DNA Supercoiling Regulates the Motility of <named-content content-type="genus-species">Campylobacter jejuni</named-content> and Is Altered by Growth in the Presence of Chicken Mucus

ABSTRACT Campylobacter jejuni is the leading cause of bacterial gastroenteritis in humans, but relatively little is known about the global regulation of virulence factors during infection of chickens or humans. This study identified DNA supercoiling as playing a key role in regulating motility and f...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	Claire Shortt, Eoin Scanlan, Amber Hilliard, Chiara E. Cotroneo, Billy Bourke, Tadhg Ó Cróinín
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2016
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/88e298e9558549e089701a887acc5617
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:88e298e9558549e089701a887acc5617
record_format	dspace
spelling	oai:doaj.org-article:88e298e9558549e089701a887acc56172021-11-15T15:50:15ZDNA Supercoiling Regulates the Motility of <named-content content-type="genus-species">Campylobacter jejuni</named-content> and Is Altered by Growth in the Presence of Chicken Mucus10.1128/mBio.01227-162150-7511https://doaj.org/article/88e298e9558549e089701a887acc56172016-11-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01227-16https://doaj.org/toc/2150-7511ABSTRACT Campylobacter jejuni is the leading cause of bacterial gastroenteritis in humans, but relatively little is known about the global regulation of virulence factors during infection of chickens or humans. This study identified DNA supercoiling as playing a key role in regulating motility and flagellar protein production and found that this supercoiling-controlled regulon is induced by growth in chicken mucus. A direct correlation was observed between motility and resting DNA supercoiling levels in different strains of C. jejuni, and relaxation of DNA supercoiling resulted in decreased motility. Transcriptional analysis and Western immunoblotting revealed that a reduction in motility and DNA supercoiling affected the two-component regulatory system FlgRS and was associated with reduced FlgR expression, increased FlgS expression, and aberrant expression of flagellin subunits. Electron microscopy revealed that the flagellar structure remained intact. Growth in the presence of porcine mucin resulted in increased negative supercoiling, increased motility, increased FlgR expression, and reduced FlgS expression. Finally, this supercoiling-dependent regulon was shown to be induced by growth in chicken mucus, and the level of activation was dependent on the source of the mucus from within the chicken intestinal tract. In conclusion, this study reports for the first time the key role played by DNA supercoiling in regulating motility in C. jejuni and indicates that the induction of this supercoiling-induced regulon in response to mucus from different sources could play a critical role in regulating motility in vivo. IMPORTANCE Although Campylobacter jejuni is the leading cause of bacterial gastroenteritis, very little is understood about how this pathogen controls the expression of genes involved in causing disease. This study for the first time identifies DNA supercoiling as a key regulator of motility in C. jejuni, which is essential for both pathogenesis and colonization. Altering the level of DNA supercoiling results in changes in motility levels, as well as changes in the expression of genes involved in flagellar gene regulation. Furthermore, spontaneous clones of the organism with different motility profiles have altered DNA supercoiling levels. Finally, mucus was identified as a key stimulator of changes in DNA supercoiling, and it was shown that mucus from different sites in the chicken intestine induced different levels of DNA supercoiling. In conclusion, this study implicates DNA supercoiling as a key regulator of motility in C. jejuni in vivo during colonization of the mucus layer.Claire ShorttEoin ScanlanAmber HilliardChiara E. CotroneoBilly BourkeTadhg Ó CróinínAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 7, Iss 5 (2016)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Claire Shortt Eoin Scanlan Amber Hilliard Chiara E. Cotroneo Billy Bourke Tadhg Ó Cróinín DNA Supercoiling Regulates the Motility of <named-content content-type="genus-species">Campylobacter jejuni</named-content> and Is Altered by Growth in the Presence of Chicken Mucus
