Evolution of higher torque in Campylobacter-type bacterial flagellar motors
Bonnie Chaban, Izaak Coleman & Morgan Beeby
Scientific Reports 8, Article number: 97 (2018)
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Bacterial evolution Cryoelectron tomography Molecular evolution
Received: 13 October 2017 Accepted: 05 December 2017
Published online: 08 January 2018
3-D model images of the eight studied bacterial motors.
Source/Fonte: Morgan Beeby/Imperial College London
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.
Acknowledgements
The authors gratefully thank Tillmann Pape for electron microscopy assistance, Liz Sockett from the University of Nottingham for the gift of Bdellovibrio bacteriovorus, Erin Gaynor from the University of British Columbia for the gift of the straight Campylobacter mutant strain, and Bertus Beaumont, Josie Ferreira, and Florian Rossmann for critical reading of the manuscript. This work was supported by a Biotechnology and Biological Sciences Research Council Grant BB/L023091/1 (to M.B.).
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Author notes
Bonnie Chaban
Present address: Faculty of Science, Health, Education and Engineering, University of the Sunshine Coast, 90 Sippy Downs Drive, Sippy Downs, 4556, QLD, Australia
Affiliations
Department of Life Sciences, Imperial College of London, London, SW7 2AZ, UK
Bonnie Chaban, Izaak Coleman & Morgan Beeby
Contributions
B.C. and I.C. performed phylogenetic analysis, B.C. collected tomographic and motility data, B.C., I.C. and M.B. analysed data. B.C. and M.B. wrote the main manuscript text and prepared figures. All authors reviewed the manuscript.
Competing Interests
The authors declare that they have no competing interests.
Corresponding author
Correspondence to Morgan Beeby.
