Viral infection impacts volatile organic compound production in the coccolithophore Gephyrocapsa huxleyi

Abstract

Volatile Organic Compounds (VOCs) are a diverse collection of molecules critical to cell metabolism, food web interactions, and atmospheric chemistry. The eukaryotic coccolithophore Gephyrocapsa huxleyi, an abundant coastal eukaryotic phytoplankter, forms massive blooms in coastal upwelling regions, which are often terminated by viruses (EhVs). G. huxleyi produces organosulfur VOCs such as dimethyl sulfide (DMS) and halogenated metabolites that play key roles in atmospheric chemistry. Here we resolved the role of lytic viral infection by EhV207 on VOC production of the model strain G. huxleyi CCMP374. Our analysis identified 79 VOCs significantly impacted by viral infection, particularly during cell lysis, with sulfur containing VOCs like DMS dominating the profiles. Viral lysis results in a nearly six-fold increase in VOC production and generated a previously unrecognized range of VOCs, including 15 sulfur, 22 nitrogen, 2 phosphorus, 19 oxygen and 17 halogen-containing compounds. These findings reveal that viral infection of G. huxleyi releases VOCs which are much more diverse than previously recognized. We further show that EhV207 primarily accelerates existing metabolic processes in G. huxleyi and facilitates the release of pre-existing intracellular VOCs rather than inducing novel biochemical pathways. This wide range of VOCs may be produced on a massive scale during coccolithophore bloom-and-bust cycles, with important impacts on coastal biogeochemistry and surface ocean/atmosphere interactions.