Taxonomic difference in marine bloom-forming phytoplanktonic species affects dynamics of both bloom-responding prokaryotes and prokaryotic viruses

Abstract

The production of dissolved organic matter during phytoplankton blooms and consumption by heterotrophic prokaryotes promotes marine carbon biogeochemical cycling. Although prokaryotic viruses are crucial biological entities, their dynamics during such blooms are not fully understood. Here, we investigated the dynamics of coastal prokaryotic communities and viruses during blooms in a microcosm experiment using dissolved intracellular fractions of taxonomically distinct phytoplankton, the diatom Chaetoceros sp. (CIF) and the raphidophycean alga Heterosigma akashiwo (HIF). Ribosomal RNA gene amplicon and viral metagenomic analyses revealed that particular prokaryotes and prokaryotic viruses specifically increased in either CIF and HIF, indicating that different phytoplankton intracellular fractions promote distinct dynamics of not only prokaryotic community but also prokaryotic viruses. Our microcosm experiments and environmental data mining identified both known and novel possible host-virus pairs. In particular, a growth of phytoplanktonic organic matter-associated prokaryotes, such as Bacteroidetes Polaribacter and NS9 marine group, Vibrio spp., and Rhodobacteriales Nereida and Planktomarina, was accompanied by an increase in viruses predicted to infect Bacteroidetes, Vibrio, and Rhodobacteriales, respectively. Collectively, our findings suggest that elucidating tripartite relationships among phytoplankton, prokaryotes, and prokaryotic viruses would further our understanding of coastal microbial ecosystems. We state that -All the data underlying the study are available at the DNA Data Bank of Japan (DDBJ) under project number PRJDB14359 and accession number DRA014887. -This study was supported by Grants-in-Aid for Scientific Research (No. 16H06429, No. 17H03850, No. 21H05057, and No. 21J14854) from the Japan Society for the Promotion of Science (JSPS). -We have no potential conflicts of interest to declare. -We have read and understood your journals policies, and we believe that neither the manuscript nor the study violates any of these. -We do not use any clinical data, human subjects, or laboratory animals. -None of the materials have been published or are under consideration for publication elsewhere. CRediTHiroaki Takebe: Funding acquisition, conceptualization, investigation, formal analysis, visualization, and writing (original draft). Kento Tominaga: Conceptualization, investigation, and writing (review and editing). Tatsuhiro Isozaki: investigation. Tetsuhiro Watanabe: Resources. Keigo Yamamoto: Resources. Ryoma Kamikawa: Conceptualization, supervision, and writing (review and editing). Takashi Yoshida: Funding acquisition, project administration, conceptualization, supervision, and writing (review and editing).