The coccolithophore Emiliania huxleyi is one of the most successful eukaryotes in modern oceans. The two phases in its haplodiploid life cycle exhibit radically different phenotypes. The diploid calcified phase forms extensive blooms, which profoundly impact global biogeochemical equilibria. By contrast, the ecological role of the noncalcified haploid phase has been completely overlooked. Giant phycodnaviruses (Emiliania huxleyi viruses, EhVs) have been shown to infect and lyse diploid-phase cells and to be heavily implicated in the regulation of populations and the termination of blooms. Here, we demonstrate 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 ''Cheshire Cat'' ecological 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.eukaryotic life cycle ͉ haplo-diploidy ͉ marine viruses ͉ host-parasite interaction ͉ Red Queen

The current paradigm holds that cyanobacteria, which evolved oxygenic photosynthesis more than 2 billion years ago, are still the major light harvesters driving primary productivity in open oceans. Here we show that tiny unicellular eukaryotes belonging to the photosynthetic lineage of the Haptophyta are dramatically diverse and ecologically dominant in the planktonic photic realm. The use of Haptophyta-specific primers and PCR conditions adapted for GC-rich genomes circumvented biases inherent in classical genetic approaches to exploring environmental eukaryotic biodiversity and led to the discovery of hundreds of unique haptophyte taxa in 5 clone libraries from subpolar and subtropical oceanic waters. Phylogenetic analyses suggest that this diversity emerged in Paleozoic oceans, thrived and diversified in the permanently oxygenated Mesozoic Panthalassa, and currently comprises thousands of ribotypic species, belonging primarily to low-abundance and ancient lineages of the ''rare biosphere.'' This extreme biodiversity coincides with the pervasive presence in the photic zone of the world ocean of 19 -hexanoyloxyfucoxanthin (19-Hex), an accessory photosynthetic pigment found exclusively in chloroplasts of haptophyte origin. Our new estimates of depth-integrated relative abundance of 19-Hex indicate that haptophytes dominate the chlorophyll a-normalized phytoplankton standing stock in modern oceans. Their ecologic and evolutionary success, arguably based on mixotrophy, may have significantly impacted the oceanic carbon pump. These results add to the growing evidence that the evolution of complex microbial eukaryotic cells is a critical force in the functioning of the biosphere.Haptophyta ͉ photosynthesis ͉ protistan biodiversity ͉ eukaryotic biodiversity O xygenic photosynthesis, the most complex and energetically powerful molecular process in biology, originated in cyanobacteria more than 2 billion years ago in Archean oceans (1). Marine photosynthesis still contributes Ϸ50% of total primary production on Earth (2). This revolutionary process was integrated, at least once, into an ancestral phagotrophic eukaryotic lineage through the evolution of chloroplasts, which themselves were redistributed to a large variety of aquatic eukaryote lineages via permanent secondary and tertiary endosymbioses (3). Despite this evolutionary trend from photosynthetic prokaryotes to eukaryotes, particularly visible in today's coastal oceans where microalgae such as diatoms and dinoflagellates are omnipresent, cyanobacteria have been repeatedly claimed as the champions of photosynthesis in open ocean waters (4). This hypothesis followed the introduction of flow cytometry and molecular genetic approaches to biological oceanography in the 1980s, which revealed astonishing concentrations of minute cyanobacterial cells of the genera Procholorococcus and Synechococcus in marine waters (5). The physiology, ecology, and functional and environmental genomics of these prokaryotes are subjects of ongoing intensive study (6).Several lines of e...

Marine phytoplankton account for approximately half of global primary productivity , 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 , which can stimulate nutrient regeneration, primary production and upper ocean respiration 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 . 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.

Phytoplankton blooms are ephemeral events of exceptionally high primary productivity that regulate the flux of carbon across marine food webs [1-3]. Quantification of bloom turnover [4] is limited by a fundamental difficulty to decouple between physical and biological processes as observed by ocean color satellite data. This limitation hinders the quantification of bloom demise and its regulation by biological processes [5, 6], which has important consequences on the efficiency of the biological pump of carbon to the deep ocean [7-9]. Here, we address this challenge and quantify algal blooms' turnover using a combination of satellite and in situ data, which allows identification of a relatively stable oceanic patch that is subject to little mixing with its surroundings. Using a newly developed multisatellite Lagrangian diagnostic, we decouple the contributions of physical and biological processes, allowing quantification of a complete life cycle of a mesoscale (∼10-100 km) bloom of coccolithophores in the North Atlantic, from exponential growth to its rapid demise. We estimate the amount of organic carbon produced during the bloom to be in the order of 24,000 tons, of which two-thirds were turned over within 1 week. Complimentary in situ measurements of the same patch area revealed high levels of specific viruses infecting coccolithophore cells, therefore pointing at the importance of viral infection as a possible mortality agent. Application of the newly developed satellite-based approaches opens the way for large-scale quantification of the impact of diverse environmental stresses on the fate of phytoplankton blooms and derived carbon in the ocean.

A new alga-bacterium model system sheds light on mortality factors affecting phytoplankton bloom demise and sulfur cycling.

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The cosmopolitan coccolithophore Emiliania huxleyi is characterized by a strongly differentiated haplodiplontic life cycle consisting of a diploid phase, generally bearing coccoliths (calcified) but that can be also non-calcified, and a non-calcified biflagellated haploid phase. Given most studies have focused on the bloom-producing calcified phase, there is little-to-no information about non-calcified cells in nature. Using field mesocoms as experimental platforms, we quantitatively surveyed calcified and non-calcified cells using the combined calcareous detection fluorescent in situ hybridization (COD-FISH) method and qualitatively screened for haploid specific transcripts using reverse transcription-PCR during E. huxleyi bloom successions. Diploid, calcified cells formed dense blooms that were followed by the massive proliferation of E. huxleyi viruses (EhVs), which caused bloom demise. Non-calcified cells were also detected throughout the experiment, accounting for a minor fraction of the population but becoming progressively more abundant during mid-late bloom periods concomitant with EhV burst. Non-calcified cell growth also paralleled a distinct window of haploid-specific transcripts and the appearance of autotrophic flagellates morphologically similar to haploid cells, both of which are suggestive of meiosis and sexual life cycling during natural blooms of this prominent marine phytoplankton species.

Marine viruses that infect phytoplankton strongly influence the ecology and evolution of their hosts. Emiliania huxleyi is characterized by a biphasic life cycle composed of a diploid (2N) and haploid (1N) phase; diploid cells are susceptible to infection by specific coccolithoviruses, yet haploid cells are resistant. Glycosphingolipids (GSLs) play a role during infection, but their molecular distribution in haploid cells is unknown. We present mass spectrometric analyses of lipids from cultures of uninfected diploid, infected diploid, and uninfected haploid E. huxleyi. Known viral GSLs were present in the infected diploid cultures as expected, but surprisingly, trace amounts of viral GSLs were also detected in the uninfected haploid cells. Sialic-acid GSLs have been linked to viral susceptibility in diploid cells, but were found to be absent in the haploid cultures, suggesting a mechanism of haploid resistance to infection. Additional untargeted high-resolution mass spectrometry data processed via multivariate analysis unveiled a number of novel biomarkers of infected, non-infected, and haploid cells. These data expand our understanding on the dynamics of lipid metabolism during E. huxleyi host/virus interactions and highlight potential novel biomarkers for infection, susceptibility, and ploidy.