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Journal of Bacteriology, June 2009, p. 3569-3579, Vol. 191, No. 11
0021-9193/09/$08.00+0 doi:10.1128/JB.01767-08
Copyright © 2009, American Society for Microbiology. All Rights Reserved.
Analysis of Ten Brucella Genomes Reveals Evidence for Horizontal Gene Transfer Despite a Preferred Intracellular Lifestyle
,
Alice R. Wattam,1*
Kelly P. Williams,1
Eric E. Snyder,1
Nalvo F. Almeida Jr.,1,6
Maulik Shukla,1
A. W. Dickerman,1
O. R. Crasta,1
R. Kenyon,1
J. Lu,1
J. M. Shallom,1
H. Yoo,1
T. A. Ficht,2
R. M. Tsolis,3
C. Munk,4
R. Tapia,4
C. S. Han,4
J. C. Detter,4
D. Bruce,4
T. S. Brettin,4
Bruno W. Sobral,1
Stephen M. Boyle,5 and
João C. Setubal1,7
Virginia Bioinformatics Institute, Virginia Tech, Blacksburg, Virginia 24061,1 Department of Veterinary Pathobiology, Texas A&M University and Texas Agricultural Experiment Station, College Station, Texas 77843-4467,2 Department of Medical Microbiology and Immunology, School of Medicine, University of California at Davis, One Shields Ave., Davis, California 95616-8645,3 Bioscience Division, Los Alamos National Laboratory, Los Alamos, New Mexico 87544,4 Center for Molecular Medicine and Infectious Diseases, Virginia-Maryland Regional College of Veterinary Medicine, Virginia Tech, Blacksburg, Virginia 24061,5 Departamento de Computacao e Estatistica/Universidade Federal de Mato Grosso do Sul, Campo Grande, Brazil,6 Department of Computer Science, Virginia Tech, Blacksburg, Virginia 240617
Received 17 December 2008/ Accepted 12 March 2009
The facultative intracellular bacterial pathogen Brucella infects a wide range of warm-blooded land and marine vertebrates and causes brucellosis. Currently, there are nine recognized Brucella species based on host preferences and phenotypic differences. The availability of 10 different genomes consisting of two chromosomes and representing six of the species allowed for a detailed comparison among themselves and relatives in the order Rhizobiales. Phylogenomic analysis of ortholog families shows limited divergence but distinct radiations, producing four clades as follows: Brucella abortus-Brucella melitensis, Brucella suis-Brucella canis, Brucella ovis, and Brucella ceti. In addition, Brucella phylogeny does not appear to reflect the phylogeny of Brucella species' preferred hosts. About 4.6% of protein-coding genes seem to be pseudogenes, which is a relatively large fraction. Only B. suis 1330 appears to have an intact β-ketoadipate pathway, responsible for utilization of plant-derived compounds. In contrast, this pathway in the other species is highly pseudogenized and consistent with the "domino theory" of gene death. There are distinct shared anomalous regions (SARs) found in both chromosomes as the result of horizontal gene transfer unique to Brucella and not shared with its closest relative Ochrobactrum, a soil bacterium, suggesting their acquisition occurred in spite of a predominantly intracellular lifestyle. In particular, SAR 2-5 appears to have been acquired by Brucella after it became intracellular. The SARs contain many genes, including those involved in O-polysaccharide synthesis and type IV secretion, which if mutated or absent significantly affect the ability of Brucella to survive intracellularly in the infected host.
* Corresponding author. Mailing address: Virginia Bioinformatics Institute, Virginia Tech, Blacksburg, VA 24061. Phone: (540) 231-1263. Fax: (540) 231-2606. E-mail: wattam{at}vbi.vt.edu
Published ahead of print on 3 April 2009.
Supplemental material for this article may be found at http://jb.asm.org/.
Journal of Bacteriology, June 2009, p. 3569-3579, Vol. 191, No. 11
0021-9193/09/$08.00+0 doi:10.1128/JB.01767-08
Copyright © 2009, American Society for Microbiology. All Rights Reserved.
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