Conserved Patterns of Symmetric Inversion in the Genome Evolution of <italic toggle="yes">Bordetella</italic> Respiratory Pathogens

ABSTRACT Whooping cough (pertussis), primarily caused by Bordetella pertussis, has resurged in the United States, and circulating strains exhibit considerable chromosome structural fluidity in the form of rearrangement and deletion. The genus Bordetella includes additional pathogenic species infecti...

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Autores principales:	Michael R. Weigand, Yanhui Peng, Dhwani Batra, Mark Burroughs, Jamie K. Davis, Kristen Knipe, Vladimir N. Loparev, Taccara Johnson, Phalasy Juieng, Lori A. Rowe, Mili Sheth, Kevin Tang, Yvette Unoarumhi, Margaret M. Williams, M. Lucia Tondella
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	Bordetella pertussis whooping cough evolution genomics insertion sequence Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/a4bbcdce59d1483ca35b49207d91c288
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spelling	oai:doaj.org-article:a4bbcdce59d1483ca35b49207d91c2882021-12-02T18:15:44ZConserved Patterns of Symmetric Inversion in the Genome Evolution of <italic toggle="yes">Bordetella</italic> Respiratory Pathogens10.1128/mSystems.00702-192379-5077https://doaj.org/article/a4bbcdce59d1483ca35b49207d91c2882019-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00702-19https://doaj.org/toc/2379-5077ABSTRACT Whooping cough (pertussis), primarily caused by Bordetella pertussis, has resurged in the United States, and circulating strains exhibit considerable chromosome structural fluidity in the form of rearrangement and deletion. The genus Bordetella includes additional pathogenic species infecting various animals, some even causing pertussis-like respiratory disease in humans; however, investigation of their genome evolution has been limited. We studied chromosome structure in complete genome sequences from 167 Bordetella species isolates, as well as 469 B. pertussis isolates, to gain a generalized understanding of rearrangement patterns among these related pathogens. Observed changes in gene order primarily resulted from large inversions and were only detected in species with genomes harboring multicopy insertion sequence (IS) elements, most notably B. holmesii and B. parapertussis. While genomes of B. pertussis contain >240 copies of IS481, IS elements appear less numerous in other species and yield less chromosome structural diversity through rearrangement. These data were further used to predict all possible rearrangements between IS element copies present in Bordetella genomes, revealing that only a subset is observed among circulating strains. Therefore, while it appears that rearrangement occurs less frequently in other species than in B. pertussis, these clinically relevant respiratory pathogens likely experience similar mutation of gene order. The resulting chromosome structural fluidity presents both challenges and opportunity for the study of Bordetella respiratory pathogens. IMPORTANCE Bordetella pertussis is the primary agent of whooping cough (pertussis). The Bordetella genus includes additional pathogens of animals and humans, including some that cause pertussis-like respiratory illness. The chromosome of B. pertussis has previously been shown to exhibit considerable structural rearrangement, but insufficient data have prevented comparable investigation in related species. In this study, we analyze chromosome structure variation in several Bordetella species to gain a generalized understanding of rearrangement patterns in this genus. Just as in B. pertussis, we observed inversions in other species that likely result from common mutational processes. We used these data to further predict additional, unobserved inversions, suggesting that specific genome structures may be preferred in each species.Michael R. WeigandYanhui PengDhwani BatraMark BurroughsJamie K. DavisKristen KnipeVladimir N. LoparevTaccara JohnsonPhalasy JuiengLori A. RoweMili ShethKevin TangYvette UnoarumhiMargaret M. WilliamsM. Lucia TondellaAmerican Society for MicrobiologyarticleBordetellapertussiswhooping coughevolutiongenomicsinsertion sequenceMicrobiologyQR1-502ENmSystems, Vol 4, Iss 6 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	Bordetella pertussis whooping cough evolution genomics insertion sequence Microbiology QR1-502
