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MBE Advance Access published online on June 25, 2008
Molecular Biology and Evolution, doi:10.1093/molbev/msn142
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© 2008 The Authors.
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.0/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Research Article

An assessment of the impacts of molecular oxygen on the evolution of proteomes

Sara Vieira-Silva1,2 and Eduardo P. C. Rocha1,2

1 UPMC Univ Paris 06, Atelier de BioInformatique, F-75005, Paris, France
2 Institut Pasteur, Microbial Evolutionary Genomics; CNRS, URA2171, F-75015 Paris, France

Corresponding author: Sara Vieira-Silva, Atelier de Bioinformatique, Univ. Pierre et Marie Curie-Paris6, RdC Aile C - Maison Pédagogie, Boite courrier 1202, 4 Pl Jussieu, 75005 Paris. telephone number: +33 1 44 27 63 71. fax number: +33 1 44 27 63 12. e-mail: sara{at}abi.snv.jussieu.fr

Received for publication May 5, 2008. Revision received June 19, 2008. Accepted for publication June 19, 2008.

Oxygen is one of life's essential elements, but also a source of protein damage, mutagenesis and ageing. Many proteome adaptations have been proposed to tackle such stresses and we assessed them using comparative genomics in a phylogenetic context. Firstly, we find that aerobiosis is a trait with important phylogenetic inertia, but that oxygen content in proteins isn't. Instead, oxygen content is close to the expected values given nucleotide composition. Accordingly, we find no evidence of oxygen being a scarce resource for protein synthesis even among anaerobes. Secondly, we searched for counter-selection of amino acids more prone to oxidation among aerobes. Only cysteine follows the expected trend while triptophan follows the inverse one. When analyzing composition in the context of protein structures and residue accessibility we find that all oxidable residues are avoided at the surface of proteins. Yet, there is no difference between aerobes and anaerobes in this respect and the effect might be explained by the hydrophobicity of these residues. Thirdly, we revisited the hypothesis that atmospheric enrichment in molecular oxygen led to the development of the communication capabilities of eukaryotes. With a larger dataset and adequate controls, we confirm the trend of longer oxygen-rich outer domains in transmembrane proteins of eukaryotes. Yet, we find no significant association between oxygen concentration in the environment and this trait within prokaryotes, suggesting that this difference is clade-specific and independent of oxygen availability. We find that genes involved in cellular responses to oxygen are much more frequent among aerobes and we suggest that they erase most expected differences in terms of proteome composition between organisms facing high and low oxygen concentrations.

Key Words: oxidative stress • cysteine • protein evolution • hydrophobicity • evolution


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