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MBE Advance Access published online on June 17, 2008
Molecular Biology and Evolution, doi:10.1093/molbev/msn134
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© The Authors 2008
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

Intense transpositional activity of insertion sequences in an ancient obligate endosymbiont

Richard Cordaux1,*, Samuel Pichon1, Alison Ling1, Philippe Pérez1, Carine Delaunay1, Fabrice Vavre2, Didier Bouchon1 and Pierre Grève1

1 Université de Poitiers, CNRS UMR 6556 Ecologie, Evolution, Symbiose, 40 Avenue du Recteur Pineau, 86022 Poitiers, France
2 Université de Lyon, F-69000, Lyon; Université Lyon 1; CNRS, UMR5558, Laboratoire de Biométrie et Biologie Evolutive, F-69622, Villeurbanne, France

* Corresponding author: RC; Email: richard.cordaux{at}univ-poitiers.fr Phone: +33 (0)5 49 45 36 51; Fax: +33 (0)5 49 45 40 15

Received for publication March 10, 2008. Revision received May 16, 2008. Accepted for publication June 10, 2008.

The streamlined genomes of ancient obligate endosymbionts generally lack transposable elements, such as insertion sequence (IS). Yet, the genome of Wolbachia, one of the most abundant bacterial endosymbionts on Earth, is littered with IS. Such a paradox raises the question as to why there are so many IS in the genome of this ancient endosymbiont. To address this question, we investigated IS transpositional activity in the unculturable Wolbachia by tracking the evolutionary dynamics and history of ISWpi1 elements. We show that: (i) ISWpi1 is widespread in Wolbachia, being present in at least 55% of the 40 sampled strains, (ii) ISWpi1 copies exhibit virtually identical nucleotide sequences both within and among Wolbachia genomes and possess an intact transposase gene, (iii) individual ISWpi1 copies are differentially inserted among Wolbachia genomes, and (iv) ISWpi1 occurs at variable copy numbers among Wolbachia genomes. Collectively, our results provide compelling evidence for intense ISWpi1 transpositional activity and frequent ISWpi1 horizontal transmission among strains during recent Wolbachia evolution. Thus, the genomes of ancient obligate endosymbionts can carry high loads of functional and transpositionally active transposable elements. Our results also indicate that Wolbachia genomes have experienced multiple and temporally distinct ISWpi1 invasions during their evolutionary history. Such recurrent exposition to new IS invasions may explain, at least partly, the unusually high density of transposable elements found in the genomes of Wolbachia endosymbionts.

Key Words: transposable element • insertion sequence • transpositional activity • horizontal transmission • obligate endosymbiont • Wolbachia


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