Intersubunit Coupling Enables Fast CO 2 -Fixation by Reductive Carboxylases
Abstract
Enoyl-CoA carboxylases/reductases (ECRs) are some of the most efficient CO2-fixing enzymes described to date. However, the molecular mechanisms underlying the extraordinary catalytic activity of ECRs on the level of the protein assembly remain elusive. Here we used a combination of ambient-temperature X-ray free electron laser (XFEL) and cryogenic synchrotron experiments to study the structural organization of the ECR from Kitasatospora setae. The K. setae ECR is a homotetramer that differentiates into a pair of dimers of open- and closed-form subunits in the catalytically active state. Using molecular dynamics simulations and structure-based mutagenesis, we show that catalysis is synchronized in the K. setae ECR across the pair of dimers. This conformational coupling of catalytic domains is conferred by individual amino acids to achieve high CO2-fixation rates. Our results provide unprecedented insights into the dynamic organization and synchronized inter- and intrasubunit communications of this remarkably efficient CO2-fixing enzyme during catalysis.
- Authors:
-
[4];
[5];
[9];
[13]
more »
- Biosciences Division, SLAC National Accelerator Laboratory Menlo Park, California 94025, United States, PULSE Institute, SLAC National Accelerator Laboratory Menlo Park, California 94025, United States, Department of Molecular Biology and Genetics, Koc University, 34450 Sariyer/Istanbul, Turkey
- Biosciences Division, SLAC National Accelerator Laboratory Menlo Park, California 94025, United States, Departamento de Físico Química, Facultad de Ciencias Químicas, Universidad de Concepción, Concepción 4030000, Chile
- Department of Biochemistry and Synthetic Metabolism, Max Planck Institute for Terrestrial Microbiology, Karl-von-Frisch-Straße 10, D-35043 Marburg, Germany
- Departamento de Físico Química, Facultad de Ciencias Químicas, Universidad de Concepción, Concepción 4030000, Chile
- Linac Coherent Light Source, SLAC National Accelerator Laboratory Menlo Park, California 94025, United States
- Biosciences Division, SLAC National Accelerator Laboratory Menlo Park, California 94025, United States, Structural Biology Department, Stanford University Stanford, California 94305, United States
- Biosciences Division, SLAC National Accelerator Laboratory Menlo Park, California 94025, United States, PULSE Institute, SLAC National Accelerator Laboratory Menlo Park, California 94025, United States
- PULSE Institute, SLAC National Accelerator Laboratory Menlo Park, California 94025, United States
- Biosciences Division, SLAC National Accelerator Laboratory Menlo Park, California 94025, United States, Electrical Engineering Department, Stanford University Stanford, California 94305, United States
- Structural Biology Department, Stanford University Stanford, California 94305, United States
- RIKEN SPring-8 Center, Sayo, Hyogo 679-5148, Japan, Japan Synchrotron Radiation Research Institute, Sayo, Hyogo 679-5198, Japan
- Departamento de Físico Química, Facultad de Ciencias Químicas, Universidad de Concepción, Concepción 4030000, Chile, Departamento de Farmacia, Facultad de Farmacia, Universidad de Concepción, Concepción 00000, Chile
- U.S. Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Walnut Creek, California 94720, United States
- Department of Theoretical and Computational Biophysics, Max Planck Institute for Multidisciplinary Sciences, Am Fassberg 11, 37077 Göttingen, Germany
- Department of Biochemistry and Synthetic Metabolism, Max Planck Institute for Terrestrial Microbiology, Karl-von-Frisch-Straße 10, D-35043 Marburg, Germany, LOEWE Center for Synthetic Microbiology (SYNMIKRO), 35032 Marburg, Germany
- Publication Date:
- Research Org.:
- Stanford Univ., CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Office of Science (SC), Basic Energy Sciences (BES); National Science Foundation (NSF); Scientific and Technological Research Council of Turkey; Max Planck Society
- OSTI Identifier:
- 1864615
- Alternate Identifier(s):
- OSTI ID: 1885561; OSTI ID: 1894096
- Grant/Contract Number:
- AC02-76SF00515; AC02-05CH11231
- Resource Type:
- Published Article
- Journal Name:
- ACS Central Science
- Additional Journal Information:
- Journal Name: ACS Central Science Journal Volume: 8 Journal Issue: 8; Journal ID: ISSN 2374-7943
- Publisher:
- American Chemical Society
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; Adenine; Catalysis; Oligomers; Surface interactions
Citation Formats
DeMirci, Hasan, Rao, Yashas, Stoffel, Gabriele M., Vögeli, Bastian, Schell, Kristina, Gomez, Aharon, Batyuk, Alexander, Gati, Cornelius, Sierra, Raymond G., Hunter, Mark S., Dao, E. Han, Ciftci, Halil I., Hayes, Brandon, Poitevin, Fredric, Li, Po-Nan, Kaur, Manat, Tono, Kensuke, Saez, David Adrian, Deutsch, Samuel, Yoshikuni, Yasuo, Grubmüller, Helmut, Erb, Tobias J., Vöhringer-Martinez, Esteban, and Wakatsuki, Soichi. Intersubunit Coupling Enables Fast CO 2 -Fixation by Reductive Carboxylases. United States: N. p., 2022.
