Comparative genomics of the classical Bordetella subspecies

The evolution and exchange of virulence-associated diversity amongst closely related pathogens

Jihye Park, Ying Zhang, Anne M. Buboltz, Xuqing Zhang, Stephan C. Schuster, Umesh Ahuja, Minghsun Liu, Jeff F. Miller, Mohammed Sebaihia, Stephen D. Bentley, Julian Parkhill, Eric Thomas Harvill

Research output: Contribution to journalArticle

51 Citations (Scopus)

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.

Original languageEnglish (US)
Article number545
JournalBMC genomics
Volume13
Issue number1
DOIs
StatePublished - Oct 10 2012

Fingerprint

Bordetella
Genomics
Virulence
Genome
Host Specificity
Pertussis Toxin
Virulence Factors
Horizontal Gene Transfer
O Antigens
Point Mutation
Single Nucleotide Polymorphism
Sheep

All Science Journal Classification (ASJC) codes

  • Biotechnology
  • Genetics

Cite this

Park, Jihye ; Zhang, Ying ; Buboltz, Anne M. ; Zhang, Xuqing ; Schuster, Stephan C. ; Ahuja, Umesh ; Liu, Minghsun ; Miller, Jeff F. ; Sebaihia, Mohammed ; Bentley, Stephen D. ; Parkhill, Julian ; Harvill, Eric Thomas. / Comparative genomics of the classical Bordetella subspecies : The evolution and exchange of virulence-associated diversity amongst closely related pathogens. In: BMC genomics. 2012 ; Vol. 13, No. 1.
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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.",
author = "Jihye Park and Ying Zhang and Buboltz, {Anne M.} and Xuqing Zhang and Schuster, {Stephan C.} and Umesh Ahuja and Minghsun Liu and Miller, {Jeff F.} and Mohammed Sebaihia and Bentley, {Stephen D.} and Julian Parkhill and Harvill, {Eric Thomas}",
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Park, J, Zhang, Y, Buboltz, AM, Zhang, X, Schuster, SC, Ahuja, U, Liu, M, Miller, JF, Sebaihia, M, Bentley, SD, Parkhill, J & Harvill, ET 2012, 'Comparative genomics of the classical Bordetella subspecies: The evolution and exchange of virulence-associated diversity amongst closely related pathogens', BMC genomics, vol. 13, no. 1, 545. https://doi.org/10.1186/1471-2164-13-545

Comparative genomics of the classical Bordetella subspecies : The evolution and exchange of virulence-associated diversity amongst closely related pathogens. / Park, Jihye; Zhang, Ying; Buboltz, Anne M.; Zhang, Xuqing; Schuster, Stephan C.; Ahuja, Umesh; Liu, Minghsun; Miller, Jeff F.; Sebaihia, Mohammed; Bentley, Stephen D.; Parkhill, Julian; Harvill, Eric Thomas.

In: BMC genomics, Vol. 13, No. 1, 545, 10.10.2012.

Research output: Contribution to journalArticle

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T1 - Comparative genomics of the classical Bordetella subspecies

T2 - The evolution and exchange of virulence-associated diversity amongst closely related pathogens

AU - Park, Jihye

AU - Zhang, Ying

AU - Buboltz, Anne M.

AU - Zhang, Xuqing

AU - Schuster, Stephan C.

AU - Ahuja, Umesh

AU - Liu, Minghsun

AU - Miller, Jeff F.

AU - Sebaihia, Mohammed

AU - Bentley, Stephen D.

AU - Parkhill, Julian

AU - Harvill, Eric Thomas

PY - 2012/10/10

Y1 - 2012/10/10

N2 - 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.

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