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Abstract Labile dissolved organic carbon in the surface oceans accounts for ~¼ of carbon produced through photosynthesis and turns over on average every three days, fueling one of the largest engines of microbial heterotrophic production on the planet. Volatile organic compounds are poorly constrained components of dissolved organic carbon. Here, we detected 72 m/z signals, corresponding to unique volatile organic compounds, including petroleum hydrocarbons, totaling approximately 18.5 nM in the culture medium of a model diatom. In five cocultures with bacteria adapted to grow with this diatom, 1 to 59 m/z signals were depleted. Two of the most active volatile organic compound consumers, Marinobacter and Roseibium, contained more genes encoding volatile organic compound oxidation proteins, and attached to the diatom, suggesting volatile organic compound specialism. With nanoscale secondary ion mass spectrometry and stable isotope labeling, we confirmed that Marinobacter incorporated carbon from benzene, one of the depleted m/z signals detected in the co-culture. Diatom gross carbon production increased by up to 29% in the presence of volatile organic compound consumers, indicating that volatile organic compound consumption by heterotrophic bacteria in the phycosphere – a region of rapid organic carbon oxidation that surrounds phytoplankton cells – could impact global rates of gross primary production. 

Abstract Volatile Organic Compounds (VOCs) are a diverse collection of molecules critical to cell metabolism, food web interactions, and atmospheric chemistry. The eukaryotic coccolithophoreGephyrocapsa huxleyi, an abundant coastal eukaryotic phytoplankter, forms massive blooms in coastal upwelling regions, which are often terminated by viruses (EhVs).G. huxleyiproduces 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 strainG. huxleyiCCMP374. 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 ofG. huxleyireleases VOCs which are much more diverse than previously recognized. We further show that EhV207 primarily accelerates existing metabolic processes inG. huxleyiand 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.