Open Access Research article

Insights into metazoan evolution from alvinella pompejana cDNAs

Nicolas Gagnière1, Didier Jollivet23, Isabelle Boutet23, Yann Brélivet1, Didier Busso1, Corinne Da Silva4, Françoise Gaill5, Dominique Higuet6, Stéphane Hourdez23, Bernard Knoops7, François Lallier23, Emmanuelle Leize-Wagner8, Jean Mary23, Dino Moras1, Emmanuel Perrodou1, Jean-François Rees7, Béatrice Segurens4, Bruce Shillito6, Arnaud Tanguy23, Jean-Claude Thierry1, Jean Weissenbach4, Patrick Wincker4, Franck Zal23, Olivier Poch1 and Odile Lecompte1*

Author Affiliations

1 Department of Structural Biology and Genomics, Institut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC), CERBM F-67400 Illkirch, France; INSERM, U596, F-67400 Illkirch, France; CNRS, UMR7104, F-67400 Illkirch, France; Faculté des Sciences de la Vie, Université de Strasbourg, F-67000 Strasbourg, France

2 CNRS, UMR 7144, Adaptation et Diversité en Milieu Marin, Station Biologique de Roscoff, 29682, Roscoff, France

3 UPMC Université Paris 6, Station Biologique de Roscoff, 29682, Roscoff, France

4 Genoscope - Centre National de Séquençage, 2 rue Gaston Crémieux CP5706 91057 Evry cedex, France

5 CNRS Institut Ecologie et Environnement (INEE), 3 rue Michel-Ange, 75794, Paris cedex 16, France

6 UPMC Université Paris 6, UMR 7138, Systématique, Adaptation et Evolution, Campus de Jussieu, 75005 Paris, France

7 Université Catholique de Louvain, Laboratoire de Biologie Cellulaire, Institut des Sciences de la vie, Croix du sud 5, B-1348, Louvain-la-neuve, Belgium

8 UMR 7177 CNRS-UDS, LDSM2 Institut de Chimie de Strasbourg, 1 rue Blaise Pascal -BP 296 R8, 67008 Strasbourg cedex, France

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BMC Genomics 2010, 11:634  doi:10.1186/1471-2164-11-634

Published: 16 November 2010

Abstract

Background

Alvinella pompejana is a representative of Annelids, a key phylum for evo-devo studies that is still poorly studied at the sequence level. A. pompejana inhabits deep-sea hydrothermal vents and is currently known as one of the most thermotolerant Eukaryotes in marine environments, withstanding the largest known chemical and thermal ranges (from 5 to 105°C). This tube-dwelling worm forms dense colonies on the surface of hydrothermal chimneys and can withstand long periods of hypo/anoxia and long phases of exposure to hydrogen sulphides. A. pompejana specifically inhabits chimney walls of hydrothermal vents on the East Pacific Rise. To survive, Alvinella has developed numerous adaptations at the physiological and molecular levels, such as an increase in the thermostability of proteins and protein complexes. It represents an outstanding model organism for studying adaptation to harsh physicochemical conditions and for isolating stable macromolecules resistant to high temperatures.

Results

We have constructed four full length enriched cDNA libraries to investigate the biology and evolution of this intriguing animal. Analysis of more than 75,000 high quality reads led to the identification of 15,858 transcripts and 9,221 putative protein sequences. Our annotation reveals a good coverage of most animal pathways and networks with a prevalence of transcripts involved in oxidative stress resistance, detoxification, anti-bacterial defence, and heat shock protection. Alvinella proteins seem to show a slow evolutionary rate and a higher similarity with proteins from Vertebrates compared to proteins from Arthropods or Nematodes. Their composition shows enrichment in positively charged amino acids that might contribute to their thermostability. The gene content of Alvinella reveals that an important pool of genes previously considered to be specific to Deuterostomes were in fact already present in the last common ancestor of the Bilaterian animals, but have been secondarily lost in model invertebrates. This pool is enriched in glycoproteins that play a key role in intercellular communication, hormonal regulation and immunity.

Conclusions

Our study starts to unravel the gene content and sequence evolution of a deep-sea annelid, revealing key features in eukaryote adaptation to extreme environmental conditions and highlighting the proximity of Annelids and Vertebrates.