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Journal of Bacteriology, August 2008, p. 5502-5511, Vol. 190, No. 15
0021-9193/08/$08.00+0     doi:10.1128/JB.00226-08
Copyright © 2008, American Society for Microbiology. All Rights Reserved.

Replacement of Adenylate Cyclase Toxin in a Lineage of Bordetella bronchiseptica ^,

Department of Veterinary and Biomedical Sciences, The Pennsylvania State University, University Park, Pennsylvania,¹ Graduate Program in Biochemistry, Microbiology and Molecular Biology, The Pennsylvania State University, University Park, Pennsylvania,² Respiratory Diseases of Livestock Research Unit, National Animal Disease Center, Agricultural Research Service, USDA, Ames, Iowa,³ The Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton Cambridge, United Kingdom⁴

Received 13 February 2008/ Accepted 1 June 2008

Bordetella bronchiseptica is a gram-negative respiratory pathogen that infects a wide range of hosts and causes a diverse spectrum of disease. This diversity is likely affected by multiple factors, such as host immune status, polymicrobial infection, and strain diversity. In a murine model of infection, we found that the virulence of B. bronchiseptica strains, as measured by the mean lethal dose, varied widely. Strain 253 was less virulent than the typically studied strain, RB50. Transcriptome analysis showed that cyaA, the gene encoding adenylate cyclase toxin (CyaA), was the most downregulated transcript identified in strain 253 compared to that in strain RB50. Comparative genomic hybridization and genome sequencing of strain 253 revealed that the cya locus, which encodes, activates, and secretes CyaA, was replaced by an operon (ptp) predicted to encode peptide transport proteins. Other B. bronchiseptica strains from the same phylogenetic lineage as that of strain 253 also lacked the cya locus, contained the ptp genes, and were less virulent than strain RB50. Although the loss of CyaA would be expected to be counterselected since it is conserved among the classical bordetellae and believed to be important to their success, our data indicate that the loss of this toxin and the gain of the ptp genes occurred in an ancestral strain that then expanded into a lineage. This suggests that there may be ecological niches in which CyaA is not critical for the success of B. bronchiseptica.

Published ahead of print on 13 June 2008.

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