Abstract
Bordetella pertussis, B. bronchiseptica, B. parapertussishu, and B. parapertussisov are closely related respiratory pathogens that infect mammalian species. B. pertussis and B. parapertussishu are exclusively human pathogens and cause whooping cough, or pertussis, a disease that has resurged despite vaccination. Although it most often infects animals, infrequently B. bronchiseptica is isolated from humans, and these infections are thought to be zoonotic. B. pertussis and B. parapertussishu are assumed to have evolved from a B. bronchiseptica–like ancestor independently. To determine the phylogenetic relationships among these species, housekeeping and virulence genes were sequenced, comparative genomic hybridizations were performed using DNA microarrays, and the distribution of insertion sequence elements was determined, using a collection of 132 strains. This multifaceted approach distinguished four complexes, representing B. pertussis, B. parapertussishu, and two distinct B. bronchiseptica subpopulations, designated complexes I and IV. Of the two B. bronchiseptica complexes, complex IV was more closely related to B. pertussis. Of interest, while only 32% of the complex I strains were isolated from humans, 80% of the complex IV strains were human isolates. Comparative genomic hybridization analysis identified the absence of the pertussis toxin locus and dermonecrotic toxin gene, as well as a polymorphic lipopolysaccharide biosynthesis locus, as associated with adaptation of complex IV strains to the human host. Lipopolysaccharide structural diversity among these strains was confirmed by gel electrophoresis. Thus, complex IV strains may comprise a human-associated lineage of B. bronchiseptica from which B. pertussis evolved. These findings will facilitate the study of pathogen host-adaptation. Our results shed light on the origins of the disease pertussis and suggest that the association of B. pertussis with humans may be more ancient than previously assumed.
Highlights
The genus Bordetella is composed of several species, of which three are exclusively respiratory pathogens of mammalian hosts: B. bronchiseptica, B. pertussis, and B. parapertussis
Previous research indicated that B. pertussis and B. parapertussishu independently evolved from a B. bronchiseptica–like ancestor [8.9], and comparison of the genomes of the three isolates chosen for sequencing suggested that the time to the last common ancestor (LCA) for B. pertussis and B. parapertussishu and for B. bronchiseptica was 0.7 to 3.5 and 0.27 to 1.4 million years, respectively [10]
Of the B. bronchiseptica complex IV isolates, 80% were isolated from humans, while this was the case for only 32% of the complex I isolates
Summary
The genus Bordetella is composed of several species, of which three are exclusively respiratory pathogens of mammalian hosts: B. bronchiseptica, B. pertussis, and B. parapertussis ( referred to as the mammalian bordetellae). B. bronchiseptica causes chronic and often asymptomatic respiratory tract infections in a wide variety of mammals. It is only sporadically isolated from humans [1,2], from immunocompromised individuals, and human infections have been considered to be zoonotic [3]. B. pertussis and B. parapertussishu have been isolated only from humans and cause acute, transient infections and disease, designated whooping cough or pertussis. Previous research indicated that B. pertussis and B. parapertussishu independently evolved from a B. bronchiseptica–like ancestor [8.9], and comparison of the genomes of the three isolates chosen for sequencing suggested that the time to the last common ancestor (LCA) for B. pertussis and B. parapertussishu and for B. bronchiseptica was 0.7 to 3.5 and 0.27 to 1.4 million years, respectively [10]
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