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

Abstract

Purpose of review: To relate genomic changes to phenotypic adaptation and evolution from environmental bacteria to obligate human pathogens, focusing on the examples within Bordetella species.

Recent findings: 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.

Summary: 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.

Fig 1.. Heading: Whole genome phylogeny of ten Bordetella species based on a genome-wide sequence alignment.

Legend: The Neighbor-joining tree shows three clades of species that consist of B. bronchiseptica, B. parapertussis and B. pertussis (black), of B. avium, B. holmesii, B. hinzii, B. pseudohinzii and B. trematum (blue), and of B. ansorpii and B. petrii (brown). The tree was rooted according to Linz et al., 2016 [7].

Fig 2.. Heading: Genome size of environmental bacteria, pathobionts and host-restricted pathogens in the genus Bordetella.

Legend: Bordetella sp. SCN 68–11 (accession: MEFS00000000), B. sp. SCN 67–23 (MEDQ00000000), B. sp. BFMG2 (PKCD00000000), B. petrii (NC_010170), and B. sp. N (NZ_CP013111), isolated from environmental sources possess the largest genomes in the genus Bordetella. In contrast, the genomes of the obligate host-restricted pathogens B. holmesii (NZ_CP007494), B. avium (NC_010645.1), B. pertussis (NC_002929), B. parapertussis_hu (NC_002928) and B. pseudohinzii (NZ_CP016440) featured substantial reduction. Pathobionts B. trematum (NZ_LT546645), B. hinzii (NZ_CP012076), B. ansorpii (NZ_FKIF00000000), and B. bronchiseptica (NC_002927), have been isolated from multiple animal and human sources.