Unique microbial module regulates the harmful algal bloom (Cochlodinium polykrikoides) and shifts the microbial community along the Southern Coast of Korea.

Harmful algal blooms (HABs) of Cochlodinium (aka Margalefidinium) polykrikoides cause huge economic and ecological damages and thus are considered environmental problems. Previous studies uncovered that the formation and collapse of phytoplankton blooms could be closely related to their associated microbes although their roles in C. polykrikoides bloom have not been elucidated yet. To explore the potential interactions between C. polykrikoides and other microbes (archaea, bacteria, and phytoplankton), we collected water samples in the free-living (FL) (0.22 to 3 μm), nanoparticle-associated (NP) (3 to 20 μm), and microparticle-associated (MP) (>20 μm) fractions when C. polykrikoides blooms occurred from July to August in 2016, 2017, and 2018 in the South Sea of Korea. The microbial composition of the C. polykrikoides-associated microbial cluster (Module I) significantly differed from those of other modules associated with Alexandrium, Chaetoceros or Chattonella. Over half of the interspecies interactions in Module I occurred within the module. That is, specific microbial clusters were associated with the C. polykrikoides bloom. Structural equation modeling (SEM) further confirmed the stronger effects of Module I on C. polykrikoides blooms compared to environmental factors. Among the operational taxonomic units (OTUs) directly correlated with C. polykrikoides, Marine Group I was presumed to supply vitamin B, the essential element for C. polykrikoides growth, while the potential fish pathogens (Micrococcaceae and Piscirickettsiaceae) could contribute to the massive fish death together with C. polykrikoides itself. In addition, the zoospores of Syndiniales, a parasitoid to dinoflagellates, might be related to the sudden collapse of C. polykrikoides blooms. These microbial groups also contributed to significant alterations of the local microbial community structures. Collectively, network analysis and SEM revealed that the C. polykrikoides bloom is concomitant with distinct microbial communities, contributing to the rise and fall of the bloom, and finally determining the local microbial community structures.