Evolution of a large periplasmic disk in Campylobacterota flagella enables both efficient motility and autoagglutination

Eli J Cohen; Tina Drobnič; Deborah A Ribardo; Aoba Yoshioka; Trishant Umrekar; Xuefei Guo; Jose-Jesus Fernandez; Emma E Brock; Laurence Wilson; Daisuke Nakane; David R Hendrixson; Morgan Beeby

doi:10.1016/j.devcel.2024.09.008

Evolution of a large periplasmic disk in Campylobacterota flagella enables both efficient motility and autoagglutination

Eli J Cohen, Tina Drobnič, Deborah A Ribardo, Aoba Yoshioka, Trishant Umrekar, Xuefei Guo, Jose-Jesus Fernandez, Emma E Brock, Laurence Wilson, Daisuke Nakane, David R Hendrixson, Morgan Beeby

Physics

Research output: Contribution to journal › Article › peer-review

Abstract

The flagellar motors of Campylobacter jejuni (C. jejuni) and related Campylobacterota (previously epsilonproteobacteria) feature 100-nm-wide periplasmic "basal disks" that have been implicated in scaffolding a wider ring of additional motor proteins to increase torque, but the size of these disks is excessive for a role solely in scaffolding motor proteins. Here, we show that the basal disk is a flange that braces the flagellar motor during disentanglement of its flagellar filament from interactions with the cell body and other filaments. We show that motor output is unaffected when we shrink or displace the basal disk, and suppressor mutations of debilitated motors occur in flagellar-filament or cell-surface glycosylation pathways, thus sidestepping the need for a flange to overcome the interactions between two flagellar filaments and between flagellar filaments and the cell body. Our results identify unanticipated co-dependencies in the evolution of flagellar motor structure and cell-surface properties in the Campylobacterota.

Original language	English
Pages (from-to)	3306-3321.e5
Number of pages	16
Journal	Developmental Cell
Volume	59
Issue number	24
DOIs	https://doi.org/10.1016/j.devcel.2024.09.008
Publication status	Published - 16 Dec 2024

Bibliographical note

Keywords

Flagella/metabolism
Periplasm/metabolism
Campylobacter jejuni/metabolism
Bacterial Proteins/metabolism
Molecular Motor Proteins/metabolism
Agglutination

Access to Document

10.1016/j.devcel.2024.09.008Licence: CC BY

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© 2024 The Author(s)
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Cite this

Cohen, E. J., Drobnič, T., Ribardo, D. A., Yoshioka, A., Umrekar, T., Guo, X., Fernandez, J.-J., Brock, E. E., Wilson, L., Nakane, D., Hendrixson, D. R., & Beeby, M. (2024). Evolution of a large periplasmic disk in Campylobacterota flagella enables both efficient motility and autoagglutination. Developmental Cell, 59(24), 3306-3321.e5. https://doi.org/10.1016/j.devcel.2024.09.008

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abstract = "The flagellar motors of Campylobacter jejuni (C. jejuni) and related Campylobacterota (previously epsilonproteobacteria) feature 100-nm-wide periplasmic {"}basal disks{"} that have been implicated in scaffolding a wider ring of additional motor proteins to increase torque, but the size of these disks is excessive for a role solely in scaffolding motor proteins. Here, we show that the basal disk is a flange that braces the flagellar motor during disentanglement of its flagellar filament from interactions with the cell body and other filaments. We show that motor output is unaffected when we shrink or displace the basal disk, and suppressor mutations of debilitated motors occur in flagellar-filament or cell-surface glycosylation pathways, thus sidestepping the need for a flange to overcome the interactions between two flagellar filaments and between flagellar filaments and the cell body. Our results identify unanticipated co-dependencies in the evolution of flagellar motor structure and cell-surface properties in the Campylobacterota.",

keywords = "Flagella/metabolism, Periplasm/metabolism, Campylobacter jejuni/metabolism, Bacterial Proteins/metabolism, Molecular Motor Proteins/metabolism, Agglutination",

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Cohen, EJ, Drobnič, T, Ribardo, DA, Yoshioka, A, Umrekar, T, Guo, X, Fernandez, J-J, Brock, EE, Wilson, L, Nakane, D, Hendrixson, DR & Beeby, M 2024, 'Evolution of a large periplasmic disk in Campylobacterota flagella enables both efficient motility and autoagglutination', Developmental Cell, vol. 59, no. 24, pp. 3306-3321.e5. https://doi.org/10.1016/j.devcel.2024.09.008

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AU - Cohen, Eli J

AU - Drobnič, Tina

AU - Ribardo, Deborah A

AU - Yoshioka, Aoba

AU - Umrekar, Trishant

AU - Guo, Xuefei

AU - Fernandez, Jose-Jesus

AU - Brock, Emma E

AU - Wilson, Laurence

AU - Nakane, Daisuke

AU - Hendrixson, David R

AU - Beeby, Morgan

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AB - The flagellar motors of Campylobacter jejuni (C. jejuni) and related Campylobacterota (previously epsilonproteobacteria) feature 100-nm-wide periplasmic "basal disks" that have been implicated in scaffolding a wider ring of additional motor proteins to increase torque, but the size of these disks is excessive for a role solely in scaffolding motor proteins. Here, we show that the basal disk is a flange that braces the flagellar motor during disentanglement of its flagellar filament from interactions with the cell body and other filaments. We show that motor output is unaffected when we shrink or displace the basal disk, and suppressor mutations of debilitated motors occur in flagellar-filament or cell-surface glycosylation pathways, thus sidestepping the need for a flange to overcome the interactions between two flagellar filaments and between flagellar filaments and the cell body. Our results identify unanticipated co-dependencies in the evolution of flagellar motor structure and cell-surface properties in the Campylobacterota.

KW - Flagella/metabolism

KW - Periplasm/metabolism

KW - Campylobacter jejuni/metabolism

KW - Bacterial Proteins/metabolism

KW - Molecular Motor Proteins/metabolism

KW - Agglutination

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DO - 10.1016/j.devcel.2024.09.008

M3 - Article

C2 - 39362219

SN - 1534-5807

VL - 59

SP - 3306-3321.e5

JO - Developmental Cell

JF - Developmental Cell

IS - 24

ER -