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MBE Advance Access published online on October 19, 2005
Molecular Biology and Evolution, doi:10.1093/molbev/msj042
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© The Author 2005. 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 October 10, 2005

Research Article

Genome Plasticity and ori-ter Rebalancing in Salmonella typhi

Gui-Rong Liu 1, Wei-Qiao Liu 2, Randal N. Johnston 3, Kenneth E. Sanderson 4, Shao-Xian Li 5 #, and Shu-Lin Liu 1*

1 Department of Microbiology, Peking University Health Science Center, Beijing, China; Department of Microbiology and Infectious Diseases, University of Calgary, Calgary, AB, Canada; Department of Microbiology, Harbin Medical University, Harbin, China
2 Department of Microbiology and Infectious Diseases, University of Calgary, Calgary, AB, Canada; Department of Biological Sciences, University of Calgary, Calgary, AB, Canada
3 Department of Biochemistry and Molecular Biology, University of Calgary, Calgary, AB, Canada
4 Department of Biological Sciences, University of Calgary, Calgary, AB, Canada
5 Department of Microbiology, Harbin Medical University, Harbin, China

* To whom correspondence should be addressed.
Shu-Lin Liu, E-mail: slliu{at}bjmu.edu.cn, slliu@ucalgary.ca


  Abstract

Genome plasticity resulting from frequent rearrangement of the bacterial genome is a fascinating but poorly understood phenomenon. First reported in Salmonella typhi, it has been observed only in a small number of Salmonella serovars, although the over 2500 known Salmonella serovars are all very closely related. To gain insights into this phenomenon and elucidate its roles in bacterial evolution, especially those involved in the formation of particular pathogens, we systematically analyzed the genomes of 127 wild type S. typhi strains isolated from many places of the world and compared them with the two sequenced strains, Ty2 and CT18, attempting to find possible associations between genome rearrangement and other significant genomic features. Like some other host-adapted Salmonella serovars, S. typhi contained large genome insertions, including the 134 kb Salmonella pathogenicity island, SPI7. Our analyses showed that SPI7 disrupted the physical balance of the bacterial genome between the replication origin (ori) and terminus (ter) when this DNA segment was inserted into the genome, and rearrangement in individual strains further changed the genome balance status, with a general tendency towards a better balanced genome structure. In a given S. typhi strain, genome diversification occurred and resulted in different structures among cells in the culture. Under a stressed condition, bacterial cells with better balanced genome structures were selected to greatly increase in proportion; in such cases, bacteria with better balanced genomes formed larger colonies and grew with shorter generation times. Our results support the hypothesis that genome plasticity as a result of frequent rearrangement provides the opportunity for the bacterial genome to adopt a better balanced structure and thus eventually stabilizes the genome during evolution.

Keywords: Salmonella typhi; genome plasticity; ori-ter rebalancing; I-CeuI, genome rearrangement; typhoid.

#: Dr.Shao-Xian Li is deceased.


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