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Comparative analyses of a cystic fibrosis isolate of Bordetella bronchiseptica reveal differences in important pathogenic phenotypes.

ABSTRACT: Bordetella bronchiseptica is a Gram-negative bacterium that infects and causes disease in a wide variety of animals. B. bronchiseptica also infects humans, thereby demonstrating zoonotic transmission. An extensive characterization of human B. bronchiseptica isolates is needed to better understand the distinct genetic and phenotypic traits associated with these zoonotic transmission events. Using whole-genome transcriptome and CGH analysis, we report that a B. bronchiseptica cystic fibrosis isolate, T44625, contains a distinct genomic content of virulence-associated genes and differentially expresses these genes compared to the sequenced model laboratory strain RB50, a rabbit isolate. The differential gene expression pattern correlated with unique phenotypes exhibited by T44625, which included lower motility, increased aggregation, hyperbiofilm formation, and an increased in vitro capacity to adhere to respiratory epithelial cells. Using a mouse intranasal infection model, we found that although defective in establishing high bacterial burdens early during the infection process, T44625 persisted efficiently in the mouse nose. By documenting the unique genomic and phenotypic attributes of T44625, this report provides a blueprint for understanding the successful zoonotic potential of B. bronchiseptica and other zoonotic bacteria.

SUBMITTER: Sukumar N

PROVIDER: S-EPMC3993408 | biostudies-literature | 2014 Apr

REPOSITORIES: biostudies-literature

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Comparative analyses of a cystic fibrosis isolate of Bordetella bronchiseptica reveal differences in important pathogenic phenotypes.

Sukumar Neelima N Nicholson Tracy L TL Conover Matt S MS Ganguly Tridib T Deora Rajendar R

Infection and immunity 20140127 4

Bordetella bronchiseptica is a Gram-negative bacterium that infects and causes disease in a wide variety of animals. B. bronchiseptica also infects humans, thereby demonstrating zoonotic transmission. An extensive characterization of human B. bronchiseptica isolates is needed to better understand the distinct genetic and phenotypic traits associated with these zoonotic transmission events. Using whole-genome transcriptome and CGH analysis, we report that a B. bronchiseptica cystic fibrosis isola ...[more]

PMID: 24470470

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Project description:The respiratory pathogenic bacterium Bordetella bronchiseptica can persistently survive in terrestrial and aquatic environments, providing a source of infection. However, the environmental lifestyle of the bacterium is poorly understood. In this study, expecting repeated encounters of the bacteria with environmental protists, we explored the interaction between B. bronchiseptica and a representative environmental amoeba, Acanthamoeba castellanii, and found that the bacteria resisted amoeba digestion and entered contractile vacuoles (CVs), which are intracellular compartments involved in osmoregulation, to escape amoeba cells. In prolonged coculture, A. castellanii supported the proliferation of B. bronchiseptica. The avirulent Bvg- phase, but not the virulent Bvg+ phase, of the bacteria was advantageous for survival in the amoebae. We further demonstrate that two Bvg+ phase-specific virulence factors, filamentous hemagglutinin and fimbriae, were targeted for predation by A. castellanii. These results are evidence that the BvgAS two-component system, the master regulator for Bvg phase conversion, plays an indispensable role in the survival of B. bronchiseptica in amoebae. IMPORTANCE The pathogenic bacterium Bordetella bronchiseptica, which causes respiratory diseases in various mammals, exhibits distinct Bvg+ and Bvg- phenotypes. The former represents the virulent phase, in which the bacteria express a set of virulence factors, while the role of the latter in the bacterial life cycle remains to be understood. In this study, we demonstrate that B. bronchiseptica in the Bvg- phase, but not the Bvg+ phase, survives and proliferates in coculture with Acanthamoeba castellanii, an environmental amoeba. Two Bvg+ phase-specific virulence factors, filamentous hemagglutinin and fimbriae, were targeted by A. castellanii predation. B. bronchiseptica turns into the Bvg- phase at temperatures in which the bacteria normally encounter these amoebae. These findings demonstrate that the Bvg- phase of B. bronchiseptica is advantageous for survival outside mammalian hosts and that the bacteria can utilize protists as transient hosts in natural environments.

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Comparative analyses of a cystic fibrosis isolate of Bordetella bronchiseptica reveal differences in important pathogenic phenotypes.

Publications

Comparative analyses of a cystic fibrosis isolate of Bordetella bronchiseptica reveal differences in important pathogenic phenotypes.

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