Diverse ssRNA viruses associated with Karenia brevis harmful algal blooms in Southwest Florida

Abstract

Harmful algal blooms (HABs) caused by the dinoflagellate Karenia brevis 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 K. brevis 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 K. brevis bloom. Assembled viral genomes were similar to published genomes from the order Picornavirales, family Marnaviridae, and genera Sogarnavirus, Bacillarnavirus, and Marnarnavirus. Viruses from these groups infect bloom-forming diatoms (Chaetoceros sp. and Rhizosolenia setigera) and the raphidophyte Heterosigma akashiwo. We also recovered unclassified Riboviria genomes related to a Symbiodinium 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 2021 samples 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 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 K. brevis cell counts. Multiple regression revealed month and the presence of unclassified Riboviria sequences most similar to dinoflagellate viruses as significant predictors of K. brevis cellular abundance. ImportanceHarmful algal blooms caused by the dinoflagellate Karenia brevis negatively impact the tourism, fisheries, and public health sectors. Anticipated impacts of climate change, nutrient pollution, and ocean acidification may sustain and/or exacerbate K. brevis 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 K. brevis blooms. The findings lay the groundwork for studying the effects of environmental drivers on K. brevis 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 K. brevis blooms. Furthermore, the comparison of viral dynamics relative to local and regional bloom dynamics in this study helps inform future monitoring and modeling needs.