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Repurposing a chemosensory macromolecular machine

Nature Communications, vol. 11, pp. 2041

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.

Authors 14

  1. California Institute of Technology

    Affiliation as printed

    Division of Biology and Biological Engineering, California Institute of Technology, 1200 E. California Blvd, Pasadena, CA, C1125, USA

  2. Leiden University

    Affiliation as printed

    Institute of Biology, Leiden University, 2333 BE, Leiden, The Netherlands

  3. California Institute of Technology

    Affiliation as printed

    Division of Biology and Biological Engineering, California Institute of Technology, 1200 E. California Blvd, Pasadena, CA, C1125, USA

  4. Max Planck Institute for Terrestrial Microbiology

    Affiliation as printed

    Department of Ecophysiology, Max Planck Institute for Terrestrial Microbiology, D-35043, Marburg, Germany

  5. California Institute of Technology

    Affiliation as printed

    Division of Biology and Biological Engineering, California Institute of Technology, 1200 E. California Blvd, Pasadena, CA, C1125, USA

    Rex Richards Building, South Parks Road, Oxford, OX1 3QU, UK

  6. California Institute of Technology

    Affiliation as printed

    Division of Biology and Biological Engineering, California Institute of Technology, 1200 E. California Blvd, Pasadena, CA, C1125, USA

  7. Loma Linda University

    Affiliation as printed

    Division of Microbiology and Molecular Genetics, School of Medicine, Loma Linda University, Loma Linda, CA, 92350, USA

  8. University of Southern California

    Affiliation as printed

    Department of Physics and Astronomy, University of Southern California, Los Angeles, CA, 90089, USA

  9. San Diego State University

    Affiliation as printed

    Department of Biology, Viral Information Institute, San Diego State University, San Diego, CA, 92182, USA

  10. ETH Zurich · Institute of Molecular Biology and Biophysics

    Affiliation as printed

    Institute of Molecular Biology and Biophysics, Eidgenössische Technische Hochschule Zürich, CH-8093, Zürich, Switzerland

  11. San Diego State University

    Affiliation as printed

    Department of Biology, Viral Information Institute, San Diego State University, San Diego, CA, 92182, USA

  12. Max Planck Institute for Terrestrial Microbiology

    Affiliation as printed

    Department of Ecophysiology, Max Planck Institute for Terrestrial Microbiology, D-35043, Marburg, Germany

  13. Leiden University

    Affiliation as printed

    Institute of Biology, Leiden University, 2333 BE, Leiden, The Netherlands. a.briegel@biology.leidenuniv.nl

    Institute of Biology, Leiden University, 2333 BE, Leiden, The Netherlands

  14. Grant J. Jensen corresponding

    California Institute of Technology · Howard Hughes Medical Institute

    Affiliation as printed

    Division of Biology and Biological Engineering, California Institute of Technology, 1200 E. California Blvd, Pasadena, CA, C1125, USA. jensen@caltech.edu

    Howard Hughes Medical Institute, California Institute of Technology, Pasadena, CA, 91125, USA. jensen@caltech.edu

    Howard Hughes Medical Institute, California Institute of Technology, Pasadena, CA, 91125, USA

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References 76