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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 Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES); 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. https://doi.org/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. https://doi.org/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 = {Thu Nov 05 00:00:00 EST 2015},
month = {Thu Nov 05 00:00:00 EST 2015}
}

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Works referenced in this record:

The Carbon-Concentrating Mechanism of the Hydrothermal Vent Chemolithoautotroph Thiomicrospira crunogena
journal, August 2005


Overview of the CCP 4 suite and current developments
journal, March 2011

  • Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D.
  • Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4
  • DOI: 10.1107/S0907444910045749

New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0
journal, March 2010

  • Guindon, Stéphane; Dufayard, Jean-François; Lefort, Vincent
  • Systematic Biology, Vol. 59, Issue 3
  • DOI: 10.1093/sysbio/syq010

Atomic-Level Models of the Bacterial Carboxysome Shell
journal, February 2008


The cbbQ Genes, Located Downstream of the Form I and Form II RubisCO Genes, Affect the Activity of Both RubisCOs
journal, November 1999

  • Hayashi, Nobuhiro R.; Arai, Hiroyuki; Kodama, Tohru
  • Biochemical and Biophysical Research Communications, Vol. 265, Issue 1
  • DOI: 10.1006/bbrc.1999.1103

Use of Electroporation To Generate a Thiobacillus neapolitanus Carboxysome Mutant.
journal, January 1995


Towards automated crystallographic structure refinement with phenix.refine
journal, March 2012

  • Afonine, Pavel V.; Grosse-Kunstleve, Ralf W.; Echols, Nathaniel
  • Acta Crystallographica Section D Biological Crystallography, Vol. 68, Issue 4
  • DOI: 10.1107/S0907444912001308

The rbcX Gene Product Promotes the Production and Assembly of Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase of Synechococcus sp. PCC7002 in Escherichia coli
journal, October 2004

  • Onizuka, Takuo; Endo, Sumiyo; Akiyama, Hideo
  • Plant and Cell Physiology, Vol. 45, Issue 10
  • DOI: 10.1093/pcp/pch160

Identification and Structural Analysis of a Novel Carboxysome Shell Protein with Implications for Metabolite Transport
journal, September 2009

  • Klein, Michael G.; Zwart, Peter; Bagby, Sarah C.
  • Journal of Molecular Biology, Vol. 392, Issue 2
  • DOI: 10.1016/j.jmb.2009.03.056

The Minimal CO 2 -Concentrating Mechanism of Prochlorococcus spp. MED4 Is Effective and Efficient
journal, October 2014

  • Hopkinson, Brian M.; Young, Jodi N.; Tansik, Anna L.
  • Plant Physiology, Vol. 166, Issue 4
  • DOI: 10.1104/pp.114.247049

A Novel Evolutionary Lineage of Carbonic Anhydrase (  Class) Is a Component of the Carboxysome Shell
journal, January 2004


A Taxonomy of Bacterial Microcompartment Loci Constructed by a Novel Scoring Method
journal, October 2014


Multiple Rubisco forms in proteobacteria: their functional significance in relation to CO2 acquisition by the CBB cycle
journal, February 2008

  • Badger, Murray Ronald; Bek, Emily Jane
  • Journal of Experimental Botany, Vol. 59, Issue 7
  • DOI: 10.1093/jxb/erm297

Organization of Carboxysome Genes in the Thiobacilli
journal, February 2003


XDS
journal, January 2010

  • Kabsch, Wolfgang
  • Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2
  • DOI: 10.1107/S0907444909047337

Characterization of a homogenous preparation of carboxysomes from Thiobacillus neapolitanus
journal, January 1983

  • Cannon, G. C.; Shively, J. M.
  • Archives of Microbiology, Vol. 134, Issue 1
  • DOI: 10.1007/BF00429407

Improving recombinant Rubisco biogenesis, plant photosynthesis and growth by coexpressing its ancillary RAF1 chaperone
journal, March 2015

  • Whitney, Spencer M.; Birch, Rosemary; Kelso, Celine
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 11
  • DOI: 10.1073/pnas.1420536112

