Carboxysomes: metabolic modules for CO2 fixation

Turmo, Aiko; Gonzalez-Esquer, Cesar Raul; Kerfeld, Cheryl A.

doi:10.1093/femsle/fnx176

Title: Carboxysomes: metabolic modules for CO₂ fixation

Journal Article · 14 August 2017 · FEMS Microbiology Letters (Online)

DOI: https://doi.org/10.1093/femsle/fnx176 · OSTI ID:1409782

Turmo, Aiko ^[1]; Gonzalez-Esquer, Cesar Raul ^[2]; Kerfeld, Cheryl A. ^[3]

Michigan State Univ., East Lansing, MI (United States)
Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
Michigan State Univ., East Lansing, MI (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Berkeley Synthetic Biology Inst., CA (United States)

The carboxysome is a bacterial microcompartment encapsulating the enzymes carbonic anhydrase and ribulose-1,5-bisphosphate carboxylase/oxygenase. As the site of CO₂ fixation, it serves an essential role in the carbon dioxide concentrating mechanism of many chemoautotrophs and all cyanobacteria. Carboxysomes and other bacterial microcompartments self-assemble through specific protein–protein interactions that are typically mediated by conserved protein domains. In this review, we frame our current understanding of carboxysomes in the context of their component protein domains with their inherent function as the ‘building blocks’ of carboxysomes. These building blocks are organized in genetic modules (conserved chromosomal loci) that encode for carboxysomes and ancillary proteins essential for the integration of the organelle with the rest of cellular metabolism. This conceptual framework provides the foundation for ‘plug-and-play’ engineering of carboxysomes as CO₂ fixation modules in a variety of biotechnological applications.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Los Alamos National Laboratory (LANL), Los Alamos, NM (United States); Colorado School of Mines, Golden, CO (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: AC52-06NA25396; FG02-91ER20021; E0007089; EE0007089

OSTI ID:: 1409782

Alternate ID(s):: OSTI ID: 1843736

Report Number(s):: LA-UR-17-25514

Journal Information:: FEMS Microbiology Letters (Online), Vol. 364, Issue 18; ISSN 1574-6968

Publisher:: Federation of European Microbiological SocietiesCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 59 works

Citation information provided by
Web of Science

References (92)

