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Repurposing a chemosensory macromolecular machine

Ortega, Davi R. and Yang, Wen 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. (2020) Repurposing a chemosensory macromolecular machine. Nature Communications, 11 . Art. No. 2041. ISSN 2041-1723. PMCID PMC7184735. https://resolver.caltech.edu/CaltechAUTHORS:20190531-091859930

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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.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1038/s41467-020-15736-5DOIArticle
https://doi.org/10.1101/653600DOIDiscussion Paper
http://www.ncbi.nlm.nih.gov/pmc/articles/pmc7184735/PubMed CentralArticle
ORCID:
AuthorORCID
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
Alternate Title:Repurposing a macromolecular machine: Architecture and evolution of the F7 chemosensory system
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.
Funders:
Funding AgencyGrant Number
John Templeton Foundation51250
John Templeton Foundation60973
NIHR35 GM122588
NIHR01 GM108655
Max-Planck-GesellschaftUNSPECIFIED
NSFCBET-1605031
Swiss National Science Foundation (SNSF)UNSPECIFIED
Air Force Office of Scientific Research (AFOSR)FA955014-1-0294
NIHP30 DK089507
PubMed Central ID:PMC7184735
Record Number:CaltechAUTHORS:20190531-091859930
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20190531-091859930
Official Citation:Ortega, D.R., Yang, W., Subramanian, P. et al. Repurposing a chemosensory macromolecular machine. Nat Commun 11, 2041 (2020). https://doi.org/10.1038/s41467-020-15736-5
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:96000
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:31 May 2019 16:47
Last Modified:04 May 2020 16:30

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