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MBE Advance Access first published online on August 4, 2006
This version published online on September 6, 2006
Molecular Biology and Evolution, doi:10.1093/molbev/msl082
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© 2006 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.
Accepted August 1, 2006

Research Article

Impact of the Excision of an Ancient Repeat Insertion on Rickettsia conorii Guanylate Kinase Activity

Chantal Abergel 1 *, Guillaume Blanc 1, Vincent Monchois 2, Patricia Renesto-Audiffren 3, Cécile Sigoillot 1, Hiroyuki Ogata 1, Didier Raoult 3, and Jean-Michel Claverie 1

1 Information Génomique & Structurale, CNRS UPR 2589, IBSM, Parc scientifique de Luminy, 163 Avenue de Luminy, 13288 Marseille Cedex 9, France
2 Information Génomique & Structurale, CNRS UPR 2589, IBSM, Parc scientifique de Luminy, 163 Avenue de Luminy, 13288 Marseille Cedex 9, France; Present address : Protein'eXpert SA., 15 rue des martyrs, 38000 Grenoble, FRANCE
3 Unité des Rickettsies, Université de la Méditerranée, Faculté de Médecine, CNRS UMR 6020, IFR 48, 27 boulevard Jean Moulin, 13385 Marseille Cedex 05, France

* To whom correspondence should be addressed.
Chantal Abergel, E-mail: Chantal.Abergel{at}igs.cnrs-mrs.fr


  Abstract

The genomic sequencing of Rickettsia conorii revealed a new family of Rickettsia-specific palindromic elements (RPE) capable of in-frame insertion in pre-existing ORFs. Many of these altered ORFs correspond to proteins with well characterized or essential functions in other micro-organisms. Previous experiments indicated that RPE-containing genes are normally transcribed and that no excision of the repeat occurs at the mRNA level. Using mass spectrometry, we now confirmed the retention of the RPE-derived amino-acid residues in four proteins successfully expressed in E. coli, raising the general question of the consequences of this common insertion event on the fitness of Rickettsia enzymes. The predicted guanylate kinase activity of the R. conorii gmk gene product was measured both on the RPE-containing and RPE excised recombinant proteins. We show that the two proteins are active but exhibits substantial differences in their affinity for ATP, GMP and catalytic constants. The distribution of the RPEgmk insert among Rickettsia species indicates that the insertion event is ancient and occurred after the divergence of R. felis and R. conorii but before that of R. helvetica and R. conorii. We found no evidence that the gmk gene fixed adaptive changes to compensate the RPE peptide insertion. Furthermore, the analysis of the rates of divergence in 23 RPE-containing genes indicates that coding RPE repeats tend to evolve under weak selective constraint, at a rate similar to intergenic non coding RPE sequences. All together, these results suggest that the insertion of RPE-encoded "selfish peptides", although respecting the original fold and activity of the host proteins, might be slightly detrimental to the enzyme efficiency within limits tolerable for slow growing intracellular parasites such as Rickettsia.

Keywords: Rickettsia conorii; palindromic coding repeat; guanylate kinase; enzyme fitness; recombinant protein expression.
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