Mapping of the viral shunt across widespread coccolithophore blooms using metabolic biomarkers

Abstract

The viral shunt is a fundamental ecosystem process which diverts the flux of organic carbon from grazers to heterotrophic microorganisms. Through the extracellular release of metabolites, lytic viral infections supply 2-10% of photosynthetically fixed carbon in the ocean for bacterial respiration. Despite its significance for the carbon cycle, we lack tools to detect the viral shunt in the natural environment and assess its ecological impact. Here, we study the use of exometabolites as biomarkers for the viral shunt by applying molecular, metabolomics, and oceanographic tools in blooms of the cosmopolitan microalga Gephyrocapsa huxleyi across the Atlantic Ocean, spanning four biogeochemical provinces between Iceland and Patagonia. We mapped the distinct metabolic footprint of its viral infections using exo- and endometabolomics approaches and detected nineteen organohalogen metabolites across the blooms, showing their global formation. Time-resolved comparison of particulate and dissolved metabolite pools during an induced mesocosm bloom indicated virocells - actively infected host cells - as the source of the halogenated metabolites. Three trichloro-iodo metabolites were present during demise of all virus-infected blooms, highlighting them as suitable metabolic biomarkers. The environmental stability of these halometabolites in the DOM pool over a few days can recapitulate viral infections at earlier stages of phytoplankton bloom succession.