Proteome adaptation to high temperatures in the ectothermic hydrothermal vent Pompeii worm.

Didier Jollivet,Odile Lecompte,Nicolas Gagnière,Eric Fontanillas,Arnaud Tanguy,Béatrice Segurens,Jean Mary,Olivier Poch,Stéphane Hourdez,Jean Weissenbach,Isabelle Boutet

doi:10.1371/journal.pone.0031150

Abstract

Taking advantage of the massive genome sequencing effort made on thermophilic prokaryotes, thermal adaptation has been extensively studied by analysing amino acid replacements and codon usage in these unicellular organisms. In most cases, adaptation to thermophily is associated with greater residue hydrophobicity and more charged residues. Both of these characteristics are positively correlated with the optimal growth temperature of prokaryotes. In contrast, little information has been collected on the molecular ‘adaptive’ strategy of thermophilic eukaryotes. The Pompeii worm A. pompejana, whose transcriptome has recently been sequenced, is currently considered as the most thermotolerant eukaryote on Earth, withstanding the greatest thermal and chemical ranges known. We investigated the amino-acid composition bias of ribosomal proteins in the Pompeii worm when compared to other lophotrochozoans and checked for putative adaptive changes during the course of evolution using codon-based Maximum likelihood analyses. We then provided a comparative analysis of codon usage and amino-acid replacements from a greater set of orthologous genes between the Pompeii worm and Paralvinella grasslei, one of its closest relatives living in a much cooler habitat. Analyses reveal that both species display the same high GC-biased codon usage and amino-acid patterns favoring both positively-charged residues and protein hydrophobicity. These patterns may be indicative of an ancestral adaptation to the deep sea and/or thermophily. In addition, the Pompeii worm displays a set of amino-acid change patterns that may explain its greater thermotolerance, with a significant increase in Tyr, Lys and Ala against Val, Met and Gly. Present results indicate that, together with a high content in charged residues, greater proportion of smaller aliphatic residues, and especially alanine, may be a different path for metazoans to face relatively ‘high’ temperatures and thus a novelty in thermophilic metazoans.

Highlights

Adaptation to high temperatures is a complex evolutive process that can involve modifications of the intrinsic stability of proteins, and/or interactions with other proteins that stabilize or help the re-folding of the partner
Over the 8200 codons examined from ribosomal protein genes, amino-acid frequencies were almost the same among taxa with the noticeable exception of the nematod C. elegans and the polychaete A. pompejana
Thermal adaptation has been extensively studied in thermophilic microorganisms by analysing amino acid replacements and codon usage, taking advantage of the massive genome sequencing effort done on these specific prokaryotes [4,35]

Summary

Introduction

Adaptation to high temperatures is a complex evolutive process that can involve modifications of the intrinsic stability of proteins, and/or interactions with other proteins (e.g. chaperones) that stabilize or help the re-folding of the partner. Organisms that recently colonized hot environments evolved under a rather ‘‘key residue-based’’ mechanism of thermostability in which a few charged amino acids replacements or amino acid deletions favored hydrogen bonds and inter- and/or intra-subunit electrostatic interactions [9], decreased length of surface loops [10], or solely affected specific chaperones/structural proteins in order to improve their efficiency [11]. Because most thermophilic eukaryotes are only able to live at the lower thermal range of thermophilic bacteria (i.e. 40–60uC), the level of protein compactness and high GC genome content are probably less relevant. Such strategies may still hold depending on how ancestral the thermophilic character is and how severe the thermal selection is

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Conclusion