Bacterial flagella grow through an injection-diffusion mechanism
The bacterial flagellum is a self-assembling nanomachine. The external flagellar filament, several times longer than a bacterial cell body, is made of a few tens of thousands subunits of a single protein: flagellin. A fundamental problem concerns the molecular mechanism of how the flagellum grows ou...
| Main Authors: | , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
eLife Sciences Publications Ltd
2017-03-01
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| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/23136 |
| _version_ | 1811180330640474112 |
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| author | Thibaud T Renault Anthony O Abraham Tobias Bergmiller Guillaume Paradis Simon Rainville Emmanuelle Charpentier Călin C Guet Yuhai Tu Keiichi Namba James P Keener Tohru Minamino Marc Erhardt |
| author_facet | Thibaud T Renault Anthony O Abraham Tobias Bergmiller Guillaume Paradis Simon Rainville Emmanuelle Charpentier Călin C Guet Yuhai Tu Keiichi Namba James P Keener Tohru Minamino Marc Erhardt |
| author_sort | Thibaud T Renault |
| collection | DOAJ |
| description | The bacterial flagellum is a self-assembling nanomachine. The external flagellar filament, several times longer than a bacterial cell body, is made of a few tens of thousands subunits of a single protein: flagellin. A fundamental problem concerns the molecular mechanism of how the flagellum grows outside the cell, where no discernible energy source is available. Here, we monitored the dynamic assembly of individual flagella using in situ labelling and real-time immunostaining of elongating flagellar filaments. We report that the rate of flagellum growth, initially ∼1,700 amino acids per second, decreases with length and that the previously proposed chain mechanism does not contribute to the filament elongation dynamics. Inhibition of the proton motive force-dependent export apparatus revealed a major contribution of substrate injection in driving filament elongation. The combination of experimental and mathematical evidence demonstrates that a simple, injection-diffusion mechanism controls bacterial flagella growth outside the cell. |
| first_indexed | 2024-04-11T09:01:18Z |
| format | Article |
| id | doaj.art-0d8e4e5410504d0ea3fe009f4a0d60a1 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-11T09:01:18Z |
| publishDate | 2017-03-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-0d8e4e5410504d0ea3fe009f4a0d60a12022-12-22T04:32:46ZengeLife Sciences Publications LtdeLife2050-084X2017-03-01610.7554/eLife.23136Bacterial flagella grow through an injection-diffusion mechanismThibaud T Renault0https://orcid.org/0000-0002-1530-2613Anthony O Abraham1https://orcid.org/0000-0002-8710-1351Tobias Bergmiller2Guillaume Paradis3Simon Rainville4Emmanuelle Charpentier5Călin C Guet6https://orcid.org/0000-0001-6220-2052Yuhai Tu7Keiichi Namba8James P Keener9Tohru Minamino10Marc Erhardt11https://orcid.org/0000-0001-6292-619XJunior Research Group, Infection Biology of <i>Salmonella</i>, Helmholtz Centre for Infection Research, Braunschweig, Germany; Max Planck Institute for Infection Biology, Berlin, GermanyGraduate School of Frontier Biosciences, Osaka University, Osaka, JapanInstitute of Science and Technology Austria, Klosterneuburg, AustriaDepartment of Physics, Engineering Physics and Optics, Laval University, Quebec City, Quebec, CanadaDepartment of Physics, Engineering Physics and Optics, Laval University, Quebec City, Quebec, CanadaMax Planck Institute for Infection Biology, Berlin, GermanyInstitute of Science and Technology Austria, Klosterneuburg, AustriaIBM Thomas J Watson Research Center, New York, United StatesGraduate School of Frontier Biosciences, Osaka University, Osaka, Japan; RIKEN Quantitative Biology Center, Suita, JapanDepartment of Mathematics, University of Utah, Salt Lake City, United StatesGraduate School of Frontier Biosciences, Osaka University, Osaka, JapanJunior Research Group, Infection Biology of <i>Salmonella</i>, Helmholtz Centre for Infection Research, Braunschweig, GermanyThe bacterial flagellum is a self-assembling nanomachine. The external flagellar filament, several times longer than a bacterial cell body, is made of a few tens of thousands subunits of a single protein: flagellin. A fundamental problem concerns the molecular mechanism of how the flagellum grows outside the cell, where no discernible energy source is available. Here, we monitored the dynamic assembly of individual flagella using in situ labelling and real-time immunostaining of elongating flagellar filaments. We report that the rate of flagellum growth, initially ∼1,700 amino acids per second, decreases with length and that the previously proposed chain mechanism does not contribute to the filament elongation dynamics. Inhibition of the proton motive force-dependent export apparatus revealed a major contribution of substrate injection in driving filament elongation. The combination of experimental and mathematical evidence demonstrates that a simple, injection-diffusion mechanism controls bacterial flagella growth outside the cell.https://elifesciences.org/articles/23136bacterial flagellumcontinuous-flow immunostaininginjection-diffusion mechanismproton motive forceSalmonella enterica |
| spellingShingle | Thibaud T Renault Anthony O Abraham Tobias Bergmiller Guillaume Paradis Simon Rainville Emmanuelle Charpentier Călin C Guet Yuhai Tu Keiichi Namba James P Keener Tohru Minamino Marc Erhardt Bacterial flagella grow through an injection-diffusion mechanism eLife bacterial flagellum continuous-flow immunostaining injection-diffusion mechanism proton motive force Salmonella enterica |
| title | Bacterial flagella grow through an injection-diffusion mechanism |
| title_full | Bacterial flagella grow through an injection-diffusion mechanism |
| title_fullStr | Bacterial flagella grow through an injection-diffusion mechanism |
| title_full_unstemmed | Bacterial flagella grow through an injection-diffusion mechanism |
| title_short | Bacterial flagella grow through an injection-diffusion mechanism |
| title_sort | bacterial flagella grow through an injection diffusion mechanism |
| topic | bacterial flagellum continuous-flow immunostaining injection-diffusion mechanism proton motive force Salmonella enterica |
| url | https://elifesciences.org/articles/23136 |
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