Flagellum-Mediated Mechanosensing and RflP Control Motility State of Pathogenic <named-content content-type="genus-species">Escherichia coli</named-content>

ABSTRACT Bacterial flagellar motility plays an important role in many processes that occur at surfaces or in hydrogels, including adhesion, biofilm formation, and bacterium-host interactions. Consequently, expression of flagellar genes, as well as genes involved in biofilm formation and virulence, c...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	Leanid Laganenka, María Esteban López, Remy Colin, Victor Sourjik
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	Escherichia coli bacterial physiology flagellar gene regulation flagellar motility mechanosensing virulence Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/beb1adf3c43840e792e1c88a2c06b683
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:beb1adf3c43840e792e1c88a2c06b683
record_format	dspace
spelling	oai:doaj.org-article:beb1adf3c43840e792e1c88a2c06b6832021-11-15T15:57:03ZFlagellum-Mediated Mechanosensing and RflP Control Motility State of Pathogenic <named-content content-type="genus-species">Escherichia coli</named-content>10.1128/mBio.02269-192150-7511https://doaj.org/article/beb1adf3c43840e792e1c88a2c06b6832020-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02269-19https://doaj.org/toc/2150-7511ABSTRACT Bacterial flagellar motility plays an important role in many processes that occur at surfaces or in hydrogels, including adhesion, biofilm formation, and bacterium-host interactions. Consequently, expression of flagellar genes, as well as genes involved in biofilm formation and virulence, can be regulated by the surface contact. In a few bacterial species, flagella themselves are known to serve as mechanosensors, where an increased load on flagella experienced during surface contact or swimming in viscous media controls gene expression. In this study, we show that gene regulation by motility-dependent mechanosensing is common among pathogenic Escherichia coli strains. This regulatory mechanism requires flagellar rotation, and it enables pathogenic E. coli to repress flagellar genes at low loads in liquid culture, while activating motility in porous medium (soft agar) or upon surface contact. It also controls several other cellular functions, including metabolism and signaling. The mechanosensing response in pathogenic E. coli depends on the negative regulator of motility, RflP (YdiV), which inhibits basal expression of flagellar genes in liquid. While no conditional inhibition of flagellar gene expression in liquid and therefore no upregulation in porous medium was observed in the wild-type commensal or laboratory strains of E. coli, mechanosensitive regulation could be recovered by overexpression of RflP in the laboratory strain. We hypothesize that this conditional activation of flagellar genes in pathogenic E. coli reflects adaptation to the dual role played by flagella and motility during infection. IMPORTANCE Flagella and motility are widespread virulence factors among pathogenic bacteria. Motility enhances the initial host colonization, but the flagellum is a major antigen targeted by the host immune system. Here, we demonstrate that pathogenic E. coli strains employ a mechanosensory function of the flagellar motor to activate flagellar expression under high loads, while repressing it in liquid culture. We hypothesize that this mechanism allows pathogenic E. coli to regulate its motility dependent on the stage of infection, activating flagellar expression upon initial contact with the host epithelium, when motility is beneficial, but reducing it within the host to delay the immune response.Leanid LaganenkaMaría Esteban LópezRemy ColinVictor SourjikAmerican Society for MicrobiologyarticleEscherichia colibacterial physiologyflagellar gene regulationflagellar motilitymechanosensingvirulenceMicrobiologyQR1-502ENmBio, Vol 11, Iss 2 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	Escherichia coli bacterial physiology flagellar gene regulation flagellar motility mechanosensing virulence Microbiology QR1-502
spellingShingle	Escherichia coli bacterial physiology flagellar gene regulation flagellar motility mechanosensing virulence Microbiology QR1-502 Leanid Laganenka María Esteban López Remy Colin Victor Sourjik Flagellum-Mediated Mechanosensing and RflP Control Motility State of Pathogenic <named-content content-type="genus-species">Escherichia coli</named-content>
