<named-content content-type="genus-species">Bordetella pertussis</named-content> Can Be Motile and Express Flagellum-Like Structures

ABSTRACT Bordetella bronchiseptica encodes and expresses a flagellar apparatus. In contrast, Bordetella pertussis, the causative agent of whooping cough, has historically been described as a nonmotile and nonflagellated organism. The previous statements that B. pertussis was a nonmotile organism wer...

Descripción completa

Guardado en:
Detalles Bibliográficos
Autores principales: Casandra L. Hoffman, Laura A. Gonyar, Federico Zacca, Federico Sisti, Julieta Fernandez, Ting Wong, F. Heath Damron, Erik L. Hewlett
Formato: article
Lenguaje:EN
Publicado: American Society for Microbiology 2019
Materias:
Acceso en línea:https://doaj.org/article/1f505fedf6fa4c678b7d10fb7bca2872
Etiquetas: Agregar Etiqueta
Sin Etiquetas, Sea el primero en etiquetar este registro!
id oai:doaj.org-article:1f505fedf6fa4c678b7d10fb7bca2872
record_format dspace
spelling oai:doaj.org-article:1f505fedf6fa4c678b7d10fb7bca28722021-11-15T15:55:25Z<named-content content-type="genus-species">Bordetella pertussis</named-content> Can Be Motile and Express Flagellum-Like Structures10.1128/mBio.00787-192150-7511https://doaj.org/article/1f505fedf6fa4c678b7d10fb7bca28722019-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00787-19https://doaj.org/toc/2150-7511ABSTRACT Bordetella bronchiseptica encodes and expresses a flagellar apparatus. In contrast, Bordetella pertussis, the causative agent of whooping cough, has historically been described as a nonmotile and nonflagellated organism. The previous statements that B. pertussis was a nonmotile organism were consistent with a stop codon located in the flagellar biosynthesis gene, flhA, discovered when the B. pertussis Tohama I genome was sequenced and analyzed by Parkhill et al. in 2003 (J. Parkhill, M. Sebaihia, A. Preston, L. D. Murphy, et al., Nat Genet, 35:32–40, 2003, https://doi.org/10.1038/ng1227). The stop codon has subsequently been found in all annotated genomes. Parkhill et al. also showed, however, that B. pertussis contains all genetic material required for flagellar synthesis and function. We and others have determined by various transcriptomic analyses that these flagellar genes are differentially regulated under a variety of B. pertussis growth conditions. In light of these data, we tested for B. pertussis motility and found that both laboratory-adapted strains and clinical isolates can be motile. Upon isolation of motile B. pertussis, we discovered flagellum-like structures on the surface of the bacteria. B. pertussis motility appears to occur primarily in the Bvg(−) phase, consistent with regulation present in B. bronchiseptica. Motility can also be induced by the presence of fetal bovine serum. These observations demonstrate that B. pertussis can express flagellum-like structures, and although it remains to be determined if B. pertussis expresses flagella during infection or if motility and/or flagella play roles during the cycle of infection and transmission, it is clear that these data warrant further investigation. IMPORTANCE This report provides evidence for motility and expression of flagella by B. pertussis, a bacterium that has been reported as nonmotile since it was first isolated and studied. As with B. bronchiseptica, B. pertussis cells can express and assemble a flagellum-like structure on their surface, which in other organisms has been implicated in several important processes that occur in vivo. The discovery that B. pertussis is motile raises many questions, including those regarding the mechanisms of regulation for flagellar gene and protein expression and, importantly, the role of flagella during infection. This novel observation provides a foundation for further study of Bordetella flagella and motility in the contexts of infection and transmission.Casandra L. HoffmanLaura A. GonyarFederico ZaccaFederico SistiJulieta FernandezTing WongF. Heath DamronErik L. HewlettAmerican Society for MicrobiologyarticleBordetellaBordetella bronchisepticaBordetella pertussisflagellaflagellar motilityflagellar structureMicrobiologyQR1-502ENmBio, Vol 10, Iss 3 (2019)
institution DOAJ
collection DOAJ
language EN
topic Bordetella
Bordetella bronchiseptica
Bordetella pertussis
flagella
flagellar motility
flagellar structure
Microbiology
QR1-502
spellingShingle Bordetella
Bordetella bronchiseptica
Bordetella pertussis
flagella
flagellar motility
flagellar structure
Microbiology
QR1-502
Casandra L. Hoffman
Laura A. Gonyar
Federico Zacca
Federico Sisti
Julieta Fernandez
Ting Wong
F. Heath Damron
Erik L. Hewlett
<named-content content-type="genus-species">Bordetella pertussis</named-content> Can Be Motile and Express Flagellum-Like Structures
