Evolutionary relationships in the genus <i>Bordetella</i>

Aricò, Beatrice; Gross, Roy; Smida, Jan; Rappuoli, Rino

doi:10.1111/j.1365-2958.1987.tb01936.x

Cited by 86 publications

(75 citation statements)

References 22 publications

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“…The causative agents, Bordetella pertussis and Bordetella parapertussis hu , are human-adapted pathogens that belong to a clade of very closely related Gram-negative bacteria that cause respiratory infections in mammals. Phylogenetic analyses indicate that Bordetella bronchiseptica, which displays a broad host range and typically colonizes its hosts chronically and asymptomatically, was the progenitor of this clade, with B. pertussis diverging relatively early and B. parapertussis hu diverging independently and much more recently than B. pertussis (3)(4)(5)(6). Adaptation to humans and the propensity to cause acute disease (in which the infection is eventually cleared) rather than chronic disease (characterized by persistence of the bacteria, often for the lifetime of the host) has, therefore, evolved twice within this group of bacteria.…”

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confidence: 99%

Bordetellafilamentous hemagglutinin plays a critical role in immunomodulation, suggesting a mechanism for host specificity

Inatsuka

Julio

Cotter

2005

Proc. Natl. Acad. Sci. U.S.A.

120

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Bordetella pertussis, the causative agent of the acute childhood respiratory disease whooping cough, is a human-adapted variant of Bordetella bronchiseptica, which displays a broad host range and typically causes chronic, asymptomatic infections. These pathogens express a similar but not identical surface-exposed and secreted protein called filamentous hemagglutinin (FHA) that has been proposed to function as both a primary adhesin and an immunomodulator. To test the hypothesis that FHA plays an important role in determining host specificity and͞or the propensity to cause acute versus chronic disease, we constructed a B. bronchiseptica strain expressing FHA from B. pertussis (FHA Bp) and compared it with wild-type B. bronchiseptica in several naturalhost infection models. FHA Bp was able to substitute for FHA from B. bronchiseptica (FHA Bb) with regard to its ability to mediate adherence to several epithelial and macrophage-like cell lines in vitro, but it was unable to substitute for FHA Bb in vivo. Specifically, FHA Bb, but not FHABp, allowed B. bronchiseptica to colonize the lower respiratory tracts of rats, to modulate the inflammatory response in the lungs of immunocompetent mice, resulting in decreased lung damage and increased bacterial persistence, to induce a robust anti-Bordetella antibody response in these immunocompetent mice, and to overcome innate immunity and cause a lethal infection in immunodeficient mice. These results indicate a critical role for FHA in B. bronchiseptica-mediated immunomodulation, and they suggest a role for FHA in host specificity.inflammation ͉ adhesin ͉ respiratory infection ͉ filamentous hemagglutinin D espite widespread vaccine coverage, whooping cough, or pertussis, remains a serious threat to human health, and its incidence has been increasing in recent years (1, 2). The causative agents, Bordetella pertussis and Bordetella parapertussis hu , are human-adapted pathogens that belong to a clade of very closely related Gram-negative bacteria that cause respiratory infections in mammals. Phylogenetic analyses indicate that Bordetella bronchiseptica, which displays a broad host range and typically colonizes its hosts chronically and asymptomatically, was the progenitor of this clade, with B. pertussis diverging relatively early and B. parapertussis hu diverging independently and much more recently than B. pertussis (3-6). Adaptation to humans and the propensity to cause acute disease (in which the infection is eventually cleared) rather than chronic disease (characterized by persistence of the bacteria, often for the lifetime of the host) has, therefore, evolved twice within this group of bacteria. Although a variety of Bordetella virulence factors have been characterized (4, 7-10), the mechanisms that determine host specificity and disease characteristics are not understood.Filamentous hemagglutinin (FHA), a primary component of acellular pertussis vaccines, is a large, ␤-helical, highly immunogenic protein that is both surface-associated and secreted (11)(12)(13). In vitro...

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confidence: 99%

Bordetellafilamentous hemagglutinin plays a critical role in immunomodulation, suggesting a mechanism for host specificity

Inatsuka

Julio

Cotter

2005

Proc. Natl. Acad. Sci. U.S.A.

120

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“…bronchiseptica is closely related to Bordetella pertussis, the etiologic agent of human whooping cough, and this close evolutionary relationship has been documented by DNA hybridization (22), comparative sequence analysis (2), and multilocus enzyme electrophoresis (41). Both B. pertussis and B. bronchiseptica colonize the respiratory epithelium and express several factors that are likely to be important for the interaction with their respective hosts.…”