Bacterial microcompartments and the modular construction of microbial metabolism Kerfeld, Cheryl A.; Erbilgin, Onur Trends in Microbiology, Vol. 23, Issue 1 https://doi.org/10.1016/j.tim.2014.10.003	journal	January 2015
Aaa Proteins Vale, Ronald D. Journal of Cell Biology, Vol. 150, Issue 1 https://doi.org/10.1083/jcb.150.1.f13	journal	July 2000
Isolation of a Putative Carboxysomal Carbonic Anhydrase Gene from the Cyanobacterium Synechococcus PCC7942 Yu, Jian-Wei; Price, G. Dean; Song, Lirong Plant Physiology, Vol. 100, Issue 2 https://doi.org/10.1104/pp.100.2.794	journal	October 1992
The Carbon-Concentrating Mechanism of the Hydrothermal Vent Chemolithoautotroph Thiomicrospira crunogena Dobrinski, K. P.; Longo, D. L.; Scott, K. M. Journal of Bacteriology, Vol. 187, Issue 16 https://doi.org/10.1128/JB.187.16.5761-5766.2005	journal	August 2005
The Carboxysome Shell Is Permeable to Protons Menon, B. B.; Heinhorst, S.; Shively, J. M. Journal of Bacteriology, Vol. 192, Issue 22 https://doi.org/10.1128/JB.00903-10	journal	September 2010
Organization, Structure, and Assembly of α-Carboxysomes Determined by Electron Cryotomography of Intact Cells Iancu, Cristina V.; Morris, Dylan M.; Dou, Zhicheng Journal of Molecular Biology, Vol. 396, Issue 1 https://doi.org/10.1016/j.jmb.2009.11.019	journal	February 2010
Linked Rubisco Subunits Can Assemble into Functional Oligomers without Impeding Catalytic Performance Whitney, S. M.; Sharwood, R. E. Journal of Biological Chemistry, Vol. 282, Issue 6 https://doi.org/10.1074/jbc.M610479200	journal	November 2006
Plug-and-play for improving primary productivity Kerfeld, Cheryl A. American Journal of Botany, Vol. 102, Issue 12 https://doi.org/10.3732/ajb.1500409	journal	December 2015
Comparison of the crystal structures of L2 and L8S8 Rubisco suggests a functional role for the small subunit. Schneider, G.; Knight, S.; Andersson, I. The EMBO Journal, Vol. 9, Issue 7 https://doi.org/10.1002/j.1460-2075.1990.tb07371.x	journal	July 1990
A bioarchitectonic approach to the modular engineering of metabolism Kerfeld, Cheryl A. Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 372, Issue 1730 https://doi.org/10.1098/rstb.2016.0387	journal	August 2017
β-Carboxysomal proteins assemble into highly organized structures in Nicotiana chloroplasts Lin, Myat T.; Occhialini, Alessandro; Andralojc, P. John The Plant Journal, Vol. 79, Issue 1 https://doi.org/10.1111/tpj.12536	journal	June 2014
Bacterial Microcompartments Bobik, Thomas A. Microbe Magazine, Vol. 2, Issue 1 https://doi.org/10.1128/microbe.2.25.1	journal	January 2007
From molecular to modular cell biology Hartwell, Leland H.; Hopfield, John J.; Leibler, Stanislas Nature, Vol. 402, Issue S6761 https://doi.org/10.1038/35011540	journal	December 1999
Association of Carbonic Anhydrase Activity with Carboxysomes Isolated from the Cyanobacterium Synechococcus PCC7942 Price, G. Dean; Coleman, John R.; Badger, Murray R. Plant Physiology, Vol. 100, Issue 2 https://doi.org/10.1104/pp.100.2.784	journal	October 1992
Proteomic assessment of an established technique for carboxysome enrichment from Synechococcus PCC7942 Long, Ben M.; Price, G. Dean; Badger, Murray R. Canadian Journal of Botany, Vol. 83, Issue 7 https://doi.org/10.1139/b05-058	journal	July 2005
A Novel Evolutionary Lineage of Carbonic Anhydrase ( Class) Is a Component of the Carboxysome Shell So, A. K. -C.; Espie, G. S.; Williams, E. B. Journal of Bacteriology, Vol. 186, Issue 3 https://doi.org/10.1128/JB.186.3.623-630.2004	journal	January 2004