spellingShingle	Bordetella pertussis whooping cough evolution genomics insertion sequence Microbiology QR1-502 Michael R. Weigand Yanhui Peng Dhwani Batra Mark Burroughs Jamie K. Davis Kristen Knipe Vladimir N. Loparev Taccara Johnson Phalasy Juieng Lori A. Rowe Mili Sheth Kevin Tang Yvette Unoarumhi Margaret M. Williams M. Lucia Tondella Conserved Patterns of Symmetric Inversion in the Genome Evolution of <italic toggle="yes">Bordetella</italic> Respiratory Pathogens
description	ABSTRACT Whooping cough (pertussis), primarily caused by Bordetella pertussis, has resurged in the United States, and circulating strains exhibit considerable chromosome structural fluidity in the form of rearrangement and deletion. The genus Bordetella includes additional pathogenic species infecting various animals, some even causing pertussis-like respiratory disease in humans; however, investigation of their genome evolution has been limited. We studied chromosome structure in complete genome sequences from 167 Bordetella species isolates, as well as 469 B. pertussis isolates, to gain a generalized understanding of rearrangement patterns among these related pathogens. Observed changes in gene order primarily resulted from large inversions and were only detected in species with genomes harboring multicopy insertion sequence (IS) elements, most notably B. holmesii and B. parapertussis. While genomes of B. pertussis contain >240 copies of IS481, IS elements appear less numerous in other species and yield less chromosome structural diversity through rearrangement. These data were further used to predict all possible rearrangements between IS element copies present in Bordetella genomes, revealing that only a subset is observed among circulating strains. Therefore, while it appears that rearrangement occurs less frequently in other species than in B. pertussis, these clinically relevant respiratory pathogens likely experience similar mutation of gene order. The resulting chromosome structural fluidity presents both challenges and opportunity for the study of Bordetella respiratory pathogens. IMPORTANCE Bordetella pertussis is the primary agent of whooping cough (pertussis). The Bordetella genus includes additional pathogens of animals and humans, including some that cause pertussis-like respiratory illness. The chromosome of B. pertussis has previously been shown to exhibit considerable structural rearrangement, but insufficient data have prevented comparable investigation in related species. In this study, we analyze chromosome structure variation in several Bordetella species to gain a generalized understanding of rearrangement patterns in this genus. Just as in B. pertussis, we observed inversions in other species that likely result from common mutational processes. We used these data to further predict additional, unobserved inversions, suggesting that specific genome structures may be preferred in each species.
format	article
author	Michael R. Weigand Yanhui Peng Dhwani Batra Mark Burroughs Jamie K. Davis Kristen Knipe Vladimir N. Loparev Taccara Johnson Phalasy Juieng Lori A. Rowe Mili Sheth Kevin Tang Yvette Unoarumhi Margaret M. Williams M. Lucia Tondella
author_facet	Michael R. Weigand Yanhui Peng Dhwani Batra Mark Burroughs Jamie K. Davis Kristen Knipe Vladimir N. Loparev Taccara Johnson Phalasy Juieng Lori A. Rowe Mili Sheth Kevin Tang Yvette Unoarumhi Margaret M. Williams M. Lucia Tondella
author_sort	Michael R. Weigand
title	Conserved Patterns of Symmetric Inversion in the Genome Evolution of <italic toggle="yes">Bordetella</italic> Respiratory Pathogens
title_short	Conserved Patterns of Symmetric Inversion in the Genome Evolution of <italic toggle="yes">Bordetella</italic> Respiratory Pathogens
title_full	Conserved Patterns of Symmetric Inversion in the Genome Evolution of <italic toggle="yes">Bordetella</italic> Respiratory Pathogens
title_fullStr	Conserved Patterns of Symmetric Inversion in the Genome Evolution of <italic toggle="yes">Bordetella</italic> Respiratory Pathogens
title_full_unstemmed	Conserved Patterns of Symmetric Inversion in the Genome Evolution of <italic toggle="yes">Bordetella</italic> Respiratory Pathogens
title_sort	conserved patterns of symmetric inversion in the genome evolution of <italic toggle="yes">bordetella</italic> respiratory pathogens
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/a4bbcdce59d1483ca35b49207d91c288
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Conserved Patterns of Symmetric Inversion in the Genome Evolution of <italic toggle="yes">Bordetella</italic> Respiratory Pathogens

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