The MoxR ATPase RavA and Its Cofactor ViaA Interact with the NADH:Ubiquinone Oxidoreductase I in Escherichia coli
journal, January 2014


Isolation and Characterization of the Prochlorococcus Carboxysome Reveal the Presence of the Novel Shell Protein CsoS1D
journal, December 2011

  • Roberts, E. W.; Cai, F.; Kerfeld, C. A.
  • Journal of Bacteriology, Vol. 194, Issue 4
  • DOI: 10.1128/JB.06444-11

Classification of AAA+ proteins
journal, October 2006

  • Ammelburg, Moritz; Frickey, Tancred; Lupas, Andrei N.
  • Journal of Structural Biology, Vol. 156, Issue 1
  • DOI: 10.1016/j.jsb.2006.05.002

ATP Binding and Hydrolysis and Autophosphorylation of CbbQ Encoded by the Gene Located Downstream of RubisCO Genes
journal, February 2002

  • Hayashi, Nobuhiro R.; Igarashi, Yasuo
  • Biochemical and Biophysical Research Communications, Vol. 290, Issue 5
  • DOI: 10.1006/bbrc.2002.6366

Carbon cycling: the prokaryotic contribution
journal, June 2001


Bioinformatic analysis of the distribution of inorganic carbon transporters and prospective targets for bioengineering to increase Ci uptake by cyanobacteria
journal, November 2014

  • Gaudana, Sandeep B.; Zarzycki, Jan; Moparthi, Vamsi K.
  • Photosynthesis Research, Vol. 126, Issue 1
  • DOI: 10.1007/s11120-014-0059-8

Coot model-building tools for molecular graphics
journal, November 2004

  • Emsley, Paul; Cowtan, Kevin
  • Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132
  • DOI: 10.1107/S0907444904019158

Cyanobacterial-based approaches to improving photosynthesis in plants
journal, October 2012

  • Zarzycki, Jan; Axen, Seth D.; Kinney, James N.
  • Journal of Experimental Botany, Vol. 64, Issue 3
  • DOI: 10.1093/jxb/ers294

Tackling unintelligent design
journal, January 2010


The Novel Genes,cbbQandcbbO,Located Downstream from the RubisCO Genes ofPseudomonas hydrogenothermophila,Affect the Conformational States and Activity of RubisCO
journal, December 1997

  • Hayashi, Nobuhiro R.; Arai, Hiroyuki; Kodama, Tohru
  • Biochemical and Biophysical Research Communications, Vol. 241, Issue 2
  • DOI: 10.1006/bbrc.1997.7853

Adenosine triphosphate hydrolysis by purified rubisco activase
journal, January 1989


Rubisco regulation: a role for inhibitors
journal, June 2007

  • Parry, M. A. J.; Keys, A. J.; Madgwick, P. J.
  • Journal of Experimental Botany, Vol. 59, Issue 7
  • DOI: 10.1093/jxb/ern084

Structure and function of the AAA+ protein CbbX, a red-type Rubisco activase
journal, November 2011

  • Mueller-Cajar, Oliver; Stotz, Mathias; Wendler, Petra
  • Nature, Vol. 479, Issue 7372
  • DOI: 10.1038/nature10568

Characterization of the Carboxysomal Carbonic Anhydrase CsoSCA from Halothiobacillus neapolitanus
journal, September 2006

  • Heinhorst, S.; Williams, E. B.; Cai, F.
  • Journal of Bacteriology, Vol. 188, Issue 23
  • DOI: 10.1128/JB.00990-06

The cbbQ Genes, Located Downstream of the Form I and Form II RubisCO Genes, Affect the Activity of Both RubisCOs
journal, November 1999

  • Hayashi, Nobuhiro R.; Arai, Hiroyuki; Kodama, Tohru
  • Biochemical and Biophysical Research Communications, Vol. 265, Issue 1
  • DOI: 10.1006/bbrc.1999.1103