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The bvgAS locus negatively controls motility and synthesis of flagella in Bordetella bronchiseptica

et al. 1992

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The products of the bvgAS locus coordinately regulate the expression of BordeteUa virulence factors in response to environmental conditions. We have identified a phenotype in BordeteUa bronchiseptica that is negatively controlled by bvg. Environmental signals which decrease (modulate) the expression of bvg-activated genes lead to flagellum production and motility in B. bronchiseptica. Wild-type (Bvg') strains are motile and produce peritrichous flagella only in the presence of modulating signals, whereas Bvg-(AbvgAS or AbvgS) strains are motile in the absence of modulators. The bvgS-C3 mutation, which confers signal insensitivity and constitutive activation of positively controlled loci, eliminates the induction of motility and production of flagellar organelles. The response to environmental signals is conserved in a diverse set of clinical isolates of both B. bronchiseptica and B. avium, another motile BordeteUla species; however, nicotinic acid induced motility only in B. bronchiseptica. Purification of flagellar filaments from B. bronchiseptica strains by differential centrifugation followed by CsCI equilibrium density gradient centrifugation revealed two classes of flagellins of Mr 35,000 and 40,000. A survey of clinical isolates identified only these two flagellin isotypes, and coexpression of the two forms was not detected in any strain. All B. avium strains tested expressed a 42,000-M, flagellin.Amino acid sequence analysis of the two B. bronchiseptica flagellins revealed 100%o identity in the N-terminal region and 80%o identity with SalmoneUla typhimurium flagellin. Monoclonal antibody 15D8, which recognizes a conserved epitope in flagellins in members of the family Enterobacteriaceae, cross-reacted with flagellins from B. bronchiseptica and B. avium. Our results highlight the biphasic nature of the B. bronchiseptica bvg regulon and provide a preliminary characterization of the Bvg-regulated motility phenotype.

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“…These three Bordetella species are closely related at the nucleotide sequence level (4,24), and their relatedness has been further established using a variety of common molecular strain typing techniques (reviewed in reference 29). Phylogenetic analyses of the genus Bordetella, using pulsed-field gel electrophoresis, multilocus enzyme electrophoresis (MLEE), and IS typing data, suggested that B. pertussis, human-derived B. parapertussis, and sheep-derived B. parapertussis arose independently from B. bronchiseptica-like ancestors (46,47).…”

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Bordetella Species Are Distinguished by Patterns of Substantial Gene Loss and Host Adaptation

et al. 2004

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Pathogens of the bacterial genus Bordetella cause respiratory disease in humans and animals. Although virulence and host specificity vary across the genus, the genetic determinants of this diversity remain unidentified. To identify genes that may underlie key phenotypic differences between these species and clarify their evolutionary relationships, we performed a comparative analysis of genome content in 42 Bordetella strains by hybridization of genomic DNA to a microarray representing the genomes of three Bordetella species and by subtractive hybridization. Here we show that B. pertussis and B. parapertussis are predominantly differentiated from B. bronchiseptica by large, species-specific regions of difference, many of which encode or direct synthesis of surface structures, including lipopolysaccharide O antigen, which may be important determinants of host specificity. The species also exhibit sequence diversity at a number of surface protein-encoding loci, including the fimbrial major subunit gene, fim2. Gene loss, rather than gene acquisition, accompanied by the proliferation of transposons, has played a fundamental role in the evolution of the pathogenic bordetellae and may represent a conserved evolutionary mechanism among other groups of microbial pathogens.Bacteria of the genus Bordetella are important pathogens that cause respiratory disease in humans and animals. B. pertussis is the causative agent of whooping cough (8), which is responsible for up to 500,000 annual deaths worldwide in unvaccinated populations (52) and is increasing in incidence in some countries with established vaccination programs, including the United States (e.g., see references 15, 30, and 38). Although most Bordetella species can cause similar disease in the upper respiratory tract, their host specificities vary dramatically. B. pertussis infects only humans; B. parapertussis strains can be classified in two groups, one of which infects only humans and one of which infects only sheep (16,17,25); B. bronchiseptica causes respiratory infections in a wide variety of mammals and birds but only rarely in humans (22,41,51).These three Bordetella species are closely related at the nucleotide sequence level (4, 24), and their relatedness has been further established using a variety of common molecular strain typing techniques (reviewed in reference 29). Phylogenetic analyses of the genus Bordetella, using pulsed-field gel electrophoresis, multilocus enzyme electrophoresis (MLEE), and IS typing data, suggested that B. pertussis, human-derived B. parapertussis, and sheep-derived B. parapertussis arose independently from B. bronchiseptica-like ancestors (46, 47). Comparative genome sequencing of a representative strain of each species (33) confirmed that nucleotide sequence similarity is very high in conserved regions of the genome but demonstrated that B. pertussis and B. parapertussis evolved by genome decay from a B. bronchiseptica-like ancestor.Although a number of critical conserved virulence mechanisms have been identified in the bor...

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Evolutionary relationships in the genus Bordetella

Cited by 86 publications

References 22 publications

Bordetellafilamentous hemagglutinin plays a critical role in immunomodulation, suggesting a mechanism for host specificity

Bordetellafilamentous hemagglutinin plays a critical role in immunomodulation, suggesting a mechanism for host specificity

The bvgAS locus negatively controls motility and synthesis of flagella in Bordetella bronchiseptica

Bordetella Species Are Distinguished by Patterns of Substantial Gene Loss and Host Adaptation

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