Collaborative Research: Lipid lubrication of oceanic carbon and sulfur biogeochemistry via a host-virus chemical arms race

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Intellectual Merit: Despite the critical importance of viruses in shaping marine microbial ecosystems, very little is known about the molecular mechanisms mediating phytoplankton-virus interactions. As a consequence, we currently lack biomarkers to quantify active viral infection in the oceans, significantly hindering our understanding of its ecological and biogeochemical impacts. The coccolithophore Emiliania huxleyi (Prymnesiophyceae, Haptophyte) is a cosmopolitan unicellular photoautotroph whose calcite skeletons account for about a third of the total marine CaCO3 production. E. huxleyi forms massive annual spring blooms in the North Atlantic that are infected and terminated by lytic, giant double-stranded DNA containing coccolithoviruses. Findings that lytic viral infection of E. huxleyi recruits the hosts programmed cell death (PCD) machinery demonstrate that viruses employ a sophisticated, co-evolutionary "arms race" in mediating host-virus interactions. The investigators recently demonstrated that viral glycosphingolipids (vGSLs), derived from unexpected cluster of sphingolipid biosynthetic genes, a pathway never before described in a viral genome, play a crucial functional role in facilitating infection of E. huxleyi. The observations of vGSLs in the North Atlantic and Norwegian fjords further suggest that they may be novel, diagnostic biomarkers for viral infection of coccolithophore populations. At the same time, the discovery of vGSLs and a distinct, protective 802 lipid argues that a host-virus, co-evolutionary chemical arms race plays a pivotal role in regulating viral infection and in lubricating upper ocean biogeochemical fluxes of Carbon and Sulfur.The focus of this project is to elucidate the molecular, ecological, and biogeochemical links between vGSLs (and other polar lipids) and the global cycles of carbon and sulfur. The team of investigators proposes a multi-pronged approach combing a suite of lab-based, mechanistic studies using several haptophyte-virus model systems along with observational studies and manipulative field-based experiments the Northeast Atlantic. Using these diagnostic markers, they will document active viral infection of natural coccolithophore populations and couple it with a suite of oceanographic measurements in order to quantify how viral infection (via vGSLs) influences cell fate, the dissolved organic carbon (DOC) pool, vertical export of particular organic (POC) and inorganic carbon (PIC; as calcium carbonate, CaCO3) (along with associated alkenone lipid biomarkers and genetic signatures of viruses and their hosts) and the upper ocean sulfur cycle (via the cycling of dimethylsulfide [DMS] and other biogenic sulfur compounds). Furthermore, given they are unique to viruses, the investigators propose that vGSLs can be used to trace the flow of virally-derived carbon and provide quantitative insights into a "viral shunt" that diverts fixed carbon from higher trophic levels and the deep sea. The overarching hypothesis for this study is that vGSLs are cornerstone molecules in the upper ocean, which facilitate viral infection on massive scales and thereby mechanistically "lubricate" the biogeochemical fluxes of C and S in the ocean.Broader Impact: This research blends concepts in physiology, molecular biology, biochemistry, viriology and lipid chemistry, with oceanography and biogeochemistry, thereby providing an opportunity whereby researchers with different educational backgrounds can interact and develop. This project provides excellent hands-on training for development of postdocs, graduate students and undergraduate students. The research provides resources and opportunities for inter-institutional exchange Rutgers-WHOI-College of Charleston and builds both on established national and international collaborations and will foster new ones. The PIs will work with COSEE NOW and Networked Ocean World to increase ocean literacy by integrating scientific research with K-12 educators and public audiences. An important component of this project is to bring scientists at sea in touch with classroom students and the general public. As such, the project incorporates several concrete strategies, including: (1) posting web/video blogs from sea; (2) incorporating a freelance videographer to collect multimedia content on a cruise to the Northeast Atlantic, which will be used in diverse post-cruise deliverables; (3) producing "Ocean Gazing" podcasts so the general public can look at, listen to and touch the ocean and unpack some of its secrets by presenting ongoing oceanographic research and interviewing oceanographers; and (4) integrating the research activities with ongoing K-12 teacher workshops as part of the Marine Activities, Resources and Education program and through interactions with Laura Dunbar, a Science/Technology teacher at Sea Girt Elementary School (Sea Girt, NJ).