Identification and Structural Analysis of a Novel Carboxysome Shell Protein with Implications for Metabolite Transport
journal, September 2009

  • Klein, Michael G.; Zwart, Peter; Bagby, Sarah C.
  • Journal of Molecular Biology, Vol. 392, Issue 2
  • DOI: 10.1016/j.jmb.2009.03.056

Long-Term Response toward Inorganic Carbon Limitation in Wild Type and Glycolate Turnover Mutants of the Cyanobacterium Synechocystis sp. Strain PCC 6803
journal, June 2007

  • Eisenhut, Marion; von Wobeser, Eneas Aguirre; Jonas, Ludwig
  • Plant Physiology, Vol. 144, Issue 4
  • DOI: 10.1104/pp.107.103341

The Pentameric Vertex Proteins Are Necessary for the Icosahedral Carboxysome Shell to Function as a CO2 Leakage Barrier
journal, October 2009


Structure and Identification of a Pterin Dehydratase-like Protein as a Ribulose-bisphosphate Carboxylase/Oxygenase (RuBisCO) Assembly Factor in the α-Carboxysome
journal, January 2014

  • Wheatley, Nicole M.; Sundberg, Christopher D.; Gidaniyan, Soheil D.
  • Journal of Biological Chemistry, Vol. 289, Issue 11
  • DOI: 10.1074/jbc.M113.531236

Manipulation of Rubisco: the amount, activity, function and regulation
journal, March 2003

  • Parry, M. A. J.
  • Journal of Experimental Botany, Vol. 54, Issue 386
  • DOI: 10.1093/jxb/erg141

Improving recombinant Rubisco biogenesis, plant photosynthesis and growth by coexpressing its ancillary RAF1 chaperone
journal, March 2015

  • Whitney, Spencer M.; Birch, Rosemary; Kelso, Celine
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 11
  • DOI: 10.1073/pnas.1420536112

Organization of Carboxysome Genes in the Thiobacilli
journal, February 2003


MoxR AAA+ ATPases: A novel family of molecular chaperones?
journal, October 2006


A Taxonomy of Bacterial Microcompartment Loci Constructed by a Novel Scoring Method
journal, October 2014


AAA+ proteins: diversity in function, similarity in structure
journal, January 2008

  • Snider, Jamie; Houry, Walid A.
  • Biochemical Society Transactions, Vol. 36, Issue 1
  • DOI: 10.1042/BST0360072

Functions, Compositions, and Evolution of the Two Types of Carboxysomes: Polyhedral Microcompartments That Facilitate CO2 Fixation in Cyanobacteria and Some Proteobacteria
journal, September 2013

  • Rae, B. D.; Long, B. M.; Badger, M. R.
  • Microbiology and Molecular Biology Reviews, Vol. 77, Issue 3
  • DOI: 10.1128/MMBR.00061-12

Structure and Function of RbcX, an Assembly Chaperone for Hexadecameric Rubisco
journal, June 2007


AAA proteins
journal, December 2002


The rbcX Gene Product Promotes the Production and Assembly of Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase of Synechococcus sp. PCC7002 in Escherichia coli
journal, October 2004

  • Onizuka, Takuo; Endo, Sumiyo; Akiyama, Hideo
  • Plant and Cell Physiology, Vol. 45, Issue 10
  • DOI: 10.1093/pcp/pch160

Proteasomes and other self-compartmentalizing proteases in prokaryotes
journal, February 1999


Transcript analysis of the Halothiobacillus neapolitanus cso operon
journal, September 2007


Multiple Rubisco forms in proteobacteria: their functional significance in relation to CO2 acquisition by the CBB cycle
journal, February 2008

  • Badger, Murray Ronald; Bek, Emily Jane
  • Journal of Experimental Botany, Vol. 59, Issue 7
  • DOI: 10.1093/jxb/erm297

Atomic-Level Models of the Bacterial Carboxysome Shell
journal, February 2008


The correlation of the gene csoS2 of the carboxysome operon with two polypeptides of the carboxysome in Thiobacillus neapolitanus
journal, September 1999

