Unexpected Similarities between Bordetella aviumand Other Pathogenic Bordetellae

ABSTRACTBordetella aviumcauses an upper respiratory tract disease (bordetellosis) in avian species. Commercially raised turkeys are particularly susceptible. Like other pathogenic members of the genus Bordetella(B. pertussisand B. bronchiseptica) that infect mammals, B. aviumbinds preferentially to ciliated tracheal epithelial cells and produces similar signs of disease. These similarities prompted us to study bordetellosis in turkeys as a possible nonmammalian model for whooping cough, the exclusively human childhood disease caused by B. pertussis. One impediment to accepting such a host-pathogen model as relevant to the human situation is evidence suggesting that B. aviumdoes not express a number of the factors known to be associated with virulence in the other two Bordetellaspecies. Nevertheless, with signature-tagged mutagenesis, four avirulent mutants that had lesions in genes orthologous to those associated with virulence in B. pertussisand B. bronchiseptica(bvgS, fhaB, fhaC, and fimC) were identified. None of the four B. aviumgenes had been previously identified as encoding factors associated with virulence, and three of the insertions (in fhaB, bvgS, and fimC) were in genes or gene clusters inferred as being absent or incomplete in B. avium, based upon the lack of DNA sequence similarities in hybridization studies and/or the lack of immunological cross-reactivity of the putative products. We further found that the genotypic arrangements of most of the B. aviumorthologues were very similar in all three Bordetellaspecies. In vitro tests, including hemagglutination, tracheal ring binding, and serum sensitivity, helped further define the phenotypes conferred by the mutations. Our findings strengthen the connection between the causative agents and the pathogenesis of bordetellosis in all hosts and may help explain the striking similarities of the histopathologic characteristics of this upper airway disease in avian and mammalian species.