Genome Structural Diversity among 31 <named-content content-type="genus-species">Bordetella pertussis</named-content> Isolates from Two Recent U.S. Whooping Cough Statewide Epidemics

ABSTRACT During 2010 and 2012, California and Vermont, respectively, experienced statewide epidemics of pertussis with differences seen in the demographic affected, case clinical presentation, and molecular epidemiology of the circulating strains. To overcome limitations of the current molecular typ...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	Katherine E. Bowden, Michael R. Weigand, Yanhui Peng, Pamela K. Cassiday, Scott Sammons, Kristen Knipe, Lori A. Rowe, Vladimir Loparev, Mili Sheth, Keeley Weening, M. Lucia Tondella, Margaret M. Williams
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2016
Materias:	Bordetella pertussis genome rearrangements optical mapping pertactin whole-genome sequencing Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/e81a9f8423754376b7e689a964acecae
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:e81a9f8423754376b7e689a964acecae
record_format	dspace
spelling	oai:doaj.org-article:e81a9f8423754376b7e689a964acecae2021-11-15T15:21:18ZGenome Structural Diversity among 31 <named-content content-type="genus-species">Bordetella pertussis</named-content> Isolates from Two Recent U.S. Whooping Cough Statewide Epidemics10.1128/mSphere.00036-162379-5042https://doaj.org/article/e81a9f8423754376b7e689a964acecae2016-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00036-16https://doaj.org/toc/2379-5042ABSTRACT During 2010 and 2012, California and Vermont, respectively, experienced statewide epidemics of pertussis with differences seen in the demographic affected, case clinical presentation, and molecular epidemiology of the circulating strains. To overcome limitations of the current molecular typing methods for pertussis, we utilized whole-genome sequencing to gain a broader understanding of how current circulating strains are causing large epidemics. Through the use of combined next-generation sequencing technologies, this study compared de novo, single-contig genome assemblies from 31 out of 33 Bordetella pertussis isolates collected during two separate pertussis statewide epidemics and 2 resequenced vaccine strains. Final genome architecture assemblies were verified with whole-genome optical mapping. Sixteen distinct genome rearrangement profiles were observed in epidemic isolate genomes, all of which were distinct from the genome structures of the two resequenced vaccine strains. These rearrangements appear to be mediated by repetitive sequence elements, such as high-copy-number mobile genetic elements and rRNA operons. Additionally, novel and previously identified single nucleotide polymorphisms were detected in 10 virulence-related genes in the epidemic isolates. Whole-genome variation analysis identified state-specific variants, and coding regions bearing nonsynonymous mutations were classified into functional annotated orthologous groups. Comprehensive studies on whole genomes are needed to understand the resurgence of pertussis and develop novel tools to better characterize the molecular epidemiology of evolving B. pertussis populations. IMPORTANCE Pertussis, or whooping cough, is the most poorly controlled vaccine-preventable bacterial disease in the United States, which has experienced a resurgence for more than a decade. Once viewed as a monomorphic pathogen, B. pertussis strains circulating during epidemics exhibit diversity visible on a genome structural level, previously undetectable by traditional sequence analysis using short-read technologies. For the first time, we combine short- and long-read sequencing platforms with restriction optical mapping for single-contig, de novo assembly of 31 isolates to investigate two geographically and temporally independent U.S. pertussis epidemics. These complete genomes reshape our understanding of B. pertussis evolution and strengthen molecular epidemiology toward one day understanding the resurgence of pertussis.Katherine E. BowdenMichael R. WeigandYanhui PengPamela K. CassidayScott SammonsKristen KnipeLori A. RoweVladimir LoparevMili ShethKeeley WeeningM. Lucia TondellaMargaret M. WilliamsAmerican Society for MicrobiologyarticleBordetella pertussisgenome rearrangementsoptical mappingpertactinwhole-genome sequencingMicrobiologyQR1-502ENmSphere, Vol 1, Iss 3 (2016)
institution	DOAJ
collection	DOAJ
language	EN
topic	Bordetella pertussis genome rearrangements optical mapping pertactin whole-genome sequencing Microbiology QR1-502
spellingShingle	Bordetella pertussis genome rearrangements optical mapping pertactin whole-genome sequencing Microbiology QR1-502 Katherine E. Bowden Michael R. Weigand Yanhui Peng Pamela K. Cassiday Scott Sammons Kristen Knipe Lori A. Rowe Vladimir Loparev Mili Sheth Keeley Weening M. Lucia Tondella Margaret M. Williams Genome Structural Diversity among 31 <named-content content-type="genus-species">Bordetella pertussis</named-content> Isolates from Two Recent U.S. Whooping Cough Statewide Epidemics
