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MBE Advance Access published online on September 6, 2006
Molecular Biology and Evolution, doi:10.1093/molbev/msl108
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© The Author 2006. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org
Accepted September 1, 2006

Research Article

Evolution of the Terminal Regions of the Streptomyces Linear Chromosome

Frédéric Choulet 1, Bertrand Aigle 1, Alexandre Gallois 1, Sophie Mangenot 2, Claude Gerbaud 3, Chantal Truong 2, François-Xavier Francou 3, Céline Fourrier 1, Michel Guérineau 3, Bernard Decaris 1, Valérie Barbe 2, Jean-Luc Pernodet 3, and Pierre Leblond 1 *

1 Laboratoire de Génétique et Microbiologie, UMR INRA 1128, IFR 110, Université Henri Poincaré Nancy 1, Faculté des Sciences et Techniques, 54506 Vandoeuvre-lès-Nancy, France
2 Génoscope, Centre National de Séquençage, 2 rue Gaston Crémieux CP5706 91057 Evry cedex, France
3 Institut de Génétique et Microbiologie, UMR CNRS 8621, Université Paris-Sud 11, Bâtiment 400, 91405 Orsay cedex, France

* To whom correspondence should be addressed.
Pierre Leblond, E-mail: leblond{at}nancy.inra.fr


  Abstract

Comparative analysis of the Streptomyces chromosome sequences, between S. coelicolor, S. avermitilis and S. ambofaciens ATCC23877 (whose partial sequence is released in this study), revealed a highly compartmentalized genetic organization of their genome. Indeed, despite the presence of specific genomic islands, the central part of the chromosome appears highly syntenic. In contrast, the chromosome of each species exhibits large species-specific terminal regions (from 753 kb to 1393 kb), even when considering closely related species (S. ambofaciens and S. coelicolor). Interestingly, the size of the central conserved region between species decreases as the phylogenetic distance between them increases, while the specific terminal fraction reciprocally increases in size. Between highly syntenic central regions and species-specific chromosomal parts, there is a notable degeneration of synteny due to frequent insertions/deletions. This reveals a massive and constant genomic flux (from lateral gene transfer and DNA rearrangements) affecting the terminal contingency regions. We speculate that a gradient of recombination rate (i.e. insertion/deletion events) towards the extremities is the force driving the exclusion of essential genes from the terminal regions (i.e. chromosome compartmentalization), and generating a fast gene turn over for strong adaptation capabilities.

Keywords: comparative genomics; linear bacterial chromosome; lateral gene transfer; contingency regions; Streptomyces.
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