A Chaperone for the Stator Units of a Bacterial Flagellum

ABSTRACT The stator units of the flagellum supply power to the flagellar motor via ion transport across the cytoplasmic membrane and generate torque on the rotor for rotation. Flagellar motors across bacterial species have evolved adaptations that impact and enhance stator function to meet the deman...

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Autores principales:	Deborah A. Ribardo, Brittni R. Kelley, Jeremiah G. Johnson, David R. Hendrixson
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	Campylobacter jejuni FlgX MotA MotB chaperone flagellar motility Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/01f242ea5904447c8d55cd4957efb3c1
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spelling	oai:doaj.org-article:01f242ea5904447c8d55cd4957efb3c12021-11-15T16:22:09ZA Chaperone for the Stator Units of a Bacterial Flagellum10.1128/mBio.01732-192150-7511https://doaj.org/article/01f242ea5904447c8d55cd4957efb3c12019-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01732-19https://doaj.org/toc/2150-7511ABSTRACT The stator units of the flagellum supply power to the flagellar motor via ion transport across the cytoplasmic membrane and generate torque on the rotor for rotation. Flagellar motors across bacterial species have evolved adaptations that impact and enhance stator function to meet the demands of each species, including producing stator units using different fuel types or various stator units for different motility modalities. Campylobacter jejuni produces one of the most complex and powerful flagellar motors by positioning 17 stator units at a greater radial distance than in most other bacteria to increase power and torque for high velocity of motility. We report another evolutionary adaptation impacting flagellar stators by identifying FlgX as a chaperone for C. jejuni stator units to ensure sufficient power and torque for flagellar rotation and motility. We discovered that FlgX maintains MotA and MotB stator protein integrity likely through a direct interaction with MotA that prevents their degradation. Suppressor analysis suggested that the physiology of C. jejuni drives the requirement for FlgX to protect stator units from proteolysis by the FtsH protease complex. C. jejuni ΔflgX was strongly attenuated for colonization of the natural avian host, but colonization capacity was greatly restored by a single mutation in MotA. These findings suggest that the likely sole function of FlgX is to preserve stator unit integrity for the motility required for host interactions. Our findings demonstrate another evolved adaptation in motile bacteria to ensure the equipment of the flagellar motor with sufficient power to generate torque for motility. IMPORTANCE The bacterial flagellum is a reversible rotating motor powered by ion transport through stator units, which also exert torque on the rotor component to turn the flagellum for motility. Species-specific adaptations to flagellar motors impact stator function to meet the demands of each species to sufficiently power flagellar rotation. We identified another evolutionary adaptation by discovering that FlgX of Campylobacter jejuni preserves the integrity of stator units by functioning as a chaperone to protect stator proteins from degradation by the FtsH protease complex due to the physiology of the bacterium. FlgX is required to maintain a level of stator units sufficient to power the naturally high-torque flagellar motor of C. jejuni for motility in intestinal mucosal layers to colonize hosts. Our work continues to identify an increasing number of adaptations to flagellar motors across bacterial species that provide the mechanics necessary for producing an effective rotating nanomachine for motility.Deborah A. RibardoBrittni R. KelleyJeremiah G. JohnsonDavid R. HendrixsonAmerican Society for MicrobiologyarticleCampylobacter jejuniFlgXMotAMotBchaperoneflagellar motilityMicrobiologyQR1-502ENmBio, Vol 10, Iss 4 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	Campylobacter jejuni FlgX MotA MotB chaperone flagellar motility Microbiology QR1-502
spellingShingle	Campylobacter jejuni FlgX MotA MotB chaperone flagellar motility Microbiology QR1-502 Deborah A. Ribardo Brittni R. Kelley Jeremiah G. Johnson David R. Hendrixson A Chaperone for the Stator Units of a Bacterial Flagellum
description	ABSTRACT The stator units of the flagellum supply power to the flagellar motor via ion transport across the cytoplasmic membrane and generate torque on the rotor for rotation. Flagellar motors across bacterial species have evolved adaptations that impact and enhance stator function to meet the demands of each species, including producing stator units using different fuel types or various stator units for different motility modalities. Campylobacter jejuni produces one of the most complex and powerful flagellar motors by positioning 17 stator units at a greater radial distance than in most other bacteria to increase power and torque for high velocity of motility. We report another evolutionary adaptation impacting flagellar stators by identifying FlgX as a chaperone for C. jejuni stator units to ensure sufficient power and torque for flagellar rotation and motility. We discovered that FlgX maintains MotA and MotB stator protein integrity likely through a direct interaction with MotA that prevents their degradation. Suppressor analysis suggested that the physiology of C. jejuni drives the requirement for FlgX to protect stator units from proteolysis by the FtsH protease complex. C. jejuni ΔflgX was strongly attenuated for colonization of the natural avian host, but colonization capacity was greatly restored by a single mutation in MotA. These findings suggest that the likely sole function of FlgX is to preserve stator unit integrity for the motility required for host interactions. Our findings demonstrate another evolved adaptation in motile bacteria to ensure the equipment of the flagellar motor with sufficient power to generate torque for motility. IMPORTANCE The bacterial flagellum is a reversible rotating motor powered by ion transport through stator units, which also exert torque on the rotor component to turn the flagellum for motility. Species-specific adaptations to flagellar motors impact stator function to meet the demands of each species to sufficiently power flagellar rotation. We identified another evolutionary adaptation by discovering that FlgX of Campylobacter jejuni preserves the integrity of stator units by functioning as a chaperone to protect stator proteins from degradation by the FtsH protease complex due to the physiology of the bacterium. FlgX is required to maintain a level of stator units sufficient to power the naturally high-torque flagellar motor of C. jejuni for motility in intestinal mucosal layers to colonize hosts. Our work continues to identify an increasing number of adaptations to flagellar motors across bacterial species that provide the mechanics necessary for producing an effective rotating nanomachine for motility.
format	article
author	Deborah A. Ribardo Brittni R. Kelley Jeremiah G. Johnson David R. Hendrixson
author_facet	Deborah A. Ribardo Brittni R. Kelley Jeremiah G. Johnson David R. Hendrixson
author_sort	Deborah A. Ribardo
title	A Chaperone for the Stator Units of a Bacterial Flagellum
title_short	A Chaperone for the Stator Units of a Bacterial Flagellum
title_full	A Chaperone for the Stator Units of a Bacterial Flagellum
title_fullStr	A Chaperone for the Stator Units of a Bacterial Flagellum
title_full_unstemmed	A Chaperone for the Stator Units of a Bacterial Flagellum
title_sort	chaperone for the stator units of a bacterial flagellum
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/01f242ea5904447c8d55cd4957efb3c1
work_keys_str_mv	AT deboraharibardo achaperoneforthestatorunitsofabacterialflagellum AT brittnirkelley achaperoneforthestatorunitsofabacterialflagellum AT jeremiahgjohnson achaperoneforthestatorunitsofabacterialflagellum AT davidrhendrixson achaperoneforthestatorunitsofabacterialflagellum AT deboraharibardo chaperoneforthestatorunitsofabacterialflagellum AT brittnirkelley chaperoneforthestatorunitsofabacterialflagellum AT jeremiahgjohnson chaperoneforthestatorunitsofabacterialflagellum AT davidrhendrixson chaperoneforthestatorunitsofabacterialflagellum
_version_	1718426884954390528

A Chaperone for the Stator Units of a Bacterial Flagellum

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