Repurposing a chemosensory macromolecular machine.

Biological Evolution Chemotaxis Computational Biology Electron Microscope Tomography Escherichia coli / physiology Escherichia coli Proteins Flagella / physiology Gammaproteobacteria / physiology Genome, Bacterial Macromolecular Substances / chemistry Methyl-Accepting Chemotaxis Proteins / chemistry Methylococcaceae / physiology Phylogeny Pseudomonas aeruginosa / physiology Shewanella / physiology Vibrio cholerae / physiology

Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
27 04 2020
Historique:
received: 13 07 2019
accepted: 23 03 2020
entrez: 29 4 2020
pubmed: 29 4 2020
medline: 11 8 2020
Statut: epublish

Résumé

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.

Identifiants

DOI: 10.1038/s41467-020-15736-5 PMID: 32341341 PMC: PMC7184735
pubmed: 32341341
doi: 10.1038/s41467-020-15736-5
pii: 10.1038/s41467-020-15736-5
pmc: PMC7184735
doi:

Substances chimiques

Escherichia coli Proteins 0
Macromolecular Substances 0
Methyl-Accepting Chemotaxis Proteins 0
cheY protein, E coli 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

2041

Subventions

Organisme : NIGMS NIH HHS
ID : R01 GM108655
Pays : United States
Organisme : NIGMS NIH HHS
ID : R35 GM122588
Pays : United States
Organisme : Howard Hughes Medical Institute
Pays : United States
Organisme : NIDDK NIH HHS
ID : P30 DK089507
Pays : United States

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Auteurs

Davi R Ortega (DR)

Division of Biology and Biological Engineering, California Institute of Technology, 1200 E. California Blvd, Pasadena, CA, C1125, USA.
ORCID: 0000-0002-8344-2335

Wen Yang (W)

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

Poorna Subramanian (P)

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

Petra Mann (P)

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

Andreas Kjær (A)

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.
ORCID: 0000-0002-0096-5764

Songye Chen (S)

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

Kylie J Watts (KJ)

Division of Microbiology and Molecular Genetics, School of Medicine, Loma Linda University, Loma Linda, CA, 92350, USA.
ORCID: 0000-0002-8072-2745

Sahand Pirbadian (S)

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

David A Collins (DA)

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

Romain Kooger (R)

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

Marina G Kalyuzhnaya (MG)

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

Simon Ringgaard (S)

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

Ariane Briegel (A)

Institute of Biology, Leiden University, 2333 BE, Leiden, The Netherlands. a.briegel@biology.leidenuniv.nl.
ORCID: 0000-0003-3733-3725

Grant J Jensen (GJ)

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.
ORCID: 0000-0003-1556-4864

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Classifications MeSH

questionsmedicales.fr › Phénomènes biologiques › Évolution biologique › Repurposing a chemosensory macromolecular machine.
questionsmedicales.fr › Phénomènes physiologiques de l'appareil locomoteur et du système nerveux › Phénomènes physiologiques du système locomoteur › Mouvement › Locomotion › Taxie › Chimiotaxie › Repurposing a chemosensory macromolecular machine.
questionsmedicales.fr › Sciences de l'information › Informatique › Biologie informatique › Repurposing a chemosensory macromolecular machine.
questionsmedicales.fr › Techniques d'investigation › Microscopie électronique › Microscopie électronique à transmission › Tomographie en microscopie électronique › Repurposing a chemosensory macromolecular machine.
questionsmedicales.fr › Bactéries › Proteobacteria › Gammaproteobacteria › Enterobacteriaceae › Escherichia › Escherichia coli › Repurposing a chemosensory macromolecular machine.
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines bactériennes › Protéines Escherichia coli › Repurposing a chemosensory macromolecular machine.
questionsmedicales.fr › Cellules › Structures cellulaires › Prolongements cytoplasmiques › Flagelles › Repurposing a chemosensory macromolecular machine.
questionsmedicales.fr › Bactéries › Proteobacteria › Gammaproteobacteria › Repurposing a chemosensory macromolecular machine.
questionsmedicales.fr › Phénomènes génétiques › Structures génétiques › Génome › Génome microbien › Génome bactérien › Repurposing a chemosensory macromolecular machine.
questionsmedicales.fr › Structures macromoléculaires › Repurposing a chemosensory macromolecular machine.
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines membranaires › Récepteurs de surface cellulaire › Protéines chimiotactiques accepteuses de méthyle › Repurposing a chemosensory macromolecular machine.
questionsmedicales.fr › Bactéries › Proteobacteria › Gammaproteobacteria › Methylococcaceae › Repurposing a chemosensory macromolecular machine.
questionsmedicales.fr › Sciences de l'information › Phylogenèse › Repurposing a chemosensory macromolecular machine.
questionsmedicales.fr › Bactéries › Proteobacteria › Gammaproteobacteria › Pseudomonadaceae › Pseudomonas › Pseudomonas aeruginosa › Repurposing a chemosensory macromolecular machine.
questionsmedicales.fr › Bactéries › Proteobacteria › Gammaproteobacteria › Alteromonadaceae › Shewanella › Repurposing a chemosensory macromolecular machine.
questionsmedicales.fr › Bactéries › Proteobacteria › Gammaproteobacteria › Vibrionaceae › Vibrio › Vibrio cholerae › Repurposing a chemosensory macromolecular machine.