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Open Access Research article

Horizontal gene transfer of a chloroplast DnaJ-Fer protein to Thaumarchaeota and the evolutionary history of the DnaK chaperone system in Archaea

Céline Petitjean12, David Moreira2, Purificación López-García2 and Céline Brochier-Armanet3*

Author affiliations

1 UPR CNRS 9043, Laboratoire de Chimie Bactérienne, Université d’Aix-Marseille (AMU), 13402 Marseille, Cedex 20, France

2 UMR CNRS 8079, Unité d'Ecologie, Systématique et Evolution Université Paris-Sud, 91405 Orsay, Cedex, France

3 CNRS, UMR5558, Laboratoire de Biométrie et Biologie Evolutive, Université de Lyon, Université Lyon 1, 43 boulevard du 11 novembre 1918, 69622, Villeurbanne, France

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Citation and License

BMC Evolutionary Biology 2012, 12:226  doi:10.1186/1471-2148-12-226

Published: 26 November 2012

Abstract

Background

In 2004, we discovered an atypical protein in metagenomic data from marine thaumarchaeotal species. This protein, referred as DnaJ-Fer, is composed of a J domain fused to a Ferredoxin (Fer) domain. Surprisingly, the same protein was also found in Viridiplantae (green algae and land plants). Because J domain-containing proteins are known to interact with the major chaperone DnaK/Hsp70, this suggested that a DnaK protein was present in Thaumarchaeota. DnaK/Hsp70, its co-chaperone DnaJ and the nucleotide exchange factor GrpE are involved, among others, in heat shocks and heavy metal cellular stress responses.

Results

Using phylogenomic approaches we have investigated the evolutionary history of the DnaJ-Fer protein and of interacting proteins DnaK, DnaJ and GrpE in Thaumarchaeota. These proteins have very complex histories, involving several inter-domain horizontal gene transfers (HGTs) to explain the contemporary distribution of these proteins in archaea. These transfers include one from Cyanobacteria to Viridiplantae and one from Viridiplantae to Thaumarchaeota for the DnaJ-Fer protein, as well as independent HGTs from Bacteria to mesophilic archaea for the DnaK/DnaJ/GrpE system, followed by HGTs among mesophilic and thermophilic archaea.

Conclusions

We highlight the chimerical origin of the set of proteins DnaK, DnaJ, GrpE and DnaJ-Fer in Thaumarchaeota and suggest that the HGT of these proteins has played an important role in the adaptation of several archaeal groups to mesophilic and thermophilic environments from hyperthermophilic ancestors. Finally, the evolutionary history of DnaJ-Fer provides information useful for the relative dating of the diversification of Archaeplastida and Thaumarchaeota.

Keywords:
DnaJ/Hsp40; DnaK/Hsp70; Hyperthermophily; Archaeplastida; Phylogeny; Archaea; Thaumarchaeota; Horizontal gene transfer; Mesophily