description ABSTRACT Bordetella bronchiseptica encodes and expresses a flagellar apparatus. In contrast, Bordetella pertussis, the causative agent of whooping cough, has historically been described as a nonmotile and nonflagellated organism. The previous statements that B. pertussis was a nonmotile organism were consistent with a stop codon located in the flagellar biosynthesis gene, flhA, discovered when the B. pertussis Tohama I genome was sequenced and analyzed by Parkhill et al. in 2003 (J. Parkhill, M. Sebaihia, A. Preston, L. D. Murphy, et al., Nat Genet, 35:32–40, 2003, https://doi.org/10.1038/ng1227). The stop codon has subsequently been found in all annotated genomes. Parkhill et al. also showed, however, that B. pertussis contains all genetic material required for flagellar synthesis and function. We and others have determined by various transcriptomic analyses that these flagellar genes are differentially regulated under a variety of B. pertussis growth conditions. In light of these data, we tested for B. pertussis motility and found that both laboratory-adapted strains and clinical isolates can be motile. Upon isolation of motile B. pertussis, we discovered flagellum-like structures on the surface of the bacteria. B. pertussis motility appears to occur primarily in the Bvg(−) phase, consistent with regulation present in B. bronchiseptica. Motility can also be induced by the presence of fetal bovine serum. These observations demonstrate that B. pertussis can express flagellum-like structures, and although it remains to be determined if B. pertussis expresses flagella during infection or if motility and/or flagella play roles during the cycle of infection and transmission, it is clear that these data warrant further investigation. IMPORTANCE This report provides evidence for motility and expression of flagella by B. pertussis, a bacterium that has been reported as nonmotile since it was first isolated and studied. As with B. bronchiseptica, B. pertussis cells can express and assemble a flagellum-like structure on their surface, which in other organisms has been implicated in several important processes that occur in vivo. The discovery that B. pertussis is motile raises many questions, including those regarding the mechanisms of regulation for flagellar gene and protein expression and, importantly, the role of flagella during infection. This novel observation provides a foundation for further study of Bordetella flagella and motility in the contexts of infection and transmission.
format article
author Casandra L. Hoffman
Laura A. Gonyar
Federico Zacca
Federico Sisti
Julieta Fernandez
Ting Wong
F. Heath Damron
Erik L. Hewlett
author_facet Casandra L. Hoffman
Laura A. Gonyar
Federico Zacca
Federico Sisti
Julieta Fernandez
Ting Wong
F. Heath Damron
Erik L. Hewlett
author_sort Casandra L. Hoffman
title <named-content content-type="genus-species">Bordetella pertussis</named-content> Can Be Motile and Express Flagellum-Like Structures
title_short <named-content content-type="genus-species">Bordetella pertussis</named-content> Can Be Motile and Express Flagellum-Like Structures
title_full <named-content content-type="genus-species">Bordetella pertussis</named-content> Can Be Motile and Express Flagellum-Like Structures
title_fullStr <named-content content-type="genus-species">Bordetella pertussis</named-content> Can Be Motile and Express Flagellum-Like Structures
title_full_unstemmed <named-content content-type="genus-species">Bordetella pertussis</named-content> Can Be Motile and Express Flagellum-Like Structures
title_sort <named-content content-type="genus-species">bordetella pertussis</named-content> can be motile and express flagellum-like structures
publisher American Society for Microbiology
publishDate 2019
url https://doaj.org/article/1f505fedf6fa4c678b7d10fb7bca2872
work_keys_str_mv AT casandralhoffman namedcontentcontenttypegenusspeciesbordetellapertussisnamedcontentcanbemotileandexpressflagellumlikestructures
AT lauraagonyar namedcontentcontenttypegenusspeciesbordetellapertussisnamedcontentcanbemotileandexpressflagellumlikestructures
AT federicozacca namedcontentcontenttypegenusspeciesbordetellapertussisnamedcontentcanbemotileandexpressflagellumlikestructures
AT federicosisti namedcontentcontenttypegenusspeciesbordetellapertussisnamedcontentcanbemotileandexpressflagellumlikestructures
AT julietafernandez namedcontentcontenttypegenusspeciesbordetellapertussisnamedcontentcanbemotileandexpressflagellumlikestructures
AT tingwong namedcontentcontenttypegenusspeciesbordetellapertussisnamedcontentcanbemotileandexpressflagellumlikestructures
AT fheathdamron namedcontentcontenttypegenusspeciesbordetellapertussisnamedcontentcanbemotileandexpressflagellumlikestructures
AT eriklhewlett namedcontentcontenttypegenusspeciesbordetellapertussisnamedcontentcanbemotileandexpressflagellumlikestructures
_version_ 1718427139064201216