterns between the bacterial and fungal consortia. Furthermore, microbial specialists were more susceptible to disturbance from algal proliferation, as evidenced by greater community dissimilarity and determinacy-dominated assembly processes. Compared with their counterparts, the molecular networks of bacterial generalists and fungal specialists were more complex and robust, suggesting that they significantly contributed to resistance to environmental stress and functional maintenance. Evolutionarily speaking, bacterial generalists and fungal specialists showed much higher diversification potential, and others featured higher extinction rates. Despite these differences, a continuous transition from the former two to their counterparts was observed, alleviating the "Matthew effect" in the biological world for ecological trade-offs. Collectively, these findings emphasize that bacterial generalists and fungal specialists play important roles in maintaining community stability and regulating microbial diversity during the growth process, which expands the current understanding of the maintenance mechanisms of the diversity and community of phytoplankton-associated microbes in the face of disturbance from bloom-forming dinoflagellates.IMPORTANCELike the microbes residing in the rhizosphere and human gut, bacteria that coexist chronically with microalgae exemplify a relationship, forming potentially intimate partnerships with the host. However, studies on the ecological significance of algae-associated microbiomes with different niches under the interference of bloom-forming species are still lacking. This work investigated the ecological interactions and contributions of generalists and specialists within algae-associated bacterial and fungal communities across the growth cycle of Alexandrium pacificum for the first time. These results increase the understanding of the microbial ecology of algae-associated microbes in the context of interference from the proliferation of harmful algal bloom species.