Evolution of higher torque in Campylobacter-type bacterial flagellar motors

Bonnie Chaban,Morgan Beeby,Izaak Coleman

doi:10.1038/s41598-017-18115-1

Bonnie Chaban, Morgan Beeby + Show 1 more

Open Access

https://doi.org/10.1038/s41598-017-18115-1

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Abstract

Understanding the evolution of molecular machines underpins our understanding of the development of life on earth. A well-studied case are bacterial flagellar motors that spin helical propellers for bacterial motility. Diverse motors produce different torques, but how this diversity evolved remains unknown. To gain insights into evolution of the high-torque ε-proteobacterial motor exemplified by the Campylobacter jejuni motor, we inferred ancestral states by combining phylogenetics, electron cryotomography, and motility assays to characterize motors from Wolinella succinogenes, Arcobacter butzleri and Bdellovibrio bacteriovorus. Observation of ~12 stator complexes in many proteobacteria, yet ~17 in ε-proteobacteria suggest a “quantum leap” evolutionary event. Campylobacter-type motors have high stator occupancy in wider rings of additional stator complexes that are scaffolded by large proteinaceous periplasmic rings. We propose a model for motor evolution wherein independent inner- and outer-membrane structures fused to form a scaffold for additional stator complexes. Significantly, inner- and outer-membrane associated structures have evolved independently multiple times, suggesting that evolution of such structures is facile and poised the ε-proteobacteria to fuse them to form the high-torque Campylobacter-type motor.

Highlights

How molecular machines evolve and develop in complexity is a fundamental question for molecular biology
Sequences of 11 core motor proteins (C-ring proteins FliG, FliM, and FliN, T3SS proteins FlhB, FliI, FliP, and FliR, proximal rod proteins FlgB, FlgC, and FliE, and MS-ring protein FliF; Supplementary Table S1) from the core ε-proteobacterial flagellar motor were identified in each species, concatenated, and used to build a maximum likelihood motor phylogeny
In this study we combined phylogenetic, structural, and phenotypic studies to understand by inference possible evolutionary pathways to high torque in the Campylobacter-type ε-proteobacterial motors

Summary

Introduction

How molecular machines evolve and develop in complexity is a fundamental question for molecular biology. Torque is generated by proton flux through inner membrane stator complexes, MotA4B2, that exert force on the cytoplasmic C-ring; C-ring torque is transmitted by a rigid rod across the periplasm to the extracellular propeller Other components beside these core motor structures include a dedicated type III secretion system (T3SS) export apparatus that recruits, unfolds, and exports axial flagellar components; the inner membrane MS-ring that houses the the T3SS, and the P- and L-rings that act as bushings and portals through the peptidoglycan and outer membrane, respectively. A large scaffold structure named the ‘disk complex’ composed of three periplasmic structures facilitates incorporation of a wider ring of stator complexes, increasing the lever contact point at which the stator complexes contact the C-ring, and results in exertion of greater leverage for rotation of the flagellar filament[8] This wider ring facilitates incorporation of 17 stator complexes as compared to the ~11 in S. enterica and E. coli motors[9,10,11], further increasing torque. The proximal ring has become essential for the incorporation of the stator complexes into the Campylobacter-type motor[8]

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