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Title: Structural Characterization of a Newly Identified Component of α-Carboxysomes: The AAA+ Domain Protein CsoCbbQ

Abstract

Carboxysomes are bacterial microcompartments that enhance carbon fixation by concentrating ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO) and its substrate CO2 within a proteinaceous shell. They are found in all cyanobacteria, some purple photoautotrophs and many chemoautotrophic bacteria. Carboxysomes consist of a protein shell that encapsulates several hundred molecules of RuBisCO, and contain carbonic anhydrase and other accessory proteins. Genes coding for carboxysome shell components and the encapsulated proteins are typically found together in an operon. The α-carboxysome operon is embedded in a cluster of additional, conserved genes that are presumably related to its function. In many chemoautotrophs, products of the expanded carboxysome locus include CbbO and CbbQ, a member of the AAA+ domain superfamily. We bioinformatically identified subtypes of CbbQ proteins and show that their genes frequently co-occur with both Form IA and Form II RuBisCO. The α-carboxysome-associated ortholog, CsoCbbQ, from Halothiobacillus neapolitanus forms a hexamer in solution and hydrolyzes ATP. The crystal structure shows that CsoCbbQ is a hexamer of the typical AAA+ domain; the additional C-terminal domain, diagnostic of the CbbQ subfamily, structurally fills the inter-monomer gaps, resulting in a distinctly hexagonal shape. Finally, we show that CsoCbbQ interacts with CsoCbbO and is a component of the carboxysome shell, the firstmore » example of ATPase activity associated with a bacterial microcompartment.« less

Authors:
 [1];  [2];  [3];  [2];  [2];  [2];  [2];  [2];  [4]
  1. Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  2. Univ. of Southern Mississippi, Hattiesburg, MS (United States)
  3. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  4. Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of California, Berkeley, CA (United States); Michigan State Univ., East Lansing, MI (United States). Dept. of Biochemistry and Molecular Biology
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22); National Science Foundation (NSF)
OSTI Identifier:
1256062
Alternate Identifier(s):
OSTI ID: 1415945
Grant/Contract Number:  
FG02-91ER20021; AC02-05CH11231; MCB-1244534
Resource Type:
Accepted Manuscript
Journal Name:
Scientific Reports
Additional Journal Information:
Journal Volume: 5; Journal ID: ISSN 2045-2322
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Sutter, Markus, Roberts, Evan W., Gonzalez, Raul C., Bates, Cassandra, Dawoud, Salma, Landry, Kimberly, Cannon, Gordon C., Heinhorst, Sabine, and Kerfeld, Cheryl A. Structural Characterization of a Newly Identified Component of α-Carboxysomes: The AAA+ Domain Protein CsoCbbQ. United States: N. p., 2015. Web. doi:10.1038/srep16243.
Sutter, Markus, Roberts, Evan W., Gonzalez, Raul C., Bates, Cassandra, Dawoud, Salma, Landry, Kimberly, Cannon, Gordon C., Heinhorst, Sabine, & Kerfeld, Cheryl A. Structural Characterization of a Newly Identified Component of α-Carboxysomes: The AAA+ Domain Protein CsoCbbQ. United States. doi:10.1038/srep16243.
Sutter, Markus, Roberts, Evan W., Gonzalez, Raul C., Bates, Cassandra, Dawoud, Salma, Landry, Kimberly, Cannon, Gordon C., Heinhorst, Sabine, and Kerfeld, Cheryl A. Thu . "Structural Characterization of a Newly Identified Component of α-Carboxysomes: The AAA+ Domain Protein CsoCbbQ". United States. doi:10.1038/srep16243. https://www.osti.gov/servlets/purl/1256062.
@article{osti_1256062,
title = {Structural Characterization of a Newly Identified Component of α-Carboxysomes: The AAA+ Domain Protein CsoCbbQ},
author = {Sutter, Markus and Roberts, Evan W. and Gonzalez, Raul C. and Bates, Cassandra and Dawoud, Salma and Landry, Kimberly and Cannon, Gordon C. and Heinhorst, Sabine and Kerfeld, Cheryl A.},
abstractNote = {Carboxysomes are bacterial microcompartments that enhance carbon fixation by concentrating ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO) and its substrate CO2 within a proteinaceous shell. They are found in all cyanobacteria, some purple photoautotrophs and many chemoautotrophic bacteria. Carboxysomes consist of a protein shell that encapsulates several hundred molecules of RuBisCO, and contain carbonic anhydrase and other accessory proteins. Genes coding for carboxysome shell components and the encapsulated proteins are typically found together in an operon. The α-carboxysome operon is embedded in a cluster of additional, conserved genes that are presumably related to its function. In many chemoautotrophs, products of the expanded carboxysome locus include CbbO and CbbQ, a member of the AAA+ domain superfamily. We bioinformatically identified subtypes of CbbQ proteins and show that their genes frequently co-occur with both Form IA and Form II RuBisCO. The α-carboxysome-associated ortholog, CsoCbbQ, from Halothiobacillus neapolitanus forms a hexamer in solution and hydrolyzes ATP. The crystal structure shows that CsoCbbQ is a hexamer of the typical AAA+ domain; the additional C-terminal domain, diagnostic of the CbbQ subfamily, structurally fills the inter-monomer gaps, resulting in a distinctly hexagonal shape. Finally, we show that CsoCbbQ interacts with CsoCbbO and is a component of the carboxysome shell, the first example of ATPase activity associated with a bacterial microcompartment.},
doi = {10.1038/srep16243},
journal = {Scientific Reports},
number = ,
volume = 5,
place = {United States},
year = {2015},
month = {11}
}

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