Evolution of a large periplasmic disk in Campylobacterota flagella enables both efficient motility and autoagglutination
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.
Authors
- Daisuke Nakane (ORCID: https://orcid.org/0000-0002-8201-2608)
- Trishant R. Umrekar (ORCID: https://orcid.org/0000-0003-3138-4185)
- José‐Jesús Fernández (ORCID: https://orcid.org/0000-0003-2222-3355)
- David R. Hendrixson (ORCID: https://orcid.org/0000-0001-8496-2466)
- Eli J. Cohen (ORCID: https://orcid.org/0000-0001-9265-7517)
- Morgan Beeby (ORCID: https://orcid.org/0000-0001-6413-9835)
- Laurence G. Wilson (ORCID: https://orcid.org/0000-0001-6659-6001)
- Deborah A. Ribardo
- Tina Drobnič (ORCID: https://orcid.org/0000-0001-6364-1874)
- Emma E. Brock (ORCID: https://orcid.org/0000-0002-7683-0153)
- Xuefei Guo (ORCID: https://orcid.org/0000-0001-7135-0954)
- Aoba Yoshioka
Institutions
- University of Electro-Communications (JP)
- National Research Council (LK)
- Imperial College London (GB)
- University of York (GB)
- The University of Texas Southwestern Medical Center (US)
Publication Details
- Journal
- Developmental Cell
- Published
- 2024-10-02
- DOI
- https://doi.org/10.1016/j.devcel.2024.09.008
- Citations
- 12
- Primary Topic
- Bacteriophages and microbial interactions
- Type
- article
- Field-Weighted Citation Impact
- 5.05
Funders
- National Institutes of Health
- Medical Research Council
- Biotechnology and Biological Sciences Research Council
- Japan Society for the Promotion of Science