Genotypic and phenotypic adaptation of pathogens: lesson from the genus Bordetella.

To relate genomic changes to phenotypic adaptation and evolution from environmental bacteria to obligate human pathogens, focusing on the examples within Bordetella species. Recent studies showed that animal-pathogenic and human-pathogenic Bordetella species evolved from environmental ancestors in soil. The animal-pathogenic Bordetella bronchiseptica can hijack the life cycle of the soil-living amoeba Dictyostelium discoideum, surviving inside single-celled trophozoites, translocating to the fruiting bodies and disseminating along with amoeba spores. The association with amoeba may have been a 'training ground' for bacteria during the evolution to pathogens. Adaptation to an animal-associated life style was characterized by decreasing metabolic versatility and genome size and by acquisition of 'virulence factors' mediating the interaction with the new animal hosts. Subsequent emergence of human-specific pathogens, such as Bordetella pertussis from zoonoses of broader host range progenitors, was accompanied by a dramatic reduction in genome size, marked by the loss of hundreds of genes. The evolution of Bordetella from environmental microbes to animal-adapted and obligate human pathogens was accompanied by significant genome reduction with large-scale gene loss during divergence.