The ‘Cheshir Cat’ escape strategy of the coccolithophore Emiliania huxleyi in response to viral infection

Equipe EPPO-Evolution du Plancton et PaléoOcéans, Centre National de la Recherche Scientifique et Université Pierre et Marie Curie (Unité Mixte de Recherche 7144), Station Biologique, 29682 Roscoff, France.
Proceedings of the National Academy of Sciences (Impact Factor: 9.67). 10/2008; 105(41):15944-9. DOI: 10.1073/pnas.0807707105
Source: PubMed


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.

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    • "theobservationsofFradaetal.(2012)fromthesamemesocosms showingthat1Ncellsbecameproportionallymoreabundant,an affirmationoftheCheshireCathypothesis(Fradaetal.,2008). AlthoughthedynamicsofsGSLsubjecttoEhVinfectionappear variablebetween2Nsystems(Fultonetal.,2014),thediscovery herethatsGSLisabsentin1NE.huxleyicellscouldmakesGSL anevenmoreimportantbiomarkerforviralinfectiondynamics andassociatedshiftsinploidy. "
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    ABSTRACT: 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.
    11/2015; 2. DOI:10.3389/fmars.2015.00081
    • "This theory is apparently well supported by a large and phylogenetically diverse group of heteromorphic organisms where haploids and diploids exhibit marked morphological divergence together with clear ecological differences. For instance, ecological differences between a resting stage resistant to biotic or abiotic stress and a fast-growing stage have been recorded for haploid– diploid yeasts (e.g., Coluccio et al. 2008), coccolithophores (e.g., Frada et al. 2008), brown algae (e.g., Carney and Edwards 2006), and red algae (e.g., Vergés et al. 2008). However, empirical evidence is much more limited for many other organisms exhibiting isomorphic, haploid–diploid life cycles such as brown, red, and green seaweeds. "
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    ABSTRACT: The evolutionary stability of haploid-diploid life cycles is still controversial. Mathematical models indicate that niche differences between ploidy phases may be a necessary condition for the evolution and maintenance of these life cycles. Nevertheless, experimental support for this prediction remains elusive. In the present work, we explored this hypothesis in natural populations of the brown alga Ectocarpus. Consistent with the life cycle described in culture, E. crouaniorum in NW France and E. siliculosus in SW Italy exhibited an alternation between haploid gametophytes and diploid sporophytes. Our field data invalidated, however, the long-standing view of an isomorphic alternation of generations. Gametophytes and sporophytes displayed marked differences in size and, conforming to theoretical predictions, occupied different spatio-temporal niches. Gametophytes were found almost exclusively on the alga Scytosiphon lomentaria during spring while sporophytes were present year-round on abiotic substrata. Paradoxically, E. siliculosus in NW France exhibited similar habitat usage despite the absence of alternation of ploidy phases. Diploid sporophytes grew both epilithically and epiphytically, and this mainly-asexual population gained the same ecological advantage postulated for haploid-diploid populations. Consequently, an ecological interpretation of the niche differences between haploid and diploid individuals does not seem to satisfactorily explain the evolution of the Ectocarpus life cycle. This article is protected by copyright. All rights reserved. This article is protected by copyright. All rights reserved.
    Evolution 06/2015; 69(7). DOI:10.1111/evo.12702 · 4.61 Impact Factor
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    • "Some of these genes have potential implications for the infection strategy of these viruses and/or relate to their host's defence system (Monier et al., 2009; Pagarete et al., 2009; Vardi et al., 2009, 2012). At an ecological level we observe how the selection pressure imposed by these viruses is potentially linked to profound somatic consequences in E. huxleyi's life cycle, namely the alternation between diploid and haploid phases as a key mechanism to evade infection (Frada et al., 2008). Host–virus interaction analyses have commonly reported established phenomena where there is a significant decrease in EhV major capsid protein (MCP) diversity during the progression of bloom events (Martínez Martínez et al., 2007; Schroeder et al., 2003). "
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    ABSTRACT: Despite the global oceanic distribution and recognized biogeochemical impact of coccolithoviruses (EhV), their diversity remains poorly understood. Here we employed a metagenomic approach to study the occurrence and progression of natural EhV community genomic variability. Analysis of EhV metagenomes from the early and late stages of an induced bloom led to three main discoveries. First, we observed resilient and specific genomic signatures in the EhV community associated with the Norwegian coast, which reinforce the existence of limitations to the capacity of dispersal and genomic exchange among EhV populations. Second, we identified a hyper-variable region (approximately 21 kbp long) in the coccolithovirus genome. Third, we observed a clear trend for EhV relative amino-acid diversity to reduce from early to late stages of the bloom. This study validated two new methodological combinations, and proved very useful in the discovery of new genomic features associated with coccolithovirus natural communities.
    Virology 10/2014; in press. DOI:10.1016/j.virol.2014.05.020 · 3.32 Impact Factor
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