A Taxonomy of Bacterial Microcompartment Loci Constructed by a Novel Scoring Method Axen, Seth D.; Erbilgin, Onur; Kerfeld, Cheryl A. PLoS Computational Biology, Vol. 10, Issue 10 https://doi.org/10.1371/journal.pcbi.1003898	journal	October 2014
Crystal structure of the active site of ribulose-bisphosphate carboxylase Andersson, Inger; Knight, Stefan; Schneider, Gunter Nature, Vol. 337, Issue 6204 https://doi.org/10.1038/337229a0	journal	January 1989
Crystallographic analysis of ribulose 1,5-bisphosphate carboxylase from spinach at 2·4 Å resolution Knight, Stefan; Andersson, Inger; Brändén, Carl-Ivar Journal of Molecular Biology, Vol. 215, Issue 1 https://doi.org/10.1016/S0022-2836(05)80100-7	journal	September 1990
Structural Analysis of CsoS1A and the Protein Shell of the Halothiobacillus neapolitanus Carboxysome Tsai, Yingssu; Sawaya, Michael R.; Cannon, Gordon C. PLoS Biology, Vol. 5, Issue 6 https://doi.org/10.1371/journal.pbio.0050144	journal	May 2007
Microcompartments in Prokaryotes: Carboxysomes and Related Polyhedra Cannon, G. C.; Bradburne, C. E.; Aldrich, H. C. Applied and Environmental Microbiology, Vol. 67, Issue 12 https://doi.org/10.1128/AEM.67.12.5351-5361.2001	journal	December 2001
Structure and function of Rubisco Andersson, Inger; Backlund, Anders Plant Physiology and Biochemistry, Vol. 46, Issue 3 https://doi.org/10.1016/j.plaphy.2008.01.001	journal	March 2008
Evidence for the role of carboxysomes in the cyanobacterial CO ₂ -concentrating mechanism Price, G. Dean; Badger, Murray R. Canadian Journal of Botany, Vol. 69, Issue 5 https://doi.org/10.1139/b91-124	journal	May 1991
Spatially Ordered Dynamics of the Bacterial Carbon Fixation Machinery Savage, D. F.; Afonso, B.; Chen, A. H. Science, Vol. 327, Issue 5970 https://doi.org/10.1126/science.1186090	journal	March 2010
Isolation and Characterization of the Prochlorococcus Carboxysome Reveal the Presence of the Novel Shell Protein CsoS1D Roberts, E. W.; Cai, F.; Kerfeld, C. A. Journal of Bacteriology, Vol. 194, Issue 4 https://doi.org/10.1128/JB.06444-11	journal	December 2011
Modularity of a carbon-fixing protein organelle Bonacci, W.; Teng, P. K.; Afonso, B. Proceedings of the National Academy of Sciences, Vol. 109, Issue 2 https://doi.org/10.1073/pnas.1108557109	journal	December 2011
Programmed Ribosomal Frameshifting Mediates Expression of the α-Carboxysome Chaijarasphong, Thawatchai; Nichols, Robert J.; Kortright, Kaitlyn E. Journal of Molecular Biology, Vol. 428, Issue 1 https://doi.org/10.1016/j.jmb.2015.11.017	journal	January 2016
The structure, kinetics and interactions of the β-carboxysomal β-carbonic anhydrase, CcaA McGurn, Leah D.; Moazami-Goudarzi, Maryam; White, Sean A. Biochemical Journal, Vol. 473, Issue 24 https://doi.org/10.1042/BCJ20160773	journal	December 2016
The Pfam protein families database: towards a more sustainable future Finn, Robert D.; Coggill, Penelope; Eberhardt, Ruth Y. Nucleic Acids Research, Vol. 44, Issue D1 https://doi.org/10.1093/nar/gkv1344	journal	December 2015
ISOLATION OF ccmKLMN GENES FROM THE MARINE CYANOBACTERIUM, SYNECHOCOCCUS SP. PCC7002 (CYANOPHYCEAE), AND EVIDENCE THAT CcmM IS ESSENTIAL FOR CARBOXYSOME ASSEMBLY Ludwig, Martha; Sültemeyer, Dieter; Price, G. Dean Journal of Phycology, Vol. 36, Issue 6 https://doi.org/10.1046/j.1529-8817.2000.00028.x	journal	December 2000
Bacterial microcompartment assembly: The key role of encapsulation peptides Aussignargues, Clément; Paasch, Bradley C.; Gonzalez-Esquer, Raul Communicative & Integrative Biology, Vol. 8, Issue 3 https://doi.org/10.1080/19420889.2015.1039755	journal	May 2015
