Expulsion mechanism of the substrate-translocating subunit in ECF transporters
Abstract Energy-coupling factor (ECF)-type transporters mediate the uptake of micronutrients in many bacteria. They consist of a substrate-translocating subunit (S-component) and an ATP-hydrolysing motor (ECF module) Previous data indicate that the S-component topples within the membrane to alternat...
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2023-07-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-023-40266-1 |
| _version_ | 1797769456214081536 |
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| author | Chancievan Thangaratnarajah Mark Nijland Luís Borges-Araújo Aike Jeucken Jan Rheinberger Siewert J. Marrink Paulo C. T. Souza Cristina Paulino Dirk J. Slotboom |
| author_facet | Chancievan Thangaratnarajah Mark Nijland Luís Borges-Araújo Aike Jeucken Jan Rheinberger Siewert J. Marrink Paulo C. T. Souza Cristina Paulino Dirk J. Slotboom |
| author_sort | Chancievan Thangaratnarajah |
| collection | DOAJ |
| description | Abstract Energy-coupling factor (ECF)-type transporters mediate the uptake of micronutrients in many bacteria. They consist of a substrate-translocating subunit (S-component) and an ATP-hydrolysing motor (ECF module) Previous data indicate that the S-component topples within the membrane to alternately expose the binding site to either side of the membrane. In many ECF transporters, the substrate-free S-component can be expelled from the ECF module. Here we study this enigmatic expulsion step by cryogenic electron microscopy and reveal that ATP induces a concave-to-convex shape change of two long helices in the motor, thereby destroying the S-component’s docking site and allowing for its dissociation. We show that adaptation of the membrane morphology to the conformational state of the motor may favour expulsion of the substrate-free S-component when ATP is bound and docking of the substrate-loaded S-component after hydrolysis. Our work provides a picture of bilayer-assisted chemo-mechanical coupling in the transport cycle of ECF transporters. |
| first_indexed | 2024-03-12T21:08:16Z |
| format | Article |
| id | doaj.art-a86a02f4371e40bf9108dd6718f5be87 |
| institution | Directory Open Access Journal |
| issn | 2041-1723 |
| language | English |
| last_indexed | 2024-03-12T21:08:16Z |
| publishDate | 2023-07-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj.art-a86a02f4371e40bf9108dd6718f5be872023-07-30T11:19:13ZengNature PortfolioNature Communications2041-17232023-07-0114111410.1038/s41467-023-40266-1Expulsion mechanism of the substrate-translocating subunit in ECF transportersChancievan Thangaratnarajah0Mark Nijland1Luís Borges-Araújo2Aike Jeucken3Jan Rheinberger4Siewert J. Marrink5Paulo C. T. Souza6Cristina Paulino7Dirk J. Slotboom8Faculty of Science and Engineering, Groningen Biomolecular Sciences and Biotechnology, Membrane Enzymology Group, University of GroningenFaculty of Science and Engineering, Groningen Biomolecular Sciences and Biotechnology, Membrane Enzymology Group, University of GroningenMolecular Microbiology and Structural Biochemistry, CNRS and University of LyonFaculty of Science and Engineering, Groningen Biomolecular Sciences and Biotechnology, Membrane Enzymology Group, University of GroningenFaculty of Science and Engineering, Groningen Biomolecular Sciences and Biotechnology, Membrane Enzymology Group, University of GroningenFaculty of Science and Engineering, Groningen Biomolecular Sciences and Biotechnology, Molecular Dynamics Group, University of GroningenMolecular Microbiology and Structural Biochemistry, CNRS and University of LyonFaculty of Science and Engineering, Groningen Biomolecular Sciences and Biotechnology, Membrane Enzymology Group, University of GroningenFaculty of Science and Engineering, Groningen Biomolecular Sciences and Biotechnology, Membrane Enzymology Group, University of GroningenAbstract Energy-coupling factor (ECF)-type transporters mediate the uptake of micronutrients in many bacteria. They consist of a substrate-translocating subunit (S-component) and an ATP-hydrolysing motor (ECF module) Previous data indicate that the S-component topples within the membrane to alternately expose the binding site to either side of the membrane. In many ECF transporters, the substrate-free S-component can be expelled from the ECF module. Here we study this enigmatic expulsion step by cryogenic electron microscopy and reveal that ATP induces a concave-to-convex shape change of two long helices in the motor, thereby destroying the S-component’s docking site and allowing for its dissociation. We show that adaptation of the membrane morphology to the conformational state of the motor may favour expulsion of the substrate-free S-component when ATP is bound and docking of the substrate-loaded S-component after hydrolysis. Our work provides a picture of bilayer-assisted chemo-mechanical coupling in the transport cycle of ECF transporters.https://doi.org/10.1038/s41467-023-40266-1 |
| spellingShingle | Chancievan Thangaratnarajah Mark Nijland Luís Borges-Araújo Aike Jeucken Jan Rheinberger Siewert J. Marrink Paulo C. T. Souza Cristina Paulino Dirk J. Slotboom Expulsion mechanism of the substrate-translocating subunit in ECF transporters Nature Communications |
| title | Expulsion mechanism of the substrate-translocating subunit in ECF transporters |
| title_full | Expulsion mechanism of the substrate-translocating subunit in ECF transporters |
| title_fullStr | Expulsion mechanism of the substrate-translocating subunit in ECF transporters |
| title_full_unstemmed | Expulsion mechanism of the substrate-translocating subunit in ECF transporters |
| title_short | Expulsion mechanism of the substrate-translocating subunit in ECF transporters |
| title_sort | expulsion mechanism of the substrate translocating subunit in ecf transporters |
| url | https://doi.org/10.1038/s41467-023-40266-1 |
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