Journal Article

Genome structure and metabolic features in the red seaweed Chondrus crispus shed light on evolution of the Archaeplastida

Adaptation et diversité en milieu marin (AD2M), Gachon, Claire M M, Denoeud, France, Universitat Pompeu Fabra (UPF), Chaparro, Cristian, Tonon, Thierry, Biologie des Organismes et Ecosystèmes Aquatiques (BOREA), Kloareg, Bernard, Observatoire océanologique de Banyuls (OOB), Symeonidi, Aikaterini, Wincker, Patrick, Charrier, Bénédicte, Laboratoire Génome et développement des plantes (LGDP), Barbosa-Neto, José F, Dittami, Simon M, Delage, Ludovic, Département de Biologie - ENS-PSL (IBENS), Collén, Jonas, Porcel, Betina, Lopez, Pascal-Jean, Elias, Marek, Samson, Gaelle, Boyen, Catherine, Labadie, Karine, Jabbari, Kamel, Ball, Steven G, Valentin, Klaus, Cladière, Lionel, Gabaldón, Toni, Weissenbach, Jean, Nyvall Collén, Pi, Panaud, Olivier, Artiguenave, François, Cabello-Hurtado, Francisco, Meslet-Cladiere, Laurence, Rousvoal, Sylvie, Génomique métabolique (UMR 8030), Laboratoire de Biologie Intégrative des Modèles Marins (LBI2M), Leblanc, Catherine, Colleoni, Christophe, Procaryotes Phototrophes Marins = MArine Phototrophic Prokaryotes (MAPP), Cock, J Mark, Bouget, Franç

2013

Overview

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.

• Publisher: National Academy of Sciences,CCSD,National Acad Sciences
• Subject: Algae / bacteria / Base Sequence / Biological Sciences / Biosynthesis / carbohydrate metabolism / cellulases / Cellulose / cellulose synthase / Chondrus / Chondrus - genetics / Chondrus crispus / Coastal ecosystems / Deoxyribonucleic acid / DNA / Economic importance / ecosystems / Enzymes / Eukaryotic cells / Evolution / Evolution, Molecular / gelling agents / Genes / Genes, Plant / Genomes / Genomics / Introns / Life Sciences / macroalgae / Marine environment / Metabolism / microRNA / MicroRNAs / MicroRNAs - genetics / Molecular Sequence Data / mosses and liverworts / oxylipins / Plant Proteins / Plant Proteins - genetics / Plants / polyphyly / Red algae / Ribonucleic acid / RNA / RNA, Plant / RNA, Plant - genetics / starch / symbiosis / transcription (genetics) / transcription factors / transposons