Dissociation of Ribulose-1,5-Bisphosphate Bound to Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase and Its Enhancement by Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase Activase-Mediated Hydrolysis of ATP Wang, Zhen Yuan; Portis, Archie R. Plant Physiology, Vol. 99, Issue 4 https://doi.org/10.1104/pp.99.4.1348	journal	August 1992
Streamlined Construction of the Cyanobacterial CO ₂ -Fixing Organelle via Protein Domain Fusions for Use in Plant Synthetic Biology Gonzalez-Esquer, C. Raul; Shubitowski, Tyler B.; Kerfeld, Cheryl A. The Plant Cell, Vol. 27, Issue 9 https://doi.org/10.1105/tpc.15.00329	journal	August 2015
Bacterial microcompartments as metabolic modules for plant synthetic biology Gonzalez-Esquer, C. Raul; Newnham, Sarah E.; Kerfeld, Cheryl A. The Plant Journal, Vol. 87, Issue 1 https://doi.org/10.1111/tpj.13166	journal	June 2016
Analysis of a genomic DNA region from the cyanobacterium Synechococcus sp. strain PCC7942 involved in carboxysome assembly and function. Price, G. D.; Howitt, S. M.; Harrison, K. Journal of Bacteriology, Vol. 175, Issue 10 https://doi.org/10.1128/jb.175.10.2871-2879.1993	journal	May 1993
Cyanobacterial-based approaches to improving photosynthesis in plants Zarzycki, Jan; Axen, Seth D.; Kinney, James N. Journal of Experimental Botany, Vol. 64, Issue 3 https://doi.org/10.1093/jxb/ers294	journal	October 2012
CO ₂ CONCENTRATING MECHANISMS IN PHOTOSYNTHETIC MICROORGANISMS Kaplan, Aaron; Reinhold, Leonora Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 50, Issue 1 https://doi.org/10.1146/annurev.arplant.50.1.539	journal	June 1999
The second wave of synthetic biology: from modules to systems Purnick, Priscilla E. M.; Weiss, Ron Nature Reviews Molecular Cell Biology, Vol. 10, Issue 6 https://doi.org/10.1038/nrm2698	journal	June 2009
Structure and function of the AAA+ protein CbbX, a red-type Rubisco activase Mueller-Cajar, Oliver; Stotz, Mathias; Wendler, Petra Nature, Vol. 479, Issue 7372 https://doi.org/10.1038/nature10568	journal	November 2011
Characterization of the Carboxysomal Carbonic Anhydrase CsoSCA from Halothiobacillus neapolitanus Heinhorst, S.; Williams, E. B.; Cai, F. Journal of Bacteriology, Vol. 188, Issue 23 https://doi.org/10.1128/JB.00990-06	journal	September 2006
Using comparative genomics to uncover new kinds of protein-based metabolic organelles in bacteria: Bacterial Microcompartments Jorda, Julien; Lopez, David; Wheatley, Nicole M. Protein Science, Vol. 22, Issue 2 https://doi.org/10.1002/pro.2196	journal	January 2013
The Structure of CcmP, a Tandem Bacterial Microcompartment Domain Protein from the β-Carboxysome, Forms a Subcompartment Within a Microcompartment Cai, Fei; Sutter, Markus; Cameron, Jeffrey C. Journal of Biological Chemistry, Vol. 288, Issue 22 https://doi.org/10.1074/jbc.M113.456897	journal	April 2013
Biochemical characterization of predicted Precambrian RuBisCO Shih, Patrick M.; Occhialini, Alessandro; Cameron, Jeffrey C. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms10382	journal	January 2016
Two new high-resolution crystal structures of carboxysome pentamer proteins reveal high structural conservation of CcmL orthologs among distantly related cyanobacterial species Sutter, Markus; Wilson, Steven C.; Deutsch, Samuel Photosynthesis Research, Vol. 118, Issue 1-2 https://doi.org/10.1007/s11120-013-9909-z	journal	August 2013
Comparing the in Vivo Function of α-Carboxysomes and β-Carboxysomes in Two Model Cyanobacteria Whitehead, Lynne; Long, Benedict M.; Price, G. Dean Plant Physiology, Vol. 165, Issue 1 https://doi.org/10.1104/pp.114.237941	journal	March 2014
Carboxysomal Carbonic Anhydrases Kimber, Matthew S. Subcellular Biochemistry https://doi.org/10.1007/978-94-007-7359-2_6	book	September 2013
