Genomic Adaptations of Marine Algae to Viruses – ALGALVIRUS

Aquatic microalgae contribute about a half of global primary production, with picoeukaryotes contributing the greatest fraction (49-69%). The diversity of unicellular eukaryotes is currently a subject of intense investigations, but the class Mamiellophyceae (genera Micromonas, Bathycoccus, Ostreococcus, Mantoniella, Mamiella, Crustomastix, Dolichomastix and Monomastix, all Chlorophyta) is especially important in marine environments, Monomastix having the only known freshwater representatives. Three main picoeukaryotic groups in the Mamiellophyceae, Micromonas pusilla, Bathycoccus prasinos and Ostreococcus spp. are distributed throughout the Earth's oceans, different species within each group being well adapted to thrive in different environments (polar, temperate, tropical, high or low nutrients). These genera represent complexes of cryptic species, because their small size hinders definition of morphological differences, and the 18S ribosomal gene, a classical phylogenetic marker, is inadequate for describing their diversity. Increasing levels of eutrophication (for example along coastlines), or higher levels of CO2, promote higher population densities in this group of algae and long-term exposure to higher CO2 might also affect the long-term ability for adaptation to climatic variations in the Mamiellales. Their population densities are also controlled partly by the huge diversity of viruses that infest them.
Prasinoviruses are not only the most abundant large DNA viruses in our oceans, but are also numerous in freshwater lakes and rivers. In marine ecosystems we know that algae of the Mamiellophyceae are the main hosts of prasinoviruses, and our laboratory has contributed largely to the analysis of both host and viral genomes. All of the six characterized small streamlined genomes of these haplont phylogenetically divergent species of Mamiellales have a similar structure, carrying about twenty chromosomes, including two "outlier" chromosomes that differ in their composition from the 18 "autosomal" chromosomes in several ways: - a lower GC content, a higher number of genes predicted to encode transposons and genes originating from horizontal gene transfer. We refer to these two chromosomes as the big and small outlier chromosomes (BOC and SOC). In laboratory cultures, we showed previously that spontaneous resistance to prasinoviruses arises frequently, and we now know that a specific set of genes that are clustered together on the outlier chromosome (SOC), is induced in virus-resistant strains.
The three main objectives of this proposal are to characterise the molecular mechanisms of host resistance to prasinoviruses, to understand the evolutionary processes that led to this unusual and tiny genome structure present in this group of algae, which seems to be adapted to their co-evolution with omnipresent prasinoviruses and to use these data to analyze the distribution of the Mamiellophyceae in environmental samples (metagenomic data). Here, we will compare the structure of the SOC in lines of Ostreococcus tauri either susceptible or resistant to viral infection, by looking for changes in (1) the non-coding RNA landscape (2) DNA methylation (3) chromatin structure, and (4) investigating the roles of specific genes in host-virus interactions. In parallel, we will sequence and annotate the complete and larger genomes of representative ancestral algae to elucidate the evolution of these unusual chromosomes. These new genomes will not only provide insight about host-virus interactions, but will enable the development of tools for exploring the wealth of metagenomic environmental DNA sequence data available and for elucidating gene functions that act at the base of the global food web in our oceans.