Rotary mechanism of the prokaryotic Vo motor driven by proton motive force
Abstract ATP synthases play a crucial role in energy production by utilizing the proton motive force (pmf) across the membrane to rotate their membrane-embedded rotor c-ring, and thus driving ATP synthesis in the hydrophilic catalytic hexamer. However, the mechanism of how pmf converts into c-ring r...
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2024-11-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-024-53504-x |
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| author | Jun-ichi Kishikawa Yui Nishida Atsuki Nakano Takayuki Kato Kaoru Mitsuoka Kei-ichi Okazaki Ken Yokoyama |
| author_facet | Jun-ichi Kishikawa Yui Nishida Atsuki Nakano Takayuki Kato Kaoru Mitsuoka Kei-ichi Okazaki Ken Yokoyama |
| author_sort | Jun-ichi Kishikawa |
| collection | DOAJ |
| description | Abstract ATP synthases play a crucial role in energy production by utilizing the proton motive force (pmf) across the membrane to rotate their membrane-embedded rotor c-ring, and thus driving ATP synthesis in the hydrophilic catalytic hexamer. However, the mechanism of how pmf converts into c-ring rotation remains unclear. This study presents a 2.8 Å cryo-EM structure of the Vo domain of V/A-ATPase from Thermus thermophilus, revealing precise orientations of glutamate (Glu) residues in the c 12-ring. Three Glu residues face a water channel, with one forming a salt bridge with the Arginine in the stator (a/Arg). Molecular dynamics (MD) simulations show that protonation of specific Glu residues triggers unidirectional Brownian motion of the c 12-ring towards ATP synthesis. When the key Glu remains unprotonated, the salt bridge persists, blocking rotation. These findings suggest that asymmetry in the protonation of c/Glu residues biases c 12-ring movement, facilitating rotation and ATP synthesis. |
| format | Article |
| id | doaj-art-022cd08ce6ee492fb5770ca374c5fabf |
| institution | Kabale University |
| issn | 2041-1723 |
| language | English |
| publishDate | 2024-11-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj-art-022cd08ce6ee492fb5770ca374c5fabf2024-11-24T12:34:14ZengNature PortfolioNature Communications2041-17232024-11-0115111210.1038/s41467-024-53504-xRotary mechanism of the prokaryotic Vo motor driven by proton motive forceJun-ichi Kishikawa0Yui Nishida1Atsuki Nakano2Takayuki Kato3Kaoru Mitsuoka4Kei-ichi Okazaki5Ken Yokoyama6Department of Molecular Biosciences, Kyoto Sangyo University, Kamigamo-Motoyama, Kita-kuDepartment of Molecular Biosciences, Kyoto Sangyo University, Kamigamo-Motoyama, Kita-kuDepartment of Molecular Biosciences, Kyoto Sangyo University, Kamigamo-Motoyama, Kita-kuInstitute for Protein Research, Osaka University, 3-2 Yamadaoka, SuitaResearch Center for Ultra-High Voltage Electron Microscopy, Osaka UniversityResearch Center for Computational Science, Institute for Molecular Science, National Institutes of Natural SciencesDepartment of Molecular Biosciences, Kyoto Sangyo University, Kamigamo-Motoyama, Kita-kuAbstract ATP synthases play a crucial role in energy production by utilizing the proton motive force (pmf) across the membrane to rotate their membrane-embedded rotor c-ring, and thus driving ATP synthesis in the hydrophilic catalytic hexamer. However, the mechanism of how pmf converts into c-ring rotation remains unclear. This study presents a 2.8 Å cryo-EM structure of the Vo domain of V/A-ATPase from Thermus thermophilus, revealing precise orientations of glutamate (Glu) residues in the c 12-ring. Three Glu residues face a water channel, with one forming a salt bridge with the Arginine in the stator (a/Arg). Molecular dynamics (MD) simulations show that protonation of specific Glu residues triggers unidirectional Brownian motion of the c 12-ring towards ATP synthesis. When the key Glu remains unprotonated, the salt bridge persists, blocking rotation. These findings suggest that asymmetry in the protonation of c/Glu residues biases c 12-ring movement, facilitating rotation and ATP synthesis.https://doi.org/10.1038/s41467-024-53504-x |
| spellingShingle | Jun-ichi Kishikawa Yui Nishida Atsuki Nakano Takayuki Kato Kaoru Mitsuoka Kei-ichi Okazaki Ken Yokoyama Rotary mechanism of the prokaryotic Vo motor driven by proton motive force Nature Communications |
| title | Rotary mechanism of the prokaryotic Vo motor driven by proton motive force |
| title_full | Rotary mechanism of the prokaryotic Vo motor driven by proton motive force |
| title_fullStr | Rotary mechanism of the prokaryotic Vo motor driven by proton motive force |
| title_full_unstemmed | Rotary mechanism of the prokaryotic Vo motor driven by proton motive force |
| title_short | Rotary mechanism of the prokaryotic Vo motor driven by proton motive force |
| title_sort | rotary mechanism of the prokaryotic vo motor driven by proton motive force |
| url | https://doi.org/10.1038/s41467-024-53504-x |
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