Novel lipid biomarkers for algal resistance to viral infection in the ocean

Abstract

Marine viruses play a key role in regulating phytoplankton populations, greatly affecting the biogeochemical cycling of major nutrients in the ocean. Resistance to viral infection has been reported for various phytoplankton species under laboratory conditions. Nevertheless, the occurrence of resistant cells in natural populations is underexplored due to the lack of sensitive tools to detect these rare phenotypes. Consequently, our current understanding of the ecological importance of resistance and its underlying mechanisms is limited. Here, we sought to discover lipid biomarkers for the resistance of the bloom-forming alga Emiliania huxleyi to its specific virus, E. huxleyi virus (EhV). We identified novel glycosphingolipids (GSLs) that characterize resistant E. huxleyi strains by applying an untargeted lipidomics approach. Further, we detected these lipid biomarkers in E. huxleyi isolates that were recently collected from E. huxleyi blooms and used them to detect resistant cells in the demise phase of an open ocean E. huxleyi bloom. Lastly, we show that the GSL composition of E. huxleyi cultures that recover following infection and gain resistance to the virus resembles that of resistant strains. These findings highlight the metabolic plasticity and co-evolution of the GSL biosynthetic pathway and underscore its central part in this host-virus arms race.