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Repurposing a macromolecular machine: Architecture and evolution of the F7 chemosensory system

Ortega, Davi R. and Subramanian, Poorna and Mann, Petra and Kjaer, Andreas and Chen, Songye and Watts, Kylie J. and Pirbadian, Sahand and Collins, David A. and Kooger, Romain and Kalyuzhnaya, Marina G. and Ringgaard, Smion and Briegel, Ariane and Jensen, Grant J. (2019) Repurposing a macromolecular machine: Architecture and evolution of the F7 chemosensory system. . (Unpublished)

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How complex, multi-component macromolecular machines evolved remains poorly understood. Here we reveal the evolutionary origins of the chemosensory machinery that controls flagellar motility in Escherichia coli. We first identified ancestral forms still present in Vibrio cholerae, Pseudomonas aeruginosa, Shewanella oneidensis and Methylomicrobium alcaliphilum, characterizing their structures by electron cryotomography and finding evidence that they function in a stress response pathway. Using bioinformatics, we then traced the evolution of the system through γ-Proteobacteria, pinpointing key evolutionary events that led to the machine now seen in E. coli. Our results suggest that two ancient chemosensory systems with different inputs and outputs (F6 and F7) existed contemporaneously, with one (F7) ultimately taking over the inputs and outputs of the other (F6), which was subsequently lost.

Item Type:Report or Paper (Discussion Paper)
Related URLs:
URLURL TypeDescription Paper
Ortega, Davi R.0000-0002-8344-2335
Kjaer, Andreas0000-0002-0096-5764
Chen, Songye0000-0001-5407-5049
Watts, Kylie J.0000-0002-8072-2745
Kooger, Romain0000-0001-8768-1870
Kalyuzhnaya, Marina G.0000-0002-9058-7794
Briegel, Ariane0000-0003-3733-3725
Jensen, Grant J.0000-0003-1556-4864
Additional Information:The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. The authors wish to thank Drs. Zhiheng Yu, Jason de la Cruz, Chuan Hong and Rick Huang for microscopy support at HHMI Janelia Farms; Dr. Mohamed Y. El-Naggar for insights into the culturing of S. oneidensis; Dr. Kristin Wuichet for discussions about the evolutionary interpretation of the bioinformatics data and Dr. Keith Cassidy for discussions on homology model building. We also thank Dr. Catherine M. Oikonomou for helpful discussion and suggestions on the manuscript. Cryo-EM work was done in the Beckman Resource Center for Transmission Electron Microscopy at Caltech. Funding: This work was supported by the John Templeton Foundation as part of the Boundaries of Life Initiative (grants 51250 & 60973), NIGMS grant R35 GM122588 (to GJJ), NIGMS grant R01 GM108655 (to KJW), the Max-Planck-Gesellschaft (to SR), the National Science Foundation grant CBET-1605031 (to MGK), the Swiss National Science Foundation (RK), and the Air Force Office of Scientific Research Presidential Early Career Award for Scientists and Engineers grant FA955014-1-0294 (SP). P. aeruginosa strains were acquired from the transposon mutant collection that was made possible by NIH grant P30 DK089507. Author contributions: Conceptualization: DRO, AB and GJJ; Formal analysis: DRO; Funding acquisition: KJW, MGK, SR, AB and GJJ; Investigation: DRO, PS, PM, AK, SC, KJW, SP, SAC, RK and AB; Methodology: DRO, PS, PM, KJW, SP, DAC, MGK, SR and AB. Project administration: GJJ; Software: DRO; Supervision: MGK, SR, AB and GJJ. Validation: DRO, PS, PM, AK, SC, KJW, SP, SAC, RK and AB; Visualization: DRO, PS, SP and AB; Writing – original draft: DRO, PS, AB, GJJ. Writing – review and editing: DRO, PS, KJW, SP, DAC, MGK, SR, AB and GJJ. Competing interests: Authors declare no competing interests; Data and materials availability: 1D electron density profile tool is available on node package manager (npm): The script to visualize the 1D electron density profile and calculate uncertainties is available on Observable HQ: Regular Architecture code is available on npm: Tomograms are available in the Electron Tomography Database – Caltech at Phylogenetic trees and homology models are available as Supplementary Datasets.
Funding AgencyGrant Number
John Templeton Foundation51250
John Templeton Foundation60973
NIHR35 GM122588
NIHR01 GM108655
Swiss National Science Foundation (SNSF)UNSPECIFIED
Air Force Office of Scientific Research (AFOSR)FA955014-1-0294
NIHP30 DK089507
Record Number:CaltechAUTHORS:20190531-091859930
Persistent URL:
Official Citation:Repurposing a macromolecular machine: Architecture and evolution of the F7 chemosensory system Davi R Ortega, Poorna Subramanian, Petra Mann, Andreas Kjaer, Songye Chen, Kylie J. Watts, Sahand Pirbadian, David A. Collins, Romain Kooger, Marina G. Kalyuzhnaya, Smion Ringgaard, Ariane Briegel, Grant J Jensen bioRxiv 653600; doi:
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:96000
Deposited By: George Porter
Deposited On:31 May 2019 16:47
Last Modified:03 Oct 2019 21:18

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