A Chaperone for the Stator Units of a Bacterial Flagellum.

Deborah A Ribardo,Jeremiah G Johnson,David R Hendrixson,Brittni R Kelley,M Stephen Trent

doi:10.1128/mbio.01732-19

Deborah A Ribardo, Jeremiah G Johnson + Show 3 more

Open Access

https://doi.org/10.1128/mbio.01732-19

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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.

Highlights

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
We describe additional findings that suggest that the requirement for FlgX-dependent stability of stator units may be due to a specific characteristic of the physiology of C. jejuni, with the FtsH inner membrane protease as a major contributor to stator protein degradation
We propose that FlgX interacts with a cytoplasmic domain of MotA to maintain stability of MotAB stator units in C. jejuni on the basis of the following observations: (i) FlgX is localized to the cytoplasm; (ii) MotA has prominent cytoplasmic domains, in contrast to MotB, which is predicted to have a small N-terminal cytoplasmic domain of only ϳ18 residues; and (iii) FlgX efficiently coimmunoprecipitated MotA in the absence of MotB

Summary

Introduction

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. 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. 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. Ion passage causes conformational changes in MotA within a stator unit such that the cytoplasmic region contacting FliG of the rotor creates a pushing force that generates torque for flagellar rotation [8, 22, 23]

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