Acquisition and loss of virulence-associated factors during genome evolution and speciation in three clades of Bordetella species

Authors: LINZ, BODO - Pennsylvania State University; IVANOV, YURY - Pennsylvania State University; PRESTON, ANDREW - University Of Bath; BRINKAC, LAUREN - J Craig Venter Institute; PARKHILL, JULIAN - Wellcome Trust Sanger Institute; KIM, MARIA - J Craig Venter Institute; HARRIS, SIMON - Wellcome Trust Sanger Institute; GOODFIELD, LAURA - Pennsylvania State University; FRY, NORMAN - Public Health England (PHE); GORRING, ANDREW - Public Health England (PHE); Nicholson, Tracy; Register, Karen; LOSADA, LILIANA - J Craig Venter Institute; HARVILL, ERIC - Pennsylvania State University

Submitted to: BMC Genomics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/22/2016
Publication Date: 12/1/2016
Publication URL: http://handle.nal.usda.gov/10113/5642523
Citation: Linz, B., Ivanov, Y., Preston, A., Brinkac, L., Parkhill, J., Kim, M., Harris, S.R., Goodfield, L.L., Fry, N.K., Gorring, A.R., Nicholson, T.L., Register, K.B., Losada, L., Harvill, E.T. 2016. Acquisition and loss of virulence-associated factors during genome evolution and speciation in three clades of Bordetella species. Biomed Central (BMC) Genomics. 17:767. doi: 10.1186/s12864-016-3112-5.

Interpretive Summary: Bacteria in the genus Bordetella include nine species that are important pathogens. B. pertussis causes whooping cough, a serious and sometimes fatal disease in infants and in elderly people. Some strains of B. parapertussis also cause whooping cough-like disease in children while others cause pneumonia in sheep. B. bronchiseptica, a respiratory pathogen of mammals, causes a variety of chronic or acute infections, sometimes fatal, such as kennel cough in dogs, bronchitis in cats and pneumonia and atrophic rhinitis in pigs. Bordetella also includes six more distantly related and less extensively studied species: B. avium, a poultry pathogen; B. hinzii, a pathogen in poultry and, occasionally, immunocompromised humans; B. holmesii, B. trematum and B. ansorpii, associated with cases of human septicemia, endocarditis and wound infections; and B. petri, an environmental bacterium that has not been associated with disease. In this study we analyze 128 genome sequences representing all nine species and compare their sequence diversity and gene content. Our analyses reveal Bordetella species comprise three divergent families. The oldest, ancestral family includes B. petrii and B. ansorpii. From this lineage, a second family containing B. pertussis, B. parapertussis and B. bronchiseptica emerged as well as a third family that includes the remaining species. Analysis of genetic diversity within each species shows that a large number of genes were lost during the evolution of species that are restricted to one or a few hosts. In some cases, species acquired key virulence genes that subsequently contributed to their emergence as pathogens. These data greatly facilitate ongoing efforts to better understand evolution, host adaptation and virulence mechanisms of the Bordetella, potentially leading to novel diagnostic tools and vaccine approaches and improved disease prevention and management strategies.

Technical Abstract: Bacteria in the genus Bordetella include nine species that are important pathogens. B. pertussis causes whooping cough, a serious and sometimes fatal disease in infants and in elderly people. Some strains of B. parapertussis also cause whooping cough-like disease in children while others cause pneumonia in sheep. B. bronchiseptica, a respiratory pathogen of mammals, causes a variety of chronic or acute infections, sometimes fatal, such as kennel cough in dogs, bronchitis in cats and pneumonia and atrophic rhinitis in pigs. Bordetella also includes six more distantly related and less extensively studied species: B. avium, a poultry pathogen; B. hinzii, a pathogen in poultry and, occasionally, immunocompromised humans; B. holmesii, B. trematum and B. ansorpii, associated with cases of human septicemia, endocarditis and wound infections; and B. petri, an environmental bacterium that has not been associated with disease. In this study we analyze 128 genome sequences representing all nine species and compare their sequence diversity and gene content. Our analyses reveal Bordetella species comprise three divergent families. The oldest, ancestral family includes B. petrii and B. ansorpii. From this lineage, a second family containing B. pertussis, B. parapertussis and B. bronchiseptica emerged as well as a third family that includes the remaining species. Analysis of genetic diversity within each species shows that a large number of genes were lost during the evolution of species that are restricted to one or a few hosts. In some cases, species acquired key virulence genes that subsequently contributed to their emergence as pathogens. These data greatly facilitate ongoing efforts to better understand evolution, host adaptation and virulence mechanisms of the Bordetella, potentially leading to novel diagnostic tools and vaccine approaches and improved disease prevention and management strategies.