Complex viral interactions revealed for the harmful bloom-forming dinoflagellate Karenia brevis

Karenia brevis regularly forms harmful blooms along the West Florida Shelf that negatively affect marine and terrestrial organisms through toxin production. These blooms impose economic and environmental hardship, driving the need for research to understand the factors influencing their dynamics and to mitigate their impacts. A mostly unresolved issue is the potential role of viruses in bloom termination. We conducted an experiment incubating K. brevis cultures with size-fractionated bloom water samples. Flow cytometry revealed giant virus-like populations (VLPs) in replicate cultures with <1 μm-filtered and <0.2 μm-filtered bloom water. The VLPs' abundance was paralleled by declines in photoefficiency and culture lysis. Metagenomic analyses of the lysates revealed 11 giant virus genomes (35%-100% complete) representing 7 viral operational taxonomic units (vOTUs) within the order Imitervirales (Nucleocytoviricota). Ten of these vOTUs were more abundant in the incubations with <0.2 μm-filtered bloom water, coinciding with the absence or low abundance of algicidal bacteria. The vOTUs and K. brevis cell abundances showed a positive correlation at a coastal site during bloom and nonbloom periods. The most apparent association was to vOTU6, which may owe its competitive advantage to the presence of the auxiliary metabolic genes bacteriorhodopsin, carbonic anhydrase, and dinoflagellate viral nucleoprotein. The metagenomes also contained polinton-like virus (PLV) genomes. Since many PLVs are hypothesized to depend on co-infection with Nucleocytoviricota viruses for their propagation, our results suggest complex viral interactions within K. brevis blooms. Future research to elucidate virus-bacteria-K. brevis interaction mechanisms may be key to understanding bloom dynamics and developing management tools.