Web. doi:10.1021/acscentsci.2c00057.
DeMirci, Hasan, Rao, Yashas, Stoffel, Gabriele M., Vögeli, Bastian, Schell, Kristina, Gomez, Aharon, Batyuk, Alexander, Gati, Cornelius, Sierra, Raymond G., Hunter, Mark S., Dao, E. Han, Ciftci, Halil I., Hayes, Brandon, Poitevin, Fredric, Li, Po-Nan, Kaur, Manat, Tono, Kensuke, Saez, David Adrian, Deutsch, Samuel, Yoshikuni, Yasuo, Grubmüller, Helmut, Erb, Tobias J., Vöhringer-Martinez, Esteban, & Wakatsuki, Soichi. Intersubunit Coupling Enables Fast CO 2 -Fixation by Reductive Carboxylases. United States. https://doi.org/10.1021/acscentsci.2c00057
DeMirci, Hasan, Rao, Yashas, Stoffel, Gabriele M., Vögeli, Bastian, Schell, Kristina, Gomez, Aharon, Batyuk, Alexander, Gati, Cornelius, Sierra, Raymond G., Hunter, Mark S., Dao, E. Han, Ciftci, Halil I., Hayes, Brandon, Poitevin, Fredric, Li, Po-Nan, Kaur, Manat, Tono, Kensuke, Saez, David Adrian, Deutsch, Samuel, Yoshikuni, Yasuo, Grubmüller, Helmut, Erb, Tobias J., Vöhringer-Martinez, Esteban, and Wakatsuki, Soichi. Mon .
"Intersubunit Coupling Enables Fast CO 2 -Fixation by Reductive Carboxylases". United States. https://doi.org/10.1021/acscentsci.2c00057.
@article{osti_1864615,
title = {Intersubunit Coupling Enables Fast CO 2 -Fixation by Reductive Carboxylases},
author = {DeMirci, Hasan and Rao, Yashas and Stoffel, Gabriele M. and Vögeli, Bastian and Schell, Kristina and Gomez, Aharon and Batyuk, Alexander and Gati, Cornelius and Sierra, Raymond G. and Hunter, Mark S. and Dao, E. Han and Ciftci, Halil I. and Hayes, Brandon and Poitevin, Fredric and Li, Po-Nan and Kaur, Manat and Tono, Kensuke and Saez, David Adrian and Deutsch, Samuel and Yoshikuni, Yasuo and Grubmüller, Helmut and Erb, Tobias J. and Vöhringer-Martinez, Esteban and Wakatsuki, Soichi},
abstractNote = {Enoyl-CoA carboxylases/reductases (ECRs) are some of the most efficient CO2-fixing enzymes described to date. However, the molecular mechanisms underlying the extraordinary catalytic activity of ECRs on the level of the protein assembly remain elusive. Here we used a combination of ambient-temperature X-ray free electron laser (XFEL) and cryogenic synchrotron experiments to study the structural organization of the ECR from Kitasatospora setae. The K. setae ECR is a homotetramer that differentiates into a pair of dimers of open- and closed-form subunits in the catalytically active state. Using molecular dynamics simulations and structure-based mutagenesis, we show that catalysis is synchronized in the K. setae ECR across the pair of dimers. This conformational coupling of catalytic domains is conferred by individual amino acids to achieve high CO2-fixation rates. Our results provide unprecedented insights into the dynamic organization and synchronized inter- and intrasubunit communications of this remarkably efficient CO2-fixing enzyme during catalysis.},
doi = {10.1021/acscentsci.2c00057},
journal = {ACS Central Science},
number = 8,
volume = 8,
place = {United States},
year = {Mon Apr 25 00:00:00 EDT 2022},
month = {Mon Apr 25 00:00:00 EDT 2022}
}
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