Multivalent interactions between CsoS2 and Rubisco mediate α-carboxysome formation
Abstract
Carboxysomes are bacterial microcompartments that function as the centerpiece of the bacterial CO2-concentrating mechanism by facilitating high CO2 concentrations near the carboxylase Rubisco. The carboxysome self-assembles from thousands of individual proteins into icosahedral-like particles with a dense enzyme cargo encapsulated within a proteinaceous shell. In the case of the α-carboxysome, there is little molecular insight into protein–protein interactions that drive the assembly process. In this work, studies on the α-carboxysome from Halothiobacillus neapolitanus demonstrate that Rubisco interacts with the N terminus of CsoS2, a multivalent, intrinsically disordered protein. X-ray structural analysis of the CsoS2 interaction motif bound to Rubisco reveals a series of conserved electrostatic interactions that are only made with properly assembled hexadecameric Rubisco. Although biophysical measurements indicate that this single interaction is weak, its implicit multivalency induces high-affinity binding through avidity. Taken together, our results indicate that CsoS2 acts as an interaction hub to condense Rubisco and enable efficient α-carboxysome formation.
- Authors:
-
[1];
[2];
[1]
- Univ. of California, Berkeley, CA (United States)
- Univ. of California, Berkeley, CA (United States). California Inst. for Quantitative Biosciences
- Publication Date:
- Research Org.:
- University of California, Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC); University of California; National Institutes of Health (NIH)
- OSTI Identifier:
- 1802884
- Grant/Contract Number:
- SC0016240; MR-15-328599; R01 GM124149; P30 GM124169; R01GM129241; R01GM050945
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Nature Structural & Molecular Biology
- Additional Journal Information:
- Journal Volume: 27; Journal Issue: 3; Journal ID: ISSN 1545-9993
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Biochemistry & molecular biology; Biophysics; Cell biology; Proteins; X-ray crystallography
Citation Formats
Oltrogge, Luke M., Chaijarasphong, Thawatchai, Chen, Allen W., Bolin, Eric R., Marqusee, Susan, and Savage, David F. Multivalent interactions between CsoS2 and Rubisco mediate α-carboxysome formation. United States: N. p., 2020.
Web. doi:10.1038/s41594-020-0387-7.
Oltrogge, Luke M., Chaijarasphong, Thawatchai, Chen, Allen W., Bolin, Eric R., Marqusee, Susan, & Savage, David F. Multivalent interactions between CsoS2 and Rubisco mediate α-carboxysome formation. United States. https://doi.org/10.1038/s41594-020-0387-7
Oltrogge, Luke M., Chaijarasphong, Thawatchai, Chen, Allen W., Bolin, Eric R., Marqusee, Susan, and Savage, David F. Mon .
"Multivalent interactions between CsoS2 and Rubisco mediate α-carboxysome formation". United States. https://doi.org/10.1038/s41594-020-0387-7. https://www.osti.gov/servlets/purl/1802884.
@article{osti_1802884,
title = {Multivalent interactions between CsoS2 and Rubisco mediate α-carboxysome formation},
author = {Oltrogge, Luke M. and Chaijarasphong, Thawatchai and Chen, Allen W. and Bolin, Eric R. and Marqusee, Susan and Savage, David F.},
abstractNote = {Carboxysomes are bacterial microcompartments that function as the centerpiece of the bacterial CO2-concentrating mechanism by facilitating high CO2 concentrations near the carboxylase Rubisco. The carboxysome self-assembles from thousands of individual proteins into icosahedral-like particles with a dense enzyme cargo encapsulated within a proteinaceous shell. In the case of the α-carboxysome, there is little molecular insight into protein–protein interactions that drive the assembly process. In this work, studies on the α-carboxysome from Halothiobacillus neapolitanus demonstrate that Rubisco interacts with the N terminus of CsoS2, a multivalent, intrinsically disordered protein. X-ray structural analysis of the CsoS2 interaction motif bound to Rubisco reveals a series of conserved electrostatic interactions that are only made with properly assembled hexadecameric Rubisco. Although biophysical measurements indicate that this single interaction is weak, its implicit multivalency induces high-affinity binding through avidity. Taken together, our results indicate that CsoS2 acts as an interaction hub to condense Rubisco and enable efficient α-carboxysome formation.},
doi = {10.1038/s41594-020-0387-7},
journal = {Nature Structural & Molecular Biology},
number = 3,
volume = 27,
place = {United States},
year = {Mon Mar 02 00:00:00 EST 2020},
month = {Mon Mar 02 00:00:00 EST 2020}
}
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