description	ABSTRACT Campylobacter jejuni is the leading cause of bacterial gastroenteritis in humans, but relatively little is known about the global regulation of virulence factors during infection of chickens or humans. This study identified DNA supercoiling as playing a key role in regulating motility and flagellar protein production and found that this supercoiling-controlled regulon is induced by growth in chicken mucus. A direct correlation was observed between motility and resting DNA supercoiling levels in different strains of C. jejuni, and relaxation of DNA supercoiling resulted in decreased motility. Transcriptional analysis and Western immunoblotting revealed that a reduction in motility and DNA supercoiling affected the two-component regulatory system FlgRS and was associated with reduced FlgR expression, increased FlgS expression, and aberrant expression of flagellin subunits. Electron microscopy revealed that the flagellar structure remained intact. Growth in the presence of porcine mucin resulted in increased negative supercoiling, increased motility, increased FlgR expression, and reduced FlgS expression. Finally, this supercoiling-dependent regulon was shown to be induced by growth in chicken mucus, and the level of activation was dependent on the source of the mucus from within the chicken intestinal tract. In conclusion, this study reports for the first time the key role played by DNA supercoiling in regulating motility in C. jejuni and indicates that the induction of this supercoiling-induced regulon in response to mucus from different sources could play a critical role in regulating motility in vivo. IMPORTANCE Although Campylobacter jejuni is the leading cause of bacterial gastroenteritis, very little is understood about how this pathogen controls the expression of genes involved in causing disease. This study for the first time identifies DNA supercoiling as a key regulator of motility in C. jejuni, which is essential for both pathogenesis and colonization. Altering the level of DNA supercoiling results in changes in motility levels, as well as changes in the expression of genes involved in flagellar gene regulation. Furthermore, spontaneous clones of the organism with different motility profiles have altered DNA supercoiling levels. Finally, mucus was identified as a key stimulator of changes in DNA supercoiling, and it was shown that mucus from different sites in the chicken intestine induced different levels of DNA supercoiling. In conclusion, this study implicates DNA supercoiling as a key regulator of motility in C. jejuni in vivo during colonization of the mucus layer.
format	article
author	Claire Shortt Eoin Scanlan Amber Hilliard Chiara E. Cotroneo Billy Bourke Tadhg Ó Cróinín
author_facet	Claire Shortt Eoin Scanlan Amber Hilliard Chiara E. Cotroneo Billy Bourke Tadhg Ó Cróinín
author_sort	Claire Shortt
title	DNA Supercoiling Regulates the Motility of <named-content content-type="genus-species">Campylobacter jejuni</named-content> and Is Altered by Growth in the Presence of Chicken Mucus
title_short	DNA Supercoiling Regulates the Motility of <named-content content-type="genus-species">Campylobacter jejuni</named-content> and Is Altered by Growth in the Presence of Chicken Mucus
title_full	DNA Supercoiling Regulates the Motility of <named-content content-type="genus-species">Campylobacter jejuni</named-content> and Is Altered by Growth in the Presence of Chicken Mucus
title_fullStr	DNA Supercoiling Regulates the Motility of <named-content content-type="genus-species">Campylobacter jejuni</named-content> and Is Altered by Growth in the Presence of Chicken Mucus
title_full_unstemmed	DNA Supercoiling Regulates the Motility of <named-content content-type="genus-species">Campylobacter jejuni</named-content> and Is Altered by Growth in the Presence of Chicken Mucus
title_sort	dna supercoiling regulates the motility of <named-content content-type="genus-species">campylobacter jejuni</named-content> and is altered by growth in the presence of chicken mucus
publisher	American Society for Microbiology
publishDate	2016
url	https://doaj.org/article/88e298e9558549e089701a887acc5617
work_keys_str_mv	AT claireshortt dnasupercoilingregulatesthemotilityofnamedcontentcontenttypegenusspeciescampylobacterjejuninamedcontentandisalteredbygrowthinthepresenceofchickenmucus AT eoinscanlan dnasupercoilingregulatesthemotilityofnamedcontentcontenttypegenusspeciescampylobacterjejuninamedcontentandisalteredbygrowthinthepresenceofchickenmucus AT amberhilliard dnasupercoilingregulatesthemotilityofnamedcontentcontenttypegenusspeciescampylobacterjejuninamedcontentandisalteredbygrowthinthepresenceofchickenmucus AT chiaraecotroneo dnasupercoilingregulatesthemotilityofnamedcontentcontenttypegenusspeciescampylobacterjejuninamedcontentandisalteredbygrowthinthepresenceofchickenmucus AT billybourke dnasupercoilingregulatesthemotilityofnamedcontentcontenttypegenusspeciescampylobacterjejuninamedcontentandisalteredbygrowthinthepresenceofchickenmucus AT tadhgocroinin dnasupercoilingregulatesthemotilityofnamedcontentcontenttypegenusspeciescampylobacterjejuninamedcontentandisalteredbygrowthinthepresenceofchickenmucus
_version_	1718427470654341120

DNA Supercoiling Regulates the Motility of <named-content content-type="genus-species">Campylobacter jejuni</named-content> and Is Altered by Growth in the Presence of Chicken Mucus

Ejemplares similares