Ecological role of the heterotrophic protist Aurantiochytrium (Labyrinthulomycetes) as a key consumer of viral-induced dissolved organic matter following the lysis of the red tide-forming microalga Heterosigma akashiwo

ABSTRACT Marine algal blooms play a vital role in oceanic carbon cycling. However, the ecological consequences of the organic matter released following bloom collapse via viral infection are poorly understood. Recent studies have shown that viral infection dramatically alters the intracellular metabolite composition of the host, and that the resulting viral lysate selectively promotes the growth of specific prokaryotic populations. This study aimed to elucidate the effects of organic matter derived from healthy and virus-infected cells of the bloom-forming alga Heterosigma akashiwo on the growth of heterotrophic eukaryotes, specifically labyrinthulomycetes. These marine protists are primarily saprotrophic or predatory and contribute to dissolved organic matter (DOM) decomposition and nutrient cycling. Field monitoring conducted in Osaka Bay over a 12-month period revealed that, although the overall Labyrinthulomycetes community showed no clear seasonality, specific populations of these protists co-occurred with Heterosigma akashiwo . To mechanistically investigate the potential trophic linkage suggested by these field observations, a co-culture system comprising H. akashiwo , its specific virus (HaV53), and Aurantiochytrium sp. NBRC102614, used as a model labyrinthulomycete, was established. In co-culture experiments, viral lysis of H. akashiwo led to a significant increase in the cell density of Aurantiochytrium sp., demonstrating that Aurantiochytrium can thrive on substrates derived from virus-infected algae, including viral-induced dissolved organic matter (vDOM). These findings highlight that heterotrophic Labyrinthulomycetes are key consumers of virus-modified organic matter, playing a pivotal role in carbon cycling following the collapse of harmful algal blooms and influencing carbon transfer within coastal microbial food webs. IMPORTANCE Marine ecosystems are shaped by interactions among microalgae, viruses, and heterotrophic eukaryotes, although the ecological roles of heterotrophic protists remain poorly understood. This study investigated the dynamics of oceanic microalgae and heterotrophic eukaryotes, namely Heterosigma species and Labyrinthulomycetes, and examined the effects of viral infection of Heterosigma akashiwo on the growth and proliferation of Aurantiochytrium species, members of the heterotrophic Labyrinthulomycetes. Our results revealed the dynamics of several Labyrinthulomycetes associated with Heterosigma populations and suggested that Aurantiochytrium species can redistribute carbon by utilizing the vDOM released during Heterosigma bloom termination induced by viral infection. These findings also reposition Aurantiochytrium from a passive heterotrophic component to an active ecological agent associated with Heterosigma viral infection, thereby influencing microalgal community dynamics. Overall, this study provides new insights into the fate of virus-infected Heterosigma in coastal marine systems, mediated by heterotrophic Labyrinthulomycetes, particularly Aurantiochytrium species, thereby filling an important knowledge gap in microbial ecology.