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Volume 11, Issue 11

No innocent bystanders: pertussis vaccination and evolutionary parallelisms between and Open Access

Abstract

Pathogens adapting to the human host and to vaccination-induced immunity may follow parallel evolutionary paths. () contributes significantly to the burden of whooping cough (pertussis) and shares vaccine antigens with ; both pathogens are phylogenetically related and ecological competitors. vaccine antigen-coding genes have accumulated variation, including pertactin (PRN) disruptions, after the introduction of acellular vaccines in the 1990s. We aimed to evaluate evolutionary parallelisms in , even though pertussis vaccines were designed against . We sequenced 242 isolates collected in France, the USA and Spain between 1937 and 2019, spanning pre-vaccine and two vaccines eras. We investigated the temporal evolution of sublineages using a Bayesian approach based on whole-genome SNPs and performed comparative genomic analyses focusing on antigen and virulence gene loci. The most recent common ancestor of all sequenced isolates was estimated around the year 1877, making it one of the youngest human pathogens, and the evolutionary rate we estimated (2.12×10 substitutions per site per year) was remarkably similar to the one previously reported for (2.24×10). PRN antigen deficiency in was driven by 18 disruptive mutations, including deletion :ΔG-1895 estimated to have occurred around 1998 and observed in 73.8 % (149/202) of post-2007 isolates. In addition, we detected two early (year ~1900) mutations in the A- intergenic region, which controls multiple virulence factors including the filamentous haemagglutinin antigen. Gene clusters for pertussis toxin and fimbriae showed a surprising lack of gene decay. Our findings suggest early adaptation of to humans through modulation of the regulon, and a rapid adaptation through the loss of PRN expression, representing a late evolutionary parallelism concomitant with acellular vaccination against whooping cough.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): Bordetella parapertussis , phylogenetic diversity , vaccine driven evolution and virulence factors
Funding
This study was supported by the:
  • Spanish “Ministerio de Economía y Competitividad” and “Instituto de Salud Carlos III” (Award FIS PI18/00703)
    • Principal Award Recipient: JuanJosé González-López
  • French Government’s Investissement d’Avenir grants (Award ANR-10-LABX-62-IBEID)
    • Principal Award Recipient: SylvainBrisse
© 2025 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
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2025-12-16

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No innocent bystanders: pertussis vaccination and evolutionary parallelisms between Bordetella parapertussis and Bordetella pertussis
M Gen 11, 001544 (2025); https://doi.org/10.1099/mgen.0.001544
/content/journal/mgen/10.1099/mgen.0.001544
/content/journal/mgen/10.1099/mgen.0.001544
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