Global Population Structure and Evolution of <named-content content-type="genus-species">Bordetella pertussis</named-content> and Their Relationship with Vaccination
ABSTRACT Bordetella pertussis causes pertussis, a respiratory disease that is most severe for infants. Vaccination was introduced in the 1950s, and in recent years, a resurgence of disease was observed worldwide, with significant mortality in infants. Possible causes for this include the switch from...
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American Society for Microbiology
2014
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oai:doaj.org-article:660166e9972641429cebdf1af2d9369b2021-11-15T15:45:13ZGlobal Population Structure and Evolution of <named-content content-type="genus-species">Bordetella pertussis</named-content> and Their Relationship with Vaccination10.1128/mBio.01074-142150-7511https://doaj.org/article/660166e9972641429cebdf1af2d9369b2014-05-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01074-14https://doaj.org/toc/2150-7511ABSTRACT Bordetella pertussis causes pertussis, a respiratory disease that is most severe for infants. Vaccination was introduced in the 1950s, and in recent years, a resurgence of disease was observed worldwide, with significant mortality in infants. Possible causes for this include the switch from whole-cell vaccines (WCVs) to less effective acellular vaccines (ACVs), waning immunity, and pathogen adaptation. Pathogen adaptation is suggested by antigenic divergence between vaccine strains and circulating strains and by the emergence of strains with increased pertussis toxin production. We applied comparative genomics to a worldwide collection of 343 B. pertussis strains isolated between 1920 and 2010. The global phylogeny showed two deep branches; the largest of these contained 98% of all strains, and its expansion correlated temporally with the first descriptions of pertussis outbreaks in Europe in the 16th century. We found little evidence of recent geographical clustering of the strains within this lineage, suggesting rapid strain flow between countries. We observed that changes in genes encoding proteins implicated in protective immunity that are included in ACVs occurred after the introduction of WCVs but before the switch to ACVs. Furthermore, our analyses consistently suggested that virulence-associated genes and genes coding for surface-exposed proteins were involved in adaptation. However, many of the putative adaptive loci identified have a physiological role, and further studies of these loci may reveal less obvious ways in which B. pertussis and the host interact. This work provides insight into ways in which pathogens may adapt to vaccination and suggests ways to improve pertussis vaccines. IMPORTANCE Whooping cough is mainly caused by Bordetella pertussis, and current vaccines are targeted against this organism. Recently, there have been increasing outbreaks of whooping cough, even where vaccine coverage is high. Analysis of the genomes of 343 B. pertussis isolates from around the world over the last 100 years suggests that the organism has emerged within the last 500 years, consistent with historical records. We show that global transmission of new strains is very rapid and that the worldwide population of B. pertussis is evolving in response to vaccine introduction, potentially enabling vaccine escape.Marieke J. BartSimon R. HarrisAbdolreza AdvaniYoshichika ArakawaDaniela BotteroValérie BouchezPamela K. CassidayChuen-Sheue ChiangTine DalbyNorman K. FryMaría Emilia GaillardMarjolein van GentNicole GuisoHans O. HallanderEric T. HarvillQiushui HeHan G. J. van der HeideKees HeuvelmanDaniela F. HozborKazunari KamachiGennady I. KarataevRuiting LanAnna LutyńskaRam P. MaharjanJussi MertsolaTatsuo MiyamuraSophie OctaviaAndrew PrestonMichael A. QuailVitali SintchenkoPaola StefanelliM. Lucia TondellaRaymond S. W. TsangYinghua XuShu-Man YaoShumin ZhangJulian ParkhillFrits R. MooiAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 5, Iss 2 (2014) |
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DOAJ |
| collection |
DOAJ |
| language |
EN |
| topic |
Microbiology QR1-502 |
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Microbiology QR1-502 Marieke J. Bart Simon R. Harris Abdolreza Advani Yoshichika Arakawa Daniela Bottero Valérie Bouchez Pamela K. Cassiday Chuen-Sheue Chiang Tine Dalby Norman K. Fry María Emilia Gaillard Marjolein van Gent Nicole Guiso Hans O. Hallander Eric T. Harvill Qiushui He Han G. J. van der Heide Kees Heuvelman Daniela F. Hozbor Kazunari Kamachi Gennady I. Karataev Ruiting Lan Anna Lutyńska Ram P. Maharjan Jussi Mertsola Tatsuo Miyamura Sophie Octavia Andrew Preston Michael A. Quail Vitali Sintchenko Paola Stefanelli M. Lucia Tondella Raymond S. W. Tsang Yinghua Xu Shu-Man Yao Shumin Zhang Julian Parkhill Frits R. Mooi Global Population Structure and Evolution of <named-content content-type="genus-species">Bordetella pertussis</named-content> and Their Relationship with Vaccination |
