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Title: Structural Analysis of CsoS1A and the Protein Shell of the Halothiobacillus neapolitanus Carboxysome

Abstract

The carboxysome is a bacterial organelle that functions to enhance the efficiency of CO2 fixation by encapsulating the enzymes ribulose bisphosphate carboxylase/oxygenase (RuBisCO) and carbonic anhydrase. The outer shell of the carboxysome is reminiscent of a viral capsid, being constructed from many copies of a few small proteins. Here we describe the structure of the shell protein CsoS1A from the chemoautotrophic bacterium Halothiobacillus neapolitanus. The CsoS1A protein forms hexameric units that pack tightly together to form a molecular layer, which is perforated by narrow pores. Sulfate ions, soaked into crystals of CsoS1A, are observed in the pores of the molecular layer, supporting the idea that the pores could be the conduit for negatively charged metabolites such as bicarbonate, which must cross the shell. The problem of diffusion across a semiporous protein shell is discussed, with the conclusion that the shell is sufficiently porous to allow adequate transport of small molecules. The molecular layer formed by CsoS1A is similar to the recently observed layers formed by cyanobacterial carboxysome shell proteins. This similarity supports the argument that the layers observed represent the natural structure of the facets of the carboxysome shell. Insights into carboxysome function are provided by comparisons of the carboxysomemore » shell to viral capsids, and a comparison of its pores to the pores of transmembrane protein channels.« less

Authors:
 [1];  [2];  [3];  [3];  [3];  [3];  [4];  [1]
  1. University of California, Los Angeles, CA (United States)
  2. University of California, Los Angeles, CA (United States); United States Department of Energy Institute for Genomics and Proteomics, Los Angeles, CA (United States)
  3. University of Southern Mississippi, Hattiesburg, MS (United States)
  4. University of California, Los Angeles, CA (United States). Life Sciences Core
Publication Date:
Research Org.:
Univ. of California, Los Angeles, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); USDA
OSTI Identifier:
1904011
Grant/Contract Number:  
2004-35318-14929
Resource Type:
Accepted Manuscript
Journal Name:
PLoS Biology (Online)
Additional Journal Information:
Journal Name: PLoS Biology (Online); Journal Volume: 5; Journal Issue: 6; Journal ID: ISSN 1545-7885
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; viral packaging; protein structure; sulfates; ribulose-1,5-bisphosphate carboxylase oxygenase; bicarbonates; carbon dioxide; viral structure; protein structure comparison

Citation Formats

Tsai, Yingssu, Sawaya, Michael R., Cannon, Gordon C., Cai, Fei, Williams, Eric B., Heinhorst, Sabine, Kerfeld, Cheryl A., and Yeates, Todd O. Structural Analysis of CsoS1A and the Protein Shell of the Halothiobacillus neapolitanus Carboxysome. United States: N. p., 2007. Web. doi:10.1371/journal.pbio.0050144.
Tsai, Yingssu, Sawaya, Michael R., Cannon, Gordon C., Cai, Fei, Williams, Eric B., Heinhorst, Sabine, Kerfeld, Cheryl A., & Yeates, Todd O. Structural Analysis of CsoS1A and the Protein Shell of the Halothiobacillus neapolitanus Carboxysome. United States. https://doi.org/10.1371/journal.pbio.0050144
Tsai, Yingssu, Sawaya, Michael R., Cannon, Gordon C., Cai, Fei, Williams, Eric B., Heinhorst, Sabine, Kerfeld, Cheryl A., and Yeates, Todd O. Tue . "Structural Analysis of CsoS1A and the Protein Shell of the Halothiobacillus neapolitanus Carboxysome". United States. https://doi.org/10.1371/journal.pbio.0050144. https://www.osti.gov/servlets/purl/1904011.
@article{osti_1904011,
title = {Structural Analysis of CsoS1A and the Protein Shell of the Halothiobacillus neapolitanus Carboxysome},
author = {Tsai, Yingssu and Sawaya, Michael R. and Cannon, Gordon C. and Cai, Fei and Williams, Eric B. and Heinhorst, Sabine and Kerfeld, Cheryl A. and Yeates, Todd O.},
abstractNote = {The carboxysome is a bacterial organelle that functions to enhance the efficiency of CO2 fixation by encapsulating the enzymes ribulose bisphosphate carboxylase/oxygenase (RuBisCO) and carbonic anhydrase. The outer shell of the carboxysome is reminiscent of a viral capsid, being constructed from many copies of a few small proteins. Here we describe the structure of the shell protein CsoS1A from the chemoautotrophic bacterium Halothiobacillus neapolitanus. The CsoS1A protein forms hexameric units that pack tightly together to form a molecular layer, which is perforated by narrow pores. Sulfate ions, soaked into crystals of CsoS1A, are observed in the pores of the molecular layer, supporting the idea that the pores could be the conduit for negatively charged metabolites such as bicarbonate, which must cross the shell. The problem of diffusion across a semiporous protein shell is discussed, with the conclusion that the shell is sufficiently porous to allow adequate transport of small molecules. The molecular layer formed by CsoS1A is similar to the recently observed layers formed by cyanobacterial carboxysome shell proteins. This similarity supports the argument that the layers observed represent the natural structure of the facets of the carboxysome shell. Insights into carboxysome function are provided by comparisons of the carboxysome shell to viral capsids, and a comparison of its pores to the pores of transmembrane protein channels.},
doi = {10.1371/journal.pbio.0050144},
journal = {PLoS Biology (Online)},
number = 6,
volume = 5,
place = {United States},
year = {Tue May 22 00:00:00 EDT 2007},
month = {Tue May 22 00:00:00 EDT 2007}
}

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