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

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

*Corresponding author for this work

Research output: Contribution to journalArticle (Academic Journal)peer-review

204 Citations (Scopus)

Abstract

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.

Original languageEnglish
Pages (from-to)5247-5252
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume110
Issue number13
DOIs
Publication statusPublished - 26 Mar 2013

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