Viral infection to the raphidophycean alga <i>Heterosigma akashiwo</i> affects both intracellular organic matter composition and dynamics of a coastal prokaryotic community

Marine microalgae play a crucial role in the marine ecosystem by supplying dissolved organic matter to heterotrophic prokaryotes, which mediate the microbial loop. Microalgae are often infected by viruses, and in infected cells (virocells), the viruses modulate and often change the host metabolism for propagation and endo-metabolites. However, the impact of algal virocells on prokaryotic communities is not fully understood. In this study, we investigated whether lysates from virocells of <i>Heterosigma akashiwo,</i> a globally prevalent bloom-forming raphidophycean alga, cause shifts in prokaryotic community structure, and which metabolic compounds in the viral lysate might affect the surrounding prokaryotic populations. Using microcosm experiments, we cultured prokaryotic communities with a viral dissolved fraction (VDF) of <i>H. akashiwo</i>. Results revealed that certain prokaryotic populations assigned as <i>Vibrio</i> spp. pathogenic to fish and crustaceans grew specifically in response to the VDF. These <i>Vibrio</i> species possessed a gene module for branched-chain amino acids transporters, which were revealed to be enriched in VDF by gas chromatography-mass spectrometry analysis. Altogether, our findings suggest that viral infection-induced changes in biochemical properties of <i>H. akashiwo</i> cells can promote the growth of taxonomically and metabolically different prokaryotic populations, potentially impacting higher trophic-level consumers in marine ecosystems.IMPORTANCEThe primary production by marine microalgae and the consumption of the produced organic matter by prokaryotes significantly contribute to biogeochemical cycling. Microalgae are often infected by viruses, and in infected cells (virocells), the viruses modulate host metabolism for propagation and endo-metabolites. However, the impact of microalgal virocells on prokaryotic communities is not fully understood. This study investigates effects of lysates from virocells of <i>Heterosigma akashiwo</i>, a globally distributed harmful bloom-forming raphidophycean alga, on the prokaryotic community. Our data suggest that changes in biochemical properties in <i>H. akashiwo</i> virocells promoted the growth of specific bacterial populations that appeared to have metabolic capacity to utilize certain organic compounds enriched in the lysate. Additionally, as those populations included fish-pathogenic bacteria, we propose that viral infection to <i>H. akashiwo</i> can indirectly affect higher trophic-level consumers in marine ecosystems.