Unexpected similarities between Bordetella avium and other pathogenic Bordetellae

Abstract

Bordetella avium causes an upper respiratory tract disease (bordetellosis) in avian species. Commercially raised turkeys are particularly susceptible. Like other pathogenic members of the genus Bordetella (B. pertussis and B. bronchiseptica) that infect mammals, B. avium binds 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. avium does not express a number of the factors known to be associated with virulence in the other two Bordetella species. Nevertheless, with signature-tagged mutagenesis, four avirulent mutants that had lesions in genes orthologous to those associated with virulence in B. pertussis and B. bronchiseptica (bvgS, fhaB, fhaC, and fimC) were identified. None of the four B. avium genes 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. avium orthologues were very similar in all three Bordetella species. 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.

FIG. 1.

Genetic and physical maps of the B. avium genes discovered by STM. (A) Sizes and arrangement of B. pertussis genes (based on data in references and 54). (B) B. avium genes discovered by STM. Locations of insertion mutations that genetically define each gene are indicated by black triangles. The insertions are alphanumerically coded as in Table 2. Each gene is shaded to indicate the approximate degree of similarity to the B. pertussis gene (or region of a gene) at the amino acid sequence level, as denoted by the key. (C) Comparison of the fimA-encoded amino acid sequence of B. avium, truncated FimA of B. pertussis, and complete FimA of B. bronchiseptica (B. bronch.). Additional differences are described in the text. Homology scores (colons indicate identity; periods indicate similarity) were measured by using the PAM 250 scoring matrix in MACAW.