description	ABSTRACT Bacterial flagellar motility plays an important role in many processes that occur at surfaces or in hydrogels, including adhesion, biofilm formation, and bacterium-host interactions. Consequently, expression of flagellar genes, as well as genes involved in biofilm formation and virulence, can be regulated by the surface contact. In a few bacterial species, flagella themselves are known to serve as mechanosensors, where an increased load on flagella experienced during surface contact or swimming in viscous media controls gene expression. In this study, we show that gene regulation by motility-dependent mechanosensing is common among pathogenic Escherichia coli strains. This regulatory mechanism requires flagellar rotation, and it enables pathogenic E. coli to repress flagellar genes at low loads in liquid culture, while activating motility in porous medium (soft agar) or upon surface contact. It also controls several other cellular functions, including metabolism and signaling. The mechanosensing response in pathogenic E. coli depends on the negative regulator of motility, RflP (YdiV), which inhibits basal expression of flagellar genes in liquid. While no conditional inhibition of flagellar gene expression in liquid and therefore no upregulation in porous medium was observed in the wild-type commensal or laboratory strains of E. coli, mechanosensitive regulation could be recovered by overexpression of RflP in the laboratory strain. We hypothesize that this conditional activation of flagellar genes in pathogenic E. coli reflects adaptation to the dual role played by flagella and motility during infection. IMPORTANCE Flagella and motility are widespread virulence factors among pathogenic bacteria. Motility enhances the initial host colonization, but the flagellum is a major antigen targeted by the host immune system. Here, we demonstrate that pathogenic E. coli strains employ a mechanosensory function of the flagellar motor to activate flagellar expression under high loads, while repressing it in liquid culture. We hypothesize that this mechanism allows pathogenic E. coli to regulate its motility dependent on the stage of infection, activating flagellar expression upon initial contact with the host epithelium, when motility is beneficial, but reducing it within the host to delay the immune response.
format	article
author	Leanid Laganenka María Esteban López Remy Colin Victor Sourjik
author_facet	Leanid Laganenka María Esteban López Remy Colin Victor Sourjik
author_sort	Leanid Laganenka
title	Flagellum-Mediated Mechanosensing and RflP Control Motility State of Pathogenic <named-content content-type="genus-species">Escherichia coli</named-content>
title_short	Flagellum-Mediated Mechanosensing and RflP Control Motility State of Pathogenic <named-content content-type="genus-species">Escherichia coli</named-content>
title_full	Flagellum-Mediated Mechanosensing and RflP Control Motility State of Pathogenic <named-content content-type="genus-species">Escherichia coli</named-content>
title_fullStr	Flagellum-Mediated Mechanosensing and RflP Control Motility State of Pathogenic <named-content content-type="genus-species">Escherichia coli</named-content>
title_full_unstemmed	Flagellum-Mediated Mechanosensing and RflP Control Motility State of Pathogenic <named-content content-type="genus-species">Escherichia coli</named-content>
title_sort	flagellum-mediated mechanosensing and rflp control motility state of pathogenic <named-content content-type="genus-species">escherichia coli</named-content>
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/beb1adf3c43840e792e1c88a2c06b683
work_keys_str_mv	AT leanidlaganenka flagellummediatedmechanosensingandrflpcontrolmotilitystateofpathogenicnamedcontentcontenttypegenusspeciesescherichiacolinamedcontent AT mariaestebanlopez flagellummediatedmechanosensingandrflpcontrolmotilitystateofpathogenicnamedcontentcontenttypegenusspeciesescherichiacolinamedcontent AT remycolin flagellummediatedmechanosensingandrflpcontrolmotilitystateofpathogenicnamedcontentcontenttypegenusspeciesescherichiacolinamedcontent AT victorsourjik flagellummediatedmechanosensingandrflpcontrolmotilitystateofpathogenicnamedcontentcontenttypegenusspeciesescherichiacolinamedcontent
_version_	1718427048982085632

Flagellum-Mediated Mechanosensing and RflP Control Motility State of Pathogenic <named-content content-type="genus-species">Escherichia coli</named-content>

Ejemplares similares