Coccolithovirus facilitation of carbon export in the North Atlantic

Christien P. Laber, Jonathan E. Hunter, Filipa Carvalho, James R. Collins, Elias J. Hunter, Brittany M. Schieler, Emmanuel Boss, Kuldeep More, Miguel Frada, Kimberlee Thamatrakoln, Christopher M. Brown, Liti Haramaty, Justin Ossolinski, Helen Fredricks, Jozef I. Nissimov, Rebecca Vandzura, Uri Sheyn, Yoav Lehahn, Robert J. Chant, Ana M. Martins, Marco J. L. Coolen, Assaf Vardi, Giacomo R. DiTullio, Benjamin A. S. Van Mooy, Kay D. Bidle

Marine phytoplankton account for approximately half of global primary productivity 1 , making their fate an important driver of the marine carbon cycle. Viruses are thought to recycle more than one-quarter of oceanic photosynthetically fixed organic carbon 2 , which can stimulate nutrient regeneration, primary production and upper ocean respiration 2 via lytic infection and the 'virus shunt'. Ultimately, this limits the trophic transfer of carbon and energy to both higher food webs and the deep ocean 2 . Using imagery taken by the Moderate Resolution Imaging Spectroradiometer (MODIS) onboard the Aqua satellite, along with a suite of diagnostic lipid- and gene-based molecular biomarkers, in situ optical sensors and sediment traps, we show that Coccolithovirus infections of mesoscale (~100 km) Emiliania huxleyi blooms in the North Atlantic are coupled with particle aggregation, high zooplankton grazing and greater downward vertical fluxes of both particulate organic and particulate inorganic carbon from the upper mixed layer. Our analyses captured blooms in different phases of infection (early, late and post) and revealed the highest export flux in 'early-infected blooms' with sinking particles being disproportionately enriched with infected cells and subsequently remineralized at depth in the mesopelagic. Our findings reveal viral infection as a previously unrecognized ecosystem process enhancing biological pump efficiency.