Viral infection of algal blooms leaves a halogenated footprint on the dissolved organic matter in the ocean

Algal blooms are important hotspots of primary production in the ocean, forming the basis of the marine food web and fueling the pool of dissolved organic matter (DOM) 1 , which is the largest global inventory of reduced carbon and a market place for metabolic exchange in the ocean 2 . Marine viruses are key players in controlling algal bloom demise and act as major biogeochemical drivers of nutrient cycling and metabolic fluxes by shunting algal biomass from higher trophic levels to the DOM pool, a process termed the ‘viral shunt’ 3,4 . Nevertheless, the metabolic composition of virus-induced DOM (vDOM) in the marine environment is unknown. To decode the metabolic footprint of the ‘viral shunt’, we induced a bloom of the ecologically important alga Emiliania huxleyi in the natural environment, and followed its succession using an untargeted exometabolomics approach. Here we show that algal bloom succession induces extensive and dynamic changes in the exometabolic landscape, especially during bloom demise. By correlating to a specific viral gene marker, we discovered a set of novel chlorine-iodine-containing metabolites that were induced by viral infection and copiously released during bloom demise. We further detected several of these chloro-iodo metabolites in virus-infected open ocean blooms of E. huxleyi , supporting their use as sensitive biomarkers for virus-induced demise in the natural environment. Therefore, we propose halogenation to be a hallmark of the E. huxleyi vDOM, providing insights into the profound metabolic consequences of viral infection for the marine DOM pool.