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

2013; National Academy of Sciences; Volume: 110; Issue: 13 Linguagem: Inglês

10.1073/pnas.1221259110

1091-6490

Jonas Collén, Betina M. Porcel, Wilfrid Carré, Steven Ball, Cristian Chaparro, Thierry Tonon, Tristan Barbeyron, Gurvan Michel, Benjamin Noël, Klaus-Ulrich Valentin, Marek Eliáš, François Artiguenave, Alok Arun, Jean‐Marc Aury, José Fernandes Barbosa-Neto, John H. Bothwell, François‐Yves Bouget, Loraine Brillet, Francisco Cabello‐Hurtado, Salvador Capella-Gutiérrez, Bénédicte Charrier, Lionel Cladière, J. Mark Cock, Susana M. Coelho, Christophe Colleoni, Mirjam Czjzek, Corinne Da Silva, Ludovic Delage, France Denœud, Philippe Deschamps, Simon M. Dittami, Toni Gabaldón, Claire M. M. Gachon, Agnès Groisillier, Cécile Hervé, Kamel Jabbari, Michaël Katinka, Bernard Kloareg, Nathalie Kowalczyk, Karine Labadie, Catherine Leblanc, Pascal Jean Lopez, Deirdre H. McLachlan, Laurence Meslet‐Cladiére, Ahmed Moustafa, Zofia Nehr, Pi Nyvall Collén, Olivier Panaud, Frédéric Partensky, Julie Poulain, Stefan A. Rensing, Sylvie Rousvoal, Gaëlle Samson, Aikaterini Symeonidi, Jean Weissenbach, Antonios Zambounis, Patrick Wincker, Catherine Boyen,

Microbial Community Ecology and Physiology

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.