Award: OCE-1061883

Intellectual Merit. The coccolithophore Emiliania huxleyi is a unicellular phytoplankton that forms massive blooms in the global ocean that span up to 100,000 km2 and can be observed with Earth-observing satellites. As a photosynthetic organism that uses sunlight to convert CO2 into biomass, it plays a key role in EarthÆs carbon cycle. This impact on the carbon cycle is two fold given its ability to also biomineralize calcium carbonate into calcite cell walls (coccoliths). In the oceans, E. huxleyi cells also face a challenge, an æarms raceÆ of sorts, in that they are routinely infected, lysed, and terminated by specific, double-stranded DNA containing viruses called Coccolithoviruses or EhVs (Figure 1). This arms race is a natural aspect of the ecology of all marine microbes, as viruses are the most abundance entities in the oceans (averaging 10 million viruses per milliliter of seawater) and have an ancient evolutionary history. As members of the Phycodnaviridae, EhVs are giant microalgal viruses (~180 nm in diameter) with an extensive genetic capability (~407 kb genomes) to manipulate host metabolic pathways for their replication. Owing to the collective insight gained from genomics (both host and virus genomes have been sequenced) and the array of genetically diverse host (sensitive and resistant) and virus strains in culture, the E. huxleyi–EhV host-virus is one of the best model systems for investigating algal host-virus interactions and the cellular processes that mediate infection dynamics. This project uncovered that coccolithoviruses employ a sophisticated, coevolutionary arms race to rewire and manipulate host lipid metabolism, altering a specific class of lipids known as glycosphingolipids (GSL), and in turn, regulate cell fate by inducing reactive oxygen species and key proteolytic enzymes (caspases and metacaspases) that trigger host programmed cell death (Figures 1-2). These unique GSL lipid molecules are central to successful infection E. huxleyi and its EhV viruses, and given their unique chemical signature and bioactivity, can be used as novel diagnostic biomarkers to detect the extent of virus infection in the oceans—an ability that microbial oceanographers have lacked until now. This project elucidated the molecular, ecological, and biogeochemical links between GSLs, EhV infection of E. huxleyi, and the global cycles of carbon and sulfur (E. huxleyi also produces dimethyl sulfide, an important sulfur-based gas that can moderate EarthÆs climate). Our work combined a suite of lab-based, mechanistic studies using E. huxleyi-virus model systems along with observational studies and manipulative field-based experiments in Norwegian fjords and the Northeast Atlantic. Using a suite of different GSLs and other cellular targets as diagnostic markers, we documented active viral infection of different natural E. huxleyi populations and coupled it with a suite of oceanographic measurements in order to quantify how viral infection (via GSLs) influences cell fate, the dissolved organic carbon (DOC) pool, sinking and vertical export of particular organic (POC) and inorganic carbon (PIC; as calcium carbonate, CaCO3) and the upper ocean sulfur cycle (via the cycling of DMS and other biogenic sulfur compounds. Our work showed that vGSLs are cornerstone molecules in the upper ocean, which facilitate viral infection on massive scales and mechanistically ælubricateÆ the biogeochemical fluxes of C and S in the ocean (Figure 3). A key finding from our work was that active EhV infection (and the cellular pathways induced by it) play key role in the formation of aggregates and the sinking flux of organic matter into the deep ocean (Figure 4). This is counter to the traditional paradigm invoking cell lysis and the retention of this carbon in the upper ocean, fueling the æmicrobial respirationÆ. This has important implications for the sequestration of carbon into the deep ocean. Broader Impact: Research blended conc...