Repurposing a chemosensory macromolecular machine
Abstract
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 identify 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 trace 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.
Additional Information
© 2020 The Author(s). This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/. Received 13 July 2019; Accepted 23 March 2020; Published 27 April 2020. 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 and for providing the Tar model used in Fig. 5. We also thank Dr. Catherine M. Oikonomou for helpful discussion and suggestions on the paper. This work was supported by the John Templeton Foundation as part of the Boundaries of Life Initiative (grants 51250 and 60973), NIGMS grant R35 GM122588 (to G.J.J.), NIGMS grant R01 GM108655 (to K.J.W.), the Max-Planck-Gesellschaft (to S.R.), the National Science Foundation grant CBET-1605031 (to M.G.K.), the Swiss National Science Foundation (R.K.), and the Air Force Office of Scientific Research Presidential Early Career Award for Scientists and Engineers grant FA955014-1-0294 (S.P.). P. aeruginosa strains were acquired from the transposon mutant collection that was made possible by NIH grant P30 DK089507. Data availability: Tomograms are available in the Electron Tomography Database—Caltech at https://etdb.caltech.edu and their identifiers are listed in the Supplementary Table 6. Phylogenetic trees in Fig. 4, Supplementary Figs. 1, 2, and 4 are available in Supplementary Data 1. The homology models in Fig. 2D are available in Supplementary Data 2. Other data are available from the corresponding authors upon reasonable request. Author Contributions: Conceptualization: D.R.O., A.B., and G.J.J.; Formal analysis: D.R.O.; Funding acquisition: K.J.W., M.G.K., S.R., A.B., and G.J.J.; Investigation: D.R.O., P.S., P.M., A.K., S.C., K.J.W., S.P., S.A.C., R.K., and A.B.; Methodology: D.R.O., W.Y., P.S., P.M., K.J.W., S.P., D.A.C., M.G.K., S.R., and A.B. Project administration: G.J.J.; Software: D.R.O.; Supervision: M.G.K., S.R., A.B., and G.J.J. Validation: D.R.O., W.Y., P.S., P.M., A.K., S.C., K.J.W., S.P., S.A.C., R.K., and A.B.; Visualization: D.R.O., W.Y., P.S., S.P., and A.B.; Writing—original draft: D.R.O., P.S., A.B., and G.J.J. Writing—review and editing: D.R.O., W.Y., P.S., K.J.W., S.P., D.A.C., M.G.K., S.R., A.B., and G.J.J. The authors declare no competing interests.Attached Files
Published - s41467-020-15736-5.pdf
Submitted - 653600.1.full.pdf
Supplemental Material - 41467_2020_15736_MOESM1_ESM.pdf
Supplemental Material - 41467_2020_15736_MOESM2_ESM.pdf
Supplemental Material - 41467_2020_15736_MOESM3_ESM.pdf
Supplemental Material - 41467_2020_15736_MOESM4_ESM.gz
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Supplemental Material - 41467_2020_15736_MOESM6_ESM.pdf
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Additional details
- Alternative title
- Repurposing a macromolecular machine: Architecture and evolution of the F7 chemosensory system
- PMCID
- PMC7184735
- Eprint ID
- 96000
- Resolver ID
- CaltechAUTHORS:20190531-091859930
- 51250
- John Templeton Foundation
- 60973
- John Templeton Foundation
- R35 GM122588
- NIH
- R01 GM108655
- NIH
- Max-Planck-Gesellschaft
- CBET-1605031
- NSF
- Swiss National Science Foundation (SNSF)
- FA955014-1-0294
- Air Force Office of Scientific Research (AFOSR)
- P30 DK089507
- NIH
- Created
-
2019-05-31Created from EPrint's datestamp field
- Updated
-
2022-02-15Created from EPrint's last_modified field
- Caltech groups
- Division of Biology and Biological Engineering