| description |
ABSTRACT Bordetella pertussis causes pertussis, a respiratory disease that is most severe for infants. Vaccination was introduced in the 1950s, and in recent years, a resurgence of disease was observed worldwide, with significant mortality in infants. Possible causes for this include the switch from whole-cell vaccines (WCVs) to less effective acellular vaccines (ACVs), waning immunity, and pathogen adaptation. Pathogen adaptation is suggested by antigenic divergence between vaccine strains and circulating strains and by the emergence of strains with increased pertussis toxin production. We applied comparative genomics to a worldwide collection of 343 B. pertussis strains isolated between 1920 and 2010. The global phylogeny showed two deep branches; the largest of these contained 98% of all strains, and its expansion correlated temporally with the first descriptions of pertussis outbreaks in Europe in the 16th century. We found little evidence of recent geographical clustering of the strains within this lineage, suggesting rapid strain flow between countries. We observed that changes in genes encoding proteins implicated in protective immunity that are included in ACVs occurred after the introduction of WCVs but before the switch to ACVs. Furthermore, our analyses consistently suggested that virulence-associated genes and genes coding for surface-exposed proteins were involved in adaptation. However, many of the putative adaptive loci identified have a physiological role, and further studies of these loci may reveal less obvious ways in which B. pertussis and the host interact. This work provides insight into ways in which pathogens may adapt to vaccination and suggests ways to improve pertussis vaccines. IMPORTANCE Whooping cough is mainly caused by Bordetella pertussis, and current vaccines are targeted against this organism. Recently, there have been increasing outbreaks of whooping cough, even where vaccine coverage is high. Analysis of the genomes of 343 B. pertussis isolates from around the world over the last 100 years suggests that the organism has emerged within the last 500 years, consistent with historical records. We show that global transmission of new strains is very rapid and that the worldwide population of B. pertussis is evolving in response to vaccine introduction, potentially enabling vaccine escape. |
| format |
article |
| author |
Marieke J. Bart Simon R. Harris Abdolreza Advani Yoshichika Arakawa Daniela Bottero Valérie Bouchez Pamela K. Cassiday Chuen-Sheue Chiang Tine Dalby Norman K. Fry María Emilia Gaillard Marjolein van Gent Nicole Guiso Hans O. Hallander Eric T. Harvill Qiushui He Han G. J. van der Heide Kees Heuvelman Daniela F. Hozbor Kazunari Kamachi Gennady I. Karataev Ruiting Lan Anna Lutyńska Ram P. Maharjan Jussi Mertsola Tatsuo Miyamura Sophie Octavia Andrew Preston Michael A. Quail Vitali Sintchenko Paola Stefanelli M. Lucia Tondella Raymond S. W. Tsang Yinghua Xu Shu-Man Yao Shumin Zhang Julian Parkhill Frits R. Mooi |
| author_facet |
Marieke J. Bart Simon R. Harris Abdolreza Advani Yoshichika Arakawa Daniela Bottero Valérie Bouchez Pamela K. Cassiday Chuen-Sheue Chiang Tine Dalby Norman K. Fry María Emilia Gaillard Marjolein van Gent Nicole Guiso Hans O. Hallander Eric T. Harvill Qiushui He Han G. J. van der Heide Kees Heuvelman Daniela F. Hozbor Kazunari Kamachi Gennady I. Karataev Ruiting Lan Anna Lutyńska Ram P. Maharjan Jussi Mertsola Tatsuo Miyamura Sophie Octavia Andrew Preston Michael A. Quail Vitali Sintchenko Paola Stefanelli M. Lucia Tondella Raymond S. W. Tsang Yinghua Xu Shu-Man Yao Shumin Zhang Julian Parkhill Frits R. Mooi |
| author_sort |
Marieke J. Bart |
| title |
Global Population Structure and Evolution of <named-content content-type="genus-species">Bordetella pertussis</named-content> and Their Relationship with Vaccination |
| title_short |
Global Population Structure and Evolution of <named-content content-type="genus-species">Bordetella pertussis</named-content> and Their Relationship with Vaccination |
| title_full |
Global Population Structure and Evolution of <named-content content-type="genus-species">Bordetella pertussis</named-content> and Their Relationship with Vaccination |
| title_fullStr |
Global Population Structure and Evolution of <named-content content-type="genus-species">Bordetella pertussis</named-content> and Their Relationship with Vaccination |
| title_full_unstemmed |
Global Population Structure and Evolution of <named-content content-type="genus-species">Bordetella pertussis</named-content> and Their Relationship with Vaccination |
| title_sort |
global population structure and evolution of <named-content content-type="genus-species">bordetella pertussis</named-content> and their relationship with vaccination |
| publisher |
American Society for Microbiology |
| publishDate |
2014 |
| url |
https://doaj.org/article/660166e9972641429cebdf1af2d9369b |
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