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Open Access Highly Accessed Research article

Comparative genomics of the classical Bordetella subspecies: the evolution and exchange of virulence-associated diversity amongst closely related pathogens

Jihye Park12, Ying Zhang1, Anne M Buboltz13, Xuqing Zhang14, Stephan C Schuster37, Umesh Ahuja5, Minghsun Liu5, Jeff F Miller5, Mohammed Sebaihia68, Stephen D Bentley6, Julian Parkhill6 and Eric T Harvill1*

Author Affiliations

1 Department of Veterinary and Biomedical Sciences, The Pennsylvania State University, University Park, PA, USA

2 Graduate Program in Bioinformatics and Genomics, The Pennsylvania State University, University Park, PA, USA

3 Department of Biochemistry and Molecular Biology, The Pennsylvania State University, 310 Wartik Laboratory, University Park, PA, USA

4 Graduate Program in Genetics, The Pennsylvania State University, University Park, PA, USA

5 Department of Microbiology, Immunology and Molecular Genetics, University of California, Los Angeles, CA, USA

6 Wellcome Trust Sanger Institute Hinxton, Cambridge, UK

7 Singapore Centre on Environmental Life Sciences Engineering, Nanyang Technical University, Nanyang, Singapore

8 Department of Biology, University Hassiba Ben-Bouali de Chlef, Chlef, Algeria

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BMC Genomics 2012, 13:545  doi:10.1186/1471-2164-13-545

Published: 10 October 2012

Abstract

Background

The classical Bordetella subspecies are phylogenetically closely related, yet differ in some of the most interesting and important characteristics of pathogens, such as host range, virulence and persistence. The compelling picture from previous comparisons of the three sequenced genomes was of genome degradation, with substantial loss of genome content (up to 24%) associated with adaptation to humans.

Results

For a more comprehensive picture of lineage evolution, we employed comparative genomic and phylogenomic analyses using seven additional diverse, newly sequenced Bordetella isolates. Genome-wide single nucleotide polymorphism (SNP) analysis supports a reevaluation of the phylogenetic relationships between the classical Bordetella subspecies, and suggests a closer link between ovine and human B. parapertussis lineages than has been previously proposed. Comparative analyses of genome content revealed that only 50% of the pan-genome is conserved in all strains, reflecting substantial diversity of genome content in these closely related pathogens that may relate to their different host ranges, virulence and persistence characteristics. Strikingly, these analyses suggest possible horizontal gene transfer (HGT) events in multiple loci encoding virulence factors, including O-antigen and pertussis toxin (Ptx). Segments of the pertussis toxin locus (ptx) and its secretion system locus (ptl) appear to have been acquired by the classical Bordetella subspecies and are divergent in different lineages, suggesting functional divergence in the classical Bordetellae.

Conclusions

Together, these observations, especially in key virulence factors, reveal that multiple mechanisms, such as point mutations, gain or loss of genes, as well as HGTs, contribute to the substantial phenotypic diversity of these versatile subspecies in various hosts.

Keywords:
Genome; Bordetella; SNP; Pan-genome; Virulence; Evolution; Horizontal gene transfer; Host adaptation; Pertussis toxin