Red seaweeds are key components of coastal ecosystems and are economically important as food and as a source of gelling agents, but their genes and genomes have received little attention. Here we report the sequencing of the 105-Mbp genome of the florideophyte Chondrus crispus (Irish moss) and the annotation of the 9,606 genes. The genome features an unusual structure characterized by gene-dense regions surrounded by repeat-rich regions dominated by transposable elements. Despite its fairly large size, this genome shows features typical of compact genomes, e.g., on average only 0.3 introns per gene, short introns, low median distance between genes, small gene families, and no indication of large-scale genome duplication. The genome also gives insights into the metabolism of marine red algae and adaptations to the marine environment, including genes related to halogen metabolism, oxylipins, and multicellularity (microRNA processing and transcription factors). Particularly interesting are features related to carbohydrate metabolism, which include a minimalistic gene set for starch biosynthesis, the presence of cellulose synthases acquired before the primary endosymbiosis showing the polyphyly of cellulose synthesis in Archaeplastida, and cellulases absent in terrestrial plants as well as the occurrence of a mannosylglycerate synthase potentially originating from a marine bacterium. To explain the observations on genome structure and gene content, we propose an evolutionary scenario involving an ancestral red alga that was driven by early ecological forces to lose genes, introns, and intergenetic DNA; this loss was followed by an expansion of genome size as a consequence of activity of transposable elements.T he red algae, together with the glaucophytes and the Chloroplastida, are members of the Archaeplastida, the phylogenetic group formed during the primary endosymbiosis event that gave rise to the first photosynthetic eukaryote. Red algal genomes, both plastid and nuclear, also contributed, via secondary endosymbiosis, to several other eukaryotic lineages, including

Culture-independent molecular analyses of open-sea microorganisms have revealed the existence and apparent abundance of novel eukaryotic lineages, opening new avenues for phylogenetic, evolutionary, and ecological research. Novel marine stramenopiles, identified by 18S ribosomal DNA sequences within the basal part of the stramenopile radiation but unrelated to any previously known group, constituted one of the most important novel lineages in these open-sea samples. Here we carry out a comparative analysis of novel stramenopiles, including new sequences from coastal genetic libraries presented here and sequences from recent reports from the open ocean and marine anoxic sites. Novel stramenopiles were found in all major habitats, generally accounting for a significant proportion of clones in genetic libraries. Phylogenetic analyses indicated the existence of 12 independent clusters. Some of these were restricted to anoxic or deep-sea environments, but the majority were typical components of coastal and open-sea waters. We specifically identified four clusters that were well represented in most marine surface waters (together they accounted for 74% of the novel stramenopile clones) and are the obvious targets for future research. Many sequences were retrieved from geographically distant regions, indicating that some organisms were cosmopolitan. Our study expands our knowledge on the phylogenetic diversity and distribution of novel marine stramenopiles and confirms that they are fundamental members of the marine eukaryotic picoplankton.Genetic libraries of small subunit (SSU) ribosomal DNA (rDNA) genes constructed from environmental DNA have proven very valuable to study the taxonomic composition of marine prokaryotic plankton (8,16). Prokaryotic assemblages in the sea appeared to be dominated by novel bacterial and archaeal lineages (17), and this was an important breakthrough for understanding the structure and function of natural assemblages (37). Picoeukaryotes (eukaryotic microbes less than 2 to 3 m in diameter) are also recognized as fundamental components of marine ecosystems. Phototrophic picoeukaryotes contribute significantly to phytoplankton biomass and primary production (26), and heterotrophic picoeukaryotes, generally small flagellates (5), are the main grazers of bacteria and play key roles within the microbial food web (41). Despite the ecological importance of marine picoeukaryotes, the use of molecular tools to investigate their taxonomic composition, in particular by 18S rDNA libraries, is very recent (9, 28, 34). The most remarkable finding of these studies was the recovery of novel lineages within the stramenopile and alveolate phylogenetic divisions that accounted for a significant fraction of clones in the libraries. These novel lineages represent organisms that must contribute to marine processes but have not been investigated before and thus deserve further detailed phylogenetic and ecological studies.The stramenopiles (Heterokonta) form one of the eight major phylogenetic groups of eukaryo...