Past and present oceanic virus-host dynamics
a. Collaborative Research: Lipid lubrication of oceanic carbon and sulfur biogeochemistry via a host-virus chemical arms race” [Kay Bidle (lead PI, Rutgers University), Marco Coolen and Ben van Mooy (co-PIs WHOI), Jack DiTullio (co-PI Charleston College), Assaf Vardi (co-PI Weizmann Institute, Israel)].
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, Haptophyta) 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 demonstrated that viruses employ a sophisticated, co-evolutionary “arms race” in mediating host-virus interactions. Our team recently also 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. Observations of vGSLs in the North Atlantic and Norwegian fjords further suggested 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 argued 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 C and S.
For our recently funded multi institutional NSF-OCE project entitled “Collaborative Research: Lipid lubrication of oceanic carbon and sulfur biogeochemistry via a host-virus chemical arms race” our team is currently studying the molecular, ecological, and biogeochemical links between vGSLs (and other polar lipids) and the global cycles of carbon and sulfur. During our recent North Atlantic VICE cruise we combined a suite of lab-based, mechanistic studies using several haptophyte-virus model systems along with observational studies, and manipulative field-based experiments to document active viral infection of natural coccolithophore populations. These studies were coupled 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). Given they are unique to viruses, we will elucidate whether 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. Our overarching hypothesis 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.
As part of this large-scale ongoing project my lab is currently studying the overall diversity of plankton and their viruses from photic zone water samples collected along a transect from the Azores to Iceland during our recent VICE cruise. While the E. huxleyi/EhV system is the cornerstone of this project, our molecular datasets will reveal the dynamics of additional important algal-virus systems in the North Atlantic, and which oceanic environmental parameters play the largest role in shaping the genetic diversity of host-virus ecosystems. From these results we will also be able to predict how these host-virus systems will be affected in a global change scenario.
b. Viral impact on past plankton distributions.
Plankton-infecting viruses are estimated to be the most abundant biological entity in the world’s oceans. Knowledge about the role of past phytoplankton-infecting viruses is essential for more precise paleoecological assessments as viral infection often results in lysis of plankton cells and greatly affects plankton distributions. Despite their importance, essentially nothing was known about phytoplankton-virus interactions in the past. I recently generated the first paleo-record for a suite of viruses (EhV) and their host (calcified diploid stage of E. huxleyi-strains) in the Black Sea, which was published in Science last year (Coolen, 2011). The data shows that the same virus and host populations can persist for centuries. Major changes in virus and host populations occurred during the warm and moist HCO until ~5600 years ago, and during the colder and wetter Subatlantic climate of the past 2500 years, when the Black Sea experienced dramatic changes in hydrologic and nutrient regimes. Unit I saw a reoccurrence of the same host genotype thousands of years later in the presence of a different subset of viruses. This study showed for the first time that historical plankton virus populations could be included in paleoecological and paleoenvironmental studies.