description	ABSTRACT During 2010 and 2012, California and Vermont, respectively, experienced statewide epidemics of pertussis with differences seen in the demographic affected, case clinical presentation, and molecular epidemiology of the circulating strains. To overcome limitations of the current molecular typing methods for pertussis, we utilized whole-genome sequencing to gain a broader understanding of how current circulating strains are causing large epidemics. Through the use of combined next-generation sequencing technologies, this study compared de novo, single-contig genome assemblies from 31 out of 33 Bordetella pertussis isolates collected during two separate pertussis statewide epidemics and 2 resequenced vaccine strains. Final genome architecture assemblies were verified with whole-genome optical mapping. Sixteen distinct genome rearrangement profiles were observed in epidemic isolate genomes, all of which were distinct from the genome structures of the two resequenced vaccine strains. These rearrangements appear to be mediated by repetitive sequence elements, such as high-copy-number mobile genetic elements and rRNA operons. Additionally, novel and previously identified single nucleotide polymorphisms were detected in 10 virulence-related genes in the epidemic isolates. Whole-genome variation analysis identified state-specific variants, and coding regions bearing nonsynonymous mutations were classified into functional annotated orthologous groups. Comprehensive studies on whole genomes are needed to understand the resurgence of pertussis and develop novel tools to better characterize the molecular epidemiology of evolving B. pertussis populations. IMPORTANCE Pertussis, or whooping cough, is the most poorly controlled vaccine-preventable bacterial disease in the United States, which has experienced a resurgence for more than a decade. Once viewed as a monomorphic pathogen, B. pertussis strains circulating during epidemics exhibit diversity visible on a genome structural level, previously undetectable by traditional sequence analysis using short-read technologies. For the first time, we combine short- and long-read sequencing platforms with restriction optical mapping for single-contig, de novo assembly of 31 isolates to investigate two geographically and temporally independent U.S. pertussis epidemics. These complete genomes reshape our understanding of B. pertussis evolution and strengthen molecular epidemiology toward one day understanding the resurgence of pertussis.
format	article
author	Katherine E. Bowden Michael R. Weigand Yanhui Peng Pamela K. Cassiday Scott Sammons Kristen Knipe Lori A. Rowe Vladimir Loparev Mili Sheth Keeley Weening M. Lucia Tondella Margaret M. Williams
author_facet	Katherine E. Bowden Michael R. Weigand Yanhui Peng Pamela K. Cassiday Scott Sammons Kristen Knipe Lori A. Rowe Vladimir Loparev Mili Sheth Keeley Weening M. Lucia Tondella Margaret M. Williams
author_sort	Katherine E. Bowden
title	Genome Structural Diversity among 31 <named-content content-type="genus-species">Bordetella pertussis</named-content> Isolates from Two Recent U.S. Whooping Cough Statewide Epidemics
title_short	Genome Structural Diversity among 31 <named-content content-type="genus-species">Bordetella pertussis</named-content> Isolates from Two Recent U.S. Whooping Cough Statewide Epidemics
title_full	Genome Structural Diversity among 31 <named-content content-type="genus-species">Bordetella pertussis</named-content> Isolates from Two Recent U.S. Whooping Cough Statewide Epidemics
title_fullStr	Genome Structural Diversity among 31 <named-content content-type="genus-species">Bordetella pertussis</named-content> Isolates from Two Recent U.S. Whooping Cough Statewide Epidemics
title_full_unstemmed	Genome Structural Diversity among 31 <named-content content-type="genus-species">Bordetella pertussis</named-content> Isolates from Two Recent U.S. Whooping Cough Statewide Epidemics
title_sort	genome structural diversity among 31 <named-content content-type="genus-species">bordetella pertussis</named-content> isolates from two recent u.s. whooping cough statewide epidemics
publisher	American Society for Microbiology
publishDate	2016
url	https://doaj.org/article/e81a9f8423754376b7e689a964acecae
work_keys_str_mv	AT katherineebowden genomestructuraldiversityamong31namedcontentcontenttypegenusspeciesbordetellapertussisnamedcontentisolatesfromtworecentuswhoopingcoughstatewideepidemics AT michaelrweigand genomestructuraldiversityamong31namedcontentcontenttypegenusspeciesbordetellapertussisnamedcontentisolatesfromtworecentuswhoopingcoughstatewideepidemics AT yanhuipeng genomestructuraldiversityamong31namedcontentcontenttypegenusspeciesbordetellapertussisnamedcontentisolatesfromtworecentuswhoopingcoughstatewideepidemics AT pamelakcassiday genomestructuraldiversityamong31namedcontentcontenttypegenusspeciesbordetellapertussisnamedcontentisolatesfromtworecentuswhoopingcoughstatewideepidemics AT scottsammons genomestructuraldiversityamong31namedcontentcontenttypegenusspeciesbordetellapertussisnamedcontentisolatesfromtworecentuswhoopingcoughstatewideepidemics AT kristenknipe genomestructuraldiversityamong31namedcontentcontenttypegenusspeciesbordetellapertussisnamedcontentisolatesfromtworecentuswhoopingcoughstatewideepidemics AT loriarowe genomestructuraldiversityamong31namedcontentcontenttypegenusspeciesbordetellapertussisnamedcontentisolatesfromtworecentuswhoopingcoughstatewideepidemics AT vladimirloparev genomestructuraldiversityamong31namedcontentcontenttypegenusspeciesbordetellapertussisnamedcontentisolatesfromtworecentuswhoopingcoughstatewideepidemics AT milisheth genomestructuraldiversityamong31namedcontentcontenttypegenusspeciesbordetellapertussisnamedcontentisolatesfromtworecentuswhoopingcoughstatewideepidemics AT keeleyweening genomestructuraldiversityamong31namedcontentcontenttypegenusspeciesbordetellapertussisnamedcontentisolatesfromtworecentuswhoopingcoughstatewideepidemics AT mluciatondella genomestructuraldiversityamong31namedcontentcontenttypegenusspeciesbordetellapertussisnamedcontentisolatesfromtworecentuswhoopingcoughstatewideepidemics AT margaretmwilliams genomestructuraldiversityamong31namedcontentcontenttypegenusspeciesbordetellapertussisnamedcontentisolatesfromtworecentuswhoopingcoughstatewideepidemics
_version_	1718428164554752000

Genome Structural Diversity among 31 <named-content content-type="genus-species">Bordetella pertussis</named-content> Isolates from Two Recent U.S. Whooping Cough Statewide Epidemics

Ejemplares similares