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

Jonas Collén (1, 2) , Betina Porcel (3, 4) , Wilfrid Carré (5) , Steven G Ball (6) , Cristian Chaparro (7) , Thierry Tonon (1, 2) , Tristan Barbeyron (1, 2) , Gurvan Michel (1, 2) , Benjamin Noel (4) , Klaus Valentin (8) , Marek Elias (9) , François Artiguenave (4) , Alok Arun (1, 2) , Jean-Marc Aury (4) , José F Barbosa-Neto (7) , John H Bothwell (10) , François-Yves Bouget (11) , Loraine Brillet (5) , Francisco Cabello-Hurtado (12) , Salvador Capella-Gutiérrez (13, 14) , Bénédicte Charrier (1, 2) , Lionel Cladière (1, 2) , J Mark Cock (1, 2) , Susana M Coelho (1, 2) , Christophe Colleoni (6) , Mirjam Czjzek (1, 2) , Corinne da Silva (4, 15) , Ludovic Delage (1, 2) , France Denoeud (4) , Philippe Deschamps (6) , Simon M Dittami (16, 1) , Toni Gabaldón (17, 13) , Claire M M Gachon (18) , Agnès Groisillier (1, 2) , Cécile Hervé (1, 2) , Kamel Jabbari (4, 19) , Michael Katinka (4) , Bernard Kloareg (1, 2) , Nathalie Kowalczyk (1, 2) , Karine Labadie (4) , Catherine Leblanc (1, 2) , Pascal J Lopez (20) , Deirdre H Mclachlan (10) , Laurence Meslet-Cladiere (1, 21, 2) , Ahmed Moustafa (22) , Zofia Nehr (1, 2) , Pi Nyvall Collén (1, 2) , Olivier Panaud (7) , Frédéric Partensky (2) , Julie Poulain (15) , Stefan A Rensing (23) , Sylvie Rousvoal (16) , Gaelle Samson (15) , Aikaterini Symeonidi (24) , Jean Weissenbach (15) , Antonios Zambounis (25) , Patrick Wincker (26) , Catherine Boyen (1, 2)

1 Végétaux marins et biomolécules
2 MAPP - MArine Phototrophic Prokaryotes
3 Commissariat à l'Energie Atomique
4 UMR 8030 - Génomique métabolique
5 SBR - Station biologique de Roscoff [Roscoff]
6 UGSF - Unité de Glycobiologie Structurale et Fonctionnelle UMR 8576
7 LGDP - Laboratoire Génome et développement des plantes
8 AWI - Alfred-Wegener-Institut, Helmholtz-Zentrum für Polar- und Meeresforschung
9 Department of Plant Physiology, Faculty of Sciences
10 BESC - Belfast e-Science Centre [Belfast]
11 LOMIC - Laboratoire d'Océanographie Microbienne
12 ECOBIO - Ecosystèmes, biodiversité, évolution [Rennes]
13 UPF - Universitat Pompeu Fabra [Barcelona]
14 CRG-UPF - Center for Genomic Regulation
15 GENOSCOPE - Genoscope - Centre national de séquençage [Evry]
16 LBI2M - Laboratoire de Biologie Intégrative des Modèles Marins
17 Bioinformatics and Genomics Programme
18 SAMS - Scottish Association for Marine Science
19 IBENS - Institut de biologie de l'ENS Paris
20 BOREA - Biologie des Organismes et Ecosystèmes Aquatiques
21 LEMAR - Laboratoire des Sciences de l'Environnement Marin (LEMAR)
22 Department of Biology and Biotechnology Graduate Program, American University in Cairo
23 University of Freiburg [Freiburg]
24 Freiburg Initiative in Systems Biology
25 CERTH - Centre for Research and Technology Hellas
26 IG - Institut de Génomique d'Evry

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.

Domains: Life Sciences [q-bio]

Jonas Collén, Betina Porcel, Wilfrid Carré, Steven G Ball, Cristian Chaparro, et al.. Genome structure and metabolic features in the red seaweed Chondrus crispus shed light on evolution of the Archaeplastida.. Proceedings of the National Academy of Sciences of the United States of America, 2013, 110 (13), pp.5247-52. ⟨10.1073/pnas.1221259110⟩. ⟨hal-01073830⟩