  • Baker, S. H.; Lorbach, S. C.; Rodriguez-Buey, M.
  • Archives of Microbiology, Vol. 172, Issue 4
  • DOI: 10.1007/s002030050765

WebLogo: A Sequence Logo Generator
journal, May 2004

  • Crooks, Gavin E.; Hon, Gary; Chandonia, John-Marc
  • Genome Research, Vol. 14, Issue 6, p. 1188-1190
  • DOI: 10.1101/gr.849004

Tackling unintelligent design
journal, January 2010


Carboxysomes and Carboxysome-like Inclusions
book, January 2006

  • Heinhorst, Sabine; Cannon, Gordon C.; Shively, Jessup M.
  • Microbiology Monographs
  • DOI: 10.1007/7171_023

The Pentameric Vertex Proteins Are Necessary for the Icosahedral Carboxysome Shell to Function as a CO2 Leakage Barrier
journal, October 2009


Bioinformatic analysis of the distribution of inorganic carbon transporters and prospective targets for bioengineering to increase Ci uptake by cyanobacteria
journal, November 2014

  • Gaudana, Sandeep B.; Zarzycki, Jan; Moparthi, Vamsi K.
  • Photosynthesis Research, Vol. 126, Issue 1
  • DOI: 10.1007/s11120-014-0059-8

Adenosine triphosphate hydrolysis by purified rubisco activase
journal, January 1989


Protein-based organelles in bacteria: carboxysomes and related microcompartments
journal, August 2008

  • Yeates, Todd O.; Kerfeld, Cheryl A.; Heinhorst, Sabine
  • Nature Reviews Microbiology, Vol. 6, Issue 9
  • DOI: 10.1038/nrmicro1913

ATP Binding and Hydrolysis and Autophosphorylation of CbbQ Encoded by the Gene Located Downstream of RubisCO Genes
journal, February 2002

  • Hayashi, Nobuhiro R.; Igarashi, Yasuo
  • Biochemical and Biophysical Research Communications, Vol. 290, Issue 5
  • DOI: 10.1006/bbrc.2002.6366

Rubisco regulation: a role for inhibitors
journal, June 2007

  • Parry, M. A. J.; Keys, A. J.; Madgwick, P. J.
  • Journal of Experimental Botany, Vol. 59, Issue 7
  • DOI: 10.1093/jxb/ern084

Structure and Function of RbcX, an Assembly Chaperone for Hexadecameric Rubisco
journal, June 2007


The MoxR ATPase RavA and Its Cofactor ViaA Interact with the NADH:Ubiquinone Oxidoreductase I in Escherichia coli
journal, January 2014


Cyanobacterial-based approaches to improving photosynthesis in plants
journal, October 2012

  • Zarzycki, Jan; Axen, Seth D.; Kinney, James N.
  • Journal of Experimental Botany, Vol. 64, Issue 3
  • DOI: 10.1093/jxb/ers294

Transcript analysis of the Halothiobacillus neapolitanus cso operon
journal, September 2007


The Structure of β-Carbonic Anhydrase from the Carboxysomal Shell Reveals a Distinct Subclass with One Active Site for the Price of Two
journal, January 2006

  • Sawaya, Michael R.; Cannon, Gordon C.; Heinhorst, Sabine
  • Journal of Biological Chemistry, Vol. 281, Issue 11
  • DOI: 10.1074/jbc.M510464200

CO 2 Fixation Kinetics of Halothiobacillus neapolitanus Mutant Carboxysomes Lacking Carbonic Anhydrase Suggest the Shell Acts as a Diffusional Barrier for CO 2
journal, February 2008

  • Dou, Zhicheng; Heinhorst, Sabine; Williams, Eric B.
  • Journal of Biological Chemistry, Vol. 283, Issue 16
  • DOI: 10.1074/jbc.M709285200

The Novel Genes,cbbQandcbbO,Located Downstream from the RubisCO Genes ofPseudomonas hydrogenothermophila,Affect the Conformational States and Activity of RubisCO
journal, December 1997