Crystal structures of β-carboxysome shell protein CcmP: ligand binding correlates with the closed or open central pore Larsson, Anna M.; Hasse, Dirk; Valegård, Karin Journal of Experimental Botany, Vol. 68, Issue 14 https://doi.org/10.1093/jxb/erx070	journal	March 2017
Identification and Structural Analysis of a Novel Carboxysome Shell Protein with Implications for Metabolite Transport Klein, Michael G.; Zwart, Peter; Bagby, Sarah C. Journal of Molecular Biology, Vol. 392, Issue 2 https://doi.org/10.1016/j.jmb.2009.03.056	journal	September 2009
The ins and outs of CO ₂ Raven, John A.; Beardall, John Journal of Experimental Botany, Vol. 67, Issue 1 https://doi.org/10.1093/jxb/erv451	journal	October 2015
Protein Structures Forming the Shell of Primitive Bacterial Organelles Kerfeld, C. A. Science, Vol. 309, Issue 5736 https://doi.org/10.1126/science.1113397	journal	August 2005
Unusual Small Subunit That Is Not Expressed in Photosynthetic Cells Alters the Catalytic Properties of Rubisco in Rice Morita, K.; Hatanaka, T.; Misoo, S. PLANT PHYSIOLOGY, Vol. 164, Issue 1 https://doi.org/10.1104/pp.113.228015	journal	November 2013
The Pentameric Vertex Proteins Are Necessary for the Icosahedral Carboxysome Shell to Function as a CO2 Leakage Barrier Cai, Fei; Menon, Balaraj B.; Cannon, Gordon C. PLoS ONE, Vol. 4, Issue 10 https://doi.org/10.1371/journal.pone.0007521	journal	October 2009
Identification and characterization of a carboxysomal γ-carbonic anhydrase from the cyanobacterium Nostoc sp. PCC 7120 de Araujo, Charlotte; Arefeen, Dewan; Tadesse, Yohannes Photosynthesis Research, Vol. 121, Issue 2-3 https://doi.org/10.1007/s11120-014-0018-4	journal	June 2014
Interactions and structural variability of β-carboxysomal shell protein CcmL Keeling, Thomas J.; Samborska, Bożena; Demers, Ryan W. Photosynthesis Research, Vol. 121, Issue 2-3 https://doi.org/10.1007/s11120-014-9973-z	journal	February 2014
Plastome Engineering of Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase in Tobacco to Form a Sunflower Large Subunit and Tobacco Small Subunit Hybrid Kanevski, Ivan; Maliga, Pal; Rhoades, Daniel F. Plant Physiology, Vol. 119, Issue 1 https://doi.org/10.1104/pp.119.1.133	journal	January 1999
A Multiprotein Bicarbonate Dehydration Complex Essential to Carboxysome Function in Cyanobacteria Cot, S. S. -W.; So, A. K. -C.; Espie, G. S. Journal of Bacteriology, Vol. 190, Issue 3 https://doi.org/10.1128/JB.01283-07	journal	November 2007
Structural Characterization of a Newly Identified Component of α-Carboxysomes: The AAA+ Domain Protein CsoCbbQ Sutter, Markus; Roberts, Evan W.; Gonzalez, Raul C. Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep16243	journal	November 2015
Advances in Understanding Carboxysome Assembly in Prochlorococcus and Synechococcus Implicate CsoS2 as a Critical Component Cai, Fei; Dou, Zhicheng; Bernstein, Susan Life, Vol. 5, Issue 2 https://doi.org/10.3390/life5021141	journal	March 2015
Modularity and evolutionary constraint on proteins Fraser, Hunter B. Nature Genetics, Vol. 37, Issue 4 https://doi.org/10.1038/ng1530	journal	March 2005
CO2-concentrating mechanism in cyanobacterial photosynthesis: organization, physiological role, and evolutionary origin Kupriyanova, Elena V.; Sinetova, Maria A.; Cho, Sung Mi Photosynthesis Research, Vol. 117, Issue 1-3 https://doi.org/10.1007/s11120-013-9860-z	journal	June 2013
Halothiobacillus neapolitanus Carboxysomes Sequester Heterologous and Chimeric RubisCO Species Menon, Balaraj B.; Dou, Zhicheng; Heinhorst, Sabine PLoS ONE, Vol. 3, Issue 10 https://doi.org/10.1371/journal.pone.0003570	journal	October 2008
