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Historical and current pHytoplankton interactions with viruses: Emiliania huxleyi case study

Final Report Summary - HI PH-IVE (Historical and current pHytoplankton interactions with viruses: Emiliania huxleyi case study.)

The major problem of the global ecology is the abrupt increase of carbon dioxide (CO2) concentration in Earth's atmosphere. As one of the most critical effects of burning fossil carbon by human action is the rapid acidification of the oceans. Indeed the CO2 diffuses into the surface layers of the global ocean, including causing a significant decrease in pH and carbonate ion (CO3-). These acidic conditions make biomineralization of calcareous shell increasingly difficult, threatening biodiversity with extinction of calcifying plankton ecosystems, with all the brutal feedback effects on regional and global climate. In particular, coccolithophores, haptophytes microalgae covered with small calcareous scales occur today ~30% of pelagic carbonates, a central process of the carbon cycle between the different compartments of the biosphere. How will coccolithophores react to abrupt climate changes? More our understanding of how biodiversity will respond to abrupt climate changes is limited by a fundamental lack of understanding of eukaryotic ocean biodiversity, and rates of biodiversity change. This project aims to understand the complexity and rate of adaptation in Emiliania huxleyi, a dominant coccolithophore in modern oceans, through the study of its ecological distribution and genetic diversity in space and time in this Hi pH-IVE project.

To achieve its objectives, the Hi pH-IVE project has produced significant research results of high quality and subsequently published them in top international conferences and journals:

- Establishment of a reference alignment for metagenomic approach for the relevant coccolithophores species Emiliania huxleyi and closely related species (Bendif et al. 2014), this study aimed to develop genetic markers to study the microdiversity on the key coccolithophore species E. huxleyi and Gephyrocapsa oceanica. This is the first study describing the microdiversity between and within these two closely related species.

- Highlighting an unsuspected evolutionary process involved in the evolution of these cosmopolitan phytoplankton species intimately controlled by environmental features, especially temperature. This study led to reconsider the species concept of the studied group as a broaden complex of population with different level of reproductive isolation instead of considering the different morphological species as strict biological species (Bendif et al 2015). This study will have a strong impact on our understanding of adaptability within the different populations/species by partial gene-flow between distant populations and future assessment of their biodiversity.

- A global survey of potential correlations between the phylogenetic structure of E. huxleyi and genomic content of culture strains led to the discovery of the loss of genes related to sexual reproduction in numerous culture strains of this species; with a partial correlation with phylogeny and complete correlation with biogeographic origin (coastal vs open ocean strains) and viral population distribution. This study highlighted the first evidence of genome erosion in eukaryotic phytoplankton within a specific phytoplankton complex. We believe that this micro-evolutionary process has important implications for future adaptation to climate change in phytoplankton (von Dassow et al. 2014). The study demonstrated how viruses are fundamentally associated with E. huxleyi life history, regulating population dynamics, representing a significant biotic stress factor, paradoxically as a positive pressure in enhancing and selecting phytoplankton adaptability and consequently biodiversity. Whereas, escape from viral pressure is leading to a negative effect on reproductive functions at a genomic level, by swaping irreversibly sex related genes and reducing significantly adaptability.

- Establishment of a wide exome library based on transcriptome, this library will be of use for future metagenomic survey of the Gephyrocapsa. This library is held at the Station Biologique de Roscoff (ABYSS-rmetat project, with Dr de Vargas).

- The global monitoring of worldwide isolates coupled with environmental data (Illumina metabarcodes) provided a robust framework for developing an ecological modeling of molecular diversity and related temperature niche adaptation within the Gephyrocapsas. These fundamental results will lead to the first global study correlating a multi-gene barcode approach to genomic and metabarcoding data in an environmental context for a cosmopolitan phytoplankton assemblage. These results will allow a refinement on our prediction of the effect of climate change on phytoplankton, as the developed models coupled with von Dassow et al. (2014) data are allowing us to study past and to predict future evolution of the group in the actual context of global warming. The significance of these results led to prepare a manuscript that would be valorized in a multidisciplinary journal with potential for a very high impact contribution (Bendif et al, in prep).

- Establishment of a plastidial 16S rRNA database (PhytoRef) for exploring phytoplankton communities using metabarcoding approach (Decelle et al 2015).
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