  • Hayashi, Nobuhiro R.; Arai, Hiroyuki; Kodama, Tohru
  • Biochemical and Biophysical Research Communications, Vol. 241, Issue 2
  • DOI: 10.1006/bbrc.1997.7853

MoxR AAA+ ATPases: A novel family of molecular chaperones?
journal, October 2006


Use of Electroporation To Generate a Thiobacillus neapolitanus Carboxysome Mutant.
journal, January 1995


Works referencing / citing this record:

Carboxysome encapsulation of the CO2-fixing enzyme Rubisco in tobacco chloroplasts
journal, September 2018


Insights into the mechanism and regulation of the CbbQO-type Rubisco activase, a MoxR AAA+ ATPase
journal, December 2019

  • Tsai, Yi-Chin Candace; Ye, Fuzhou; Liew, Lynette
  • Proceedings of the National Academy of Sciences, Vol. 117, Issue 1
  • DOI: 10.1073/pnas.1911123117

Bacterial microcompartments
journal, March 2018

  • Kerfeld, Cheryl A.; Aussignargues, Clement; Zarzycki, Jan
  • Nature Reviews Microbiology, Vol. 16, Issue 5
  • DOI: 10.1038/nrmicro.2018.10

Bacterial Microcompartments
journal, October 2010


Progress and challenges of engineering a biophysical CO2-concentrating mechanism into higher plants
journal, April 2017

  • Rae, Benjamin D.; Long, Benedict M.; Förster, Britta
  • Journal of Experimental Botany, Vol. 68, Issue 14
  • DOI: 10.1093/jxb/erx133

Assembly–disassembly is coupled to the ATPase cycle of tobacco Rubisco activase
journal, October 2018

  • Serban, Andrew J.; Breen, Isabella L.; Bui, Hoang Q.
  • Journal of Biological Chemistry, Vol. 293, Issue 50
  • DOI: 10.1074/jbc.ra118.005047

Cyanobacterial carboxysomes contain an unique rubisco‐activase‐like protein
journal, October 2019

  • Lechno‐Yossef, Sigal; Rohnke, Brandon A.; Belza, Ana C. O.
  • New Phytologist, Vol. 225, Issue 2
  • DOI: 10.1111/nph.16195

Bacterial Microcompartments
journal, January 2007


Carboxysomes: metabolic modules for CO2 fixation
journal, August 2017

  • Turmo, Aiko; Gonzalez-Esquer, C. Raul; Kerfeld, Cheryl A.
  • FEMS Microbiology Letters, Vol. 364, Issue 18
  • DOI: 10.1093/femsle/fnx176

Permanent draft genome of Thiobacillus thioparus DSM 505T, an obligately chemolithoautotrophic member of the Betaproteobacteria
journal, January 2017

  • Hutt, Lee P.; Huntemann, Marcel; Clum, Alicia
  • Standards in Genomic Sciences, Vol. 12, Issue 1
  • DOI: 10.1186/s40793-017-0229-3

From chaperonins to Rubisco assembly and metabolic repair: Role of Chaperones in Rubisco Biogenesis
journal, October 2017


The Diverse AAA+ Machines that Repair Inhibited Rubisco Active Sites
journal, May 2017


Rubisco Activases: AAA+ Chaperones Adapted to Enzyme Repair
journal, April 2017

  • Bhat, Javaid Y.; Thieulin-Pardo, Gabriel; Hartl, F. Ulrich
  • Frontiers in Molecular Biosciences, Vol. 4
  • DOI: 10.3389/fmolb.2017.00020

Permanent draft genome of Thiobacillus thioparus DSM 505T, an obligately chemolithoautotrophic member of the Betaproteobacteria
journal, January 2017

  • Hutt, Lee P.; Huntemann, Marcel; Clum, Alicia
  • Standards in Genomic Sciences, Vol. 12, Issue 1
  • DOI: 10.1186/s40793-017-0229-3