Insights into metazoan evolution from alvinella pompejana cDNAs

Nicolas Gagnière,Emmanuel Perrodou,Olivier Poch,Dominique Higuet,Jean Weissenbach,Jean Mary,Yann Brélivet,Corinne Da Silva,Odile Lecompte,Bruce Shillito,Bernard Knoops,Isabelle Boutet,Didier Busso,Françoise Gaill,Jean-François Rees,Arnaud Tanguy,Didier Jollivet,Dino Moras,Patrick Wincker,Franck Zal,Stéphane Hourdez,Jean‐Claude Thierry ,Emmanuelle Leize‐Wagner ,François H Lallier ,Béatrice Ségurens

doi:10.1186/1471-2164-11-634

Abstract

BackgroundAlvinella 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.ResultsWe 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.ConclusionsOur 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.

Highlights

Alvinella pompejana is a representative of Annelids, a key phylum for evo-devo studies that is still poorly studied at the sequence level
The construction and sequencing of four non normalized cDNA libraries from A. pompejana, one of the most thermotolerant eukaryotes known to date, resulted in 15,858 unique cDNA sequences and 9,221 annotated protein sequences
As indicated by the pathways and interaction networks mapped, our cDNA libraries provided a good coverage of the A. pompejana gene repertoire

Summary

Introduction

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. Fossil records [3], as well as comparative morphology studies [4], suggested that the urbilaterian (the last common ancestor of bilateral symmetric animals) may have resembled annelids Such an assumption is difficult to verify, it is widely accepted that polychaetes exhibit many ancestral traits in their body plan and embryonic development [5]. The genome of a bilaterian sister group, the cnidarian sea anemone Nematostella vectensis, has proved to be more complex than expected, with a gene repertoire, exon-intron structure, and large-scale gene linkage more similar to vertebrates than to flies or nematodes [8]

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