Host Specificity of Ovine Bordetella parapertussis and the Role of Complement

Abstract

The classical bordetellae are comprised of three subspecies that differ from broad to very limited host specificity. Although several lineages appear to have specialized to particular host species, most retain the ability to colonize and grow in mice, providing a powerful common experimental model to study their differences. One of the subspecies, Bordetella parapertussis, is composed of two distinct clades that have specialized to different hosts: one to humans (Bpphu), and the other to sheep (Bppov). While Bpphu and the other classical bordetellae can efficiently colonize mice, Bppov strains are severely defective in their ability to colonize the murine respiratory tract. Bppov genomic analysis did not reveal the loss of adherence genes, but substantial mutations and deletions of multiple genes involved in the production of O-antigen, which is required to prevent complement deposition on B. bronchiseptica and Bpphu strains. Bppov lacks O-antigen and, like O-antigen mutants of other bordetellae, is highly sensitive to murine complement-mediated killing in vitro. Based on these results, we hypothesized that Bppov failed to colonize mice because of its sensitivity to murine complement. Consistent with this, the Bppov defect in the colonization of wild type mice was not observed in mice lacking the central complement component C3. Furthermore, Bppov strains were highly susceptible to killing by murine complement, but not by sheep complement. These data demonstrate that the failure of Bppov to colonize mice is due to sensitivity to murine, but not sheep, complement, providing a mechanistic example of how specialization that accompanies expansion in one host can limit host range.

Pertussis: Microbiology, Disease, Treatment, and Prevention

“…B. parapertussis may cause disease in domestic animals, including ovine (sheep) and swine (14,47), though the strains infecting these mammalian species arise from different lineages and are genetically distinct (48). In addition, B. bronchiseptica has been identified as a cause of disease among immunocompromised persons and has been isolated from traumatized patients and patients with peritonitis (49)(50)(51)(52) and from domestic dogs, cats, and pigs (52)(53)(54).…”

Acquisition and loss of virulence-associated factors during genome evolution and speciation in three clades of Bordetella species

“…The highly infectious human pathogen B. pertussis is the causative agent of whooping cough, a respiratory disease that is particularly serious and sometimes fatal in infants and in elderly people. One lineage of B. parapertussis causes pneumonia in sheep, while the other lineage causes a whooping cough-like disease in children [ 1 ]. B. bronchiseptica , a respiratory pathogen of diverse mammals, causes a variety of pathologies ranging from chronic and often asymptomatic infection to more acute diseases such as kennel cough in dogs, bronchitis in cats, and bronchopneumonia and atrophic rhinitis in pigs [ 2 – 4 ].…”

Conserved Patterns of Symmetric Inversion in the Genome Evolution of Bordetella Respiratory Pathogens

“…B. bronchiseptica causes respiratory disease in a range of mammals, such as kennel cough in dogs, but also various infections in humans (3)(4)(5)(6). Divergent lineages of B. parapertussis infect the respiratory tracts of sheep and humans (7)(8)(9). The remaining "nonclassic" species are phylogenetically more distant and have been recovered from varied hosts and pathologies, in particular, B. holmesii and B. hinzii from humans, which is reflected in their discrete virulence-associated-gene compositions (10).…”