Diverse ssRNA viruses associated with <i>Karenia brevis</i> harmful algal blooms in southwest Florida

Harmful algal blooms (HABs) caused by the dinoflagellate <i>Karenia brevis</i> frequently occur in the eastern Gulf of Mexico, where they negatively impact the environment, human health, and economy. Very little is known about viruses associated with <i>K. brevis</i> blooms, although viral infection of other HAB-forming phytoplankton species can play an important role in bloom dynamics. We used viral metagenomics to identify viruses in 11 pooled seawater samples collected from southwest Florida, USA, in 2021 during a severe, spatiotemporally dynamic <i>K. brevis</i> bloom. Assembled viral genomes were similar to published genomes from the order <i>Picornavirales</i>, family <i>Marnaviridae</i>, and genera <i>Sogarnavirus</i>, <i>Bacillarnavirus</i>, and <i>Marnavirus</i>. Several of the cultured viruses from these groups infect bloom-forming diatoms (<i>Chaetoceros</i> sp. and <i>Rhizosolenia setigera</i>) and the raphidophyte <i>Heterosigma akashiwo</i>. We also recovered unclassified <i>Riboviria</i> genomes related to a <i>Symbiodinium</i> positive-sense ssRNA virus sequenced from coral dinoflagellate symbionts. Reverse-transcriptase PCR assays were performed to monitor the occurrence of seven representative virus genomes in these samples from 2021 and 43 seawater samples collected during a subsequent, typical bloom between November 2022 and May 2023. Over half of the samples contained multiple viruses, and at least one viral genome was detected in 44 of the 54 samples collected across seasons and years, highlighting the ubiquity of these viruses in this region. Alpha diversity was highest in the summer months and positively correlated with <i>K. brevis</i> cell counts. Multiple regression revealed month and the presence of unclassified <i>Riboviria</i> sequences most similar to dinoflagellate viruses as significant predictors of <i>K. brevis</i> cellular abundance.IMPORTANCEHarmful algal blooms caused by the dinoflagellate <i>Karenia brevis</i> negatively impact the tourism, fisheries, and public health sectors. Anticipated impacts of climate change, nutrient pollution, and ocean acidification may sustain and/or exacerbate <i>K. brevis</i> blooms in the future, underscoring the need for proactive monitoring, communication, and mitigation strategies. This study represents a pioneering effort in monitoring viruses associated with <i>K. brevis</i> blooms. The findings lay the groundwork for studying the effects of environmental drivers on <i>K. brevis</i> blooms and their associated viruses, as well as for exploring the roles of viruses in bloom dynamics and potential applications of viruses as biocontrol agents for <i>K. brevis</i> blooms. Furthermore, the comparison of viral dynamics relative to local and regional bloom dynamics in this study helps inform future monitoring and modeling needs.