Name: Miguel Frada

Email: frada@marine.rutgers.edu

Author: Miguel Frada1,2,*, Ian Probert1 , Michael J. Allen3, William H. Wilson4, Colomban de Vargas1

Author affiliation: 1 Station Biologique, Equipe EPPO-Evolution du Plancton et PaleOceans, CNRS et Université Pierre et Marie Curie (UMR 7144), Station Biologique, 29682 Roscoff, France 2 (present address) Environmental Biophysics and Molecular Ecology Program Institute of Marine and Coastal Sciences Rutgers University 71 Dudley Road New Brunswick, NJ 08901 3 Plymouth Marine Laboratory, Prospect Place, The Hoe, Plymouth PL1 3DH, United Kingdom 4 Bigelow Laboratory for Ocean Sciences, 180 McKown Point, P.O. Box 475, West Boothbay Harbor, ME 04575-0475 * Presenting author

Abstract title: The Cheshire Cat escape strategy of the coccolithophore Emiliania huxleyi in response to viral infection: in vitro and in situ observations

Absstract:

The coccolithophore Emiliania huxleyi is one of the most successful eukaryotes in modern oceans. Similarly to what is frequent among haptophytes, E. huxleyi is characterized by two phases in its life cycle, one haploid and the other diploid, each exhibit radically different phenotypes. The diploid calcified phase forms extensive blooms, profoundly impacting global biogeochemistry. By contrast, the role of the non-calcified haploid phase has been completely overlooked. Giant phycodnaviruses (E. huxleyi viruses, EhVs) have been shown to infect the diploid phase cells and to be heavily implicated in the termination of blooms. Here, we demonstrate in vitro using multiple host and viral strains that the haploid phase of E. huxleyi is unrecognizable and therefore resistant to EhVs that kill the diploid phase. We further show that exposure of diploid E. huxleyi to EhVs induces transition to the haploid phase. Thus we have clearly demonstrated a drastic difference in viral susceptibility between life cycle stages with different ploidy levels in a unicellular eukaryote. Resistance of the haploid phase of E. huxleyi provides an escape mechanism that involves separation of meiosis from sexual fusion in time, thus ensuring that genes of dominant diploid clones are passed on to the next generation in a virus-free environment. These ecological dynamics, that we named the “Cheshire cat” dynamics, release host evolution from pathogen pressure and thus can be seen as an opposite force to a classic ‚”Red Queen” coevolutionary arms race. In E. huxleyi, this phenomenon can account for the fact that the selective balance is tilted toward the boom-and-bust scenario of optimization of both growth rates of calcifying E. huxleyi cells and infectivity of EhVs. Furthermore, recent in situ observations during a mesocosm field experiment where E. huxleyi bloom were induced by nutrients addition, we revealed that calcified (diploid) and non-calcified E. huxleyi cells were present in the water since the begining of the experiment. Later after the exponential growth and subsequent collapse of the calcified cells due to viral infection we observed a rapid development of a small E. huxleyi non-calcified population. At the same time we also observed the appearence in the water of groups of flagellated autotrophic cells attached to agglomerated E.huxleyi calcareous scales, probably representing new haploid cells formed through meiosis. These observations suggest that the “Cheshire cat” dynamics may indeed take place in natural populations in response to viral threaten, being probably a fundamental strategy for E. huxleyi survival and ecological success.