Carboxysomal carbonic anhydrases: Structure and role in microbial CO2 fixation Cannon, Gordon C.; Heinhorst, Sabine; Kerfeld, Cheryl A. Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1804, Issue 2 https://doi.org/10.1016/j.bbapap.2009.09.026	journal	February 2010
Structural Determinants of the Outer Shell of β-Carboxysomes in Synechococcus elongatus PCC 7942: Roles for CcmK2, K3-K4, CcmO, and CcmL Rae, Benjamin D.; Long, Benedict M.; Badger, Murray R. PLoS ONE, Vol. 7, Issue 8 https://doi.org/10.1371/journal.pone.0043871	journal	August 2012
AAA+ proteins: diversity in function, similarity in structure Snider, Jamie; Houry, Walid A. Biochemical Society Transactions, Vol. 36, Issue 1 https://doi.org/10.1042/BST0360072	journal	January 2008
Functional Cyanobacterial β -Carboxysomes Have an Absolute Requirement for Both Long and Short Forms of the CcmM Protein Long, Benedict M.; Tucker, Loraine; Badger, Murray R. Plant Physiology, Vol. 153, Issue 1 https://doi.org/10.1104/pp.110.154948	journal	March 2010
Functions, Compositions, and Evolution of the Two Types of Carboxysomes: Polyhedral Microcompartments That Facilitate CO2 Fixation in Cyanobacteria and Some Proteobacteria Rae, B. D.; Long, B. M.; Badger, M. R. Microbiology and Molecular Biology Reviews, Vol. 77, Issue 3 https://doi.org/10.1128/MMBR.00061-12	journal	September 2013
Carboxysomes: The Genes of Thiobacillus Neapolitanus Shively, Jessup M.; Lorbach, Stanley C.; Jin, Songmo Microbial Growth on C1 Compounds https://doi.org/10.1007/978-94-009-0213-8_9	book	January 1996
Bacterial Microcompartments Kerfeld, Cheryl A.; Heinhorst, Sabine; Cannon, Gordon C. Annual Review of Microbiology, Vol. 64, Issue 1 https://doi.org/10.1146/annurev.micro.112408.134211	journal	October 2010
AAA proteins Lupas, A. Current Opinion in Structural Biology, Vol. 12, Issue 6 https://doi.org/10.1016/S0959-440X(02)00388-3	journal	December 2002
The CO2concentrating mechanism in cyanobactiria and microalgae Badger, Murray R.; Price, G. Dean Physiologia Plantarum, Vol. 84, Issue 4 https://doi.org/10.1111/j.1399-3054.1992.tb04711.x	journal	April 1992
Short N-terminal sequences package proteins into bacterial microcompartments Fan, C.; Cheng, S.; Liu, Y. Proceedings of the National Academy of Sciences, Vol. 107, Issue 16 https://doi.org/10.1073/pnas.0913199107	journal	March 2010
A faster Rubisco with potential to increase photosynthesis in crops Lin, Myat T.; Occhialini, Alessandro; Andralojc, P. John Nature, Vol. 513, Issue 7519 https://doi.org/10.1038/nature13776	journal	September 2014
Assembly principles and structure of a 6.5-MDa bacterial microcompartment shell Sutter, Markus; Greber, Basil; Aussignargues, Clement Science, Vol. 356, Issue 6344 https://doi.org/10.1126/science.aan3289	journal	June 2017
Assembly, function and evolution of cyanobacterial carboxysomes Kerfeld, Cheryl A.; Melnicki, Matthew R. Current Opinion in Plant Biology, Vol. 31 https://doi.org/10.1016/j.pbi.2016.03.009	journal	June 2016
Atomic-Level Models of the Bacterial Carboxysome Shell Tanaka, S.; Kerfeld, C. A.; Sawaya, M. R. Science, Vol. 319, Issue 5866 https://doi.org/10.1126/science.1151458	journal	February 2008
The correlation of the gene csoS2 of the carboxysome operon with two polypeptides of the carboxysome in Thiobacillus neapolitanus Baker, S. H.; Lorbach, S. C.; Rodriguez-Buey, M. Archives of Microbiology, Vol. 172, Issue 4 https://doi.org/10.1007/s002030050765	journal	September 1999
Cyanobacterial CO2-concentrating mechanism components: function and prospects for plant metabolic engineering Long, Benedict M.; Rae, Benjamin D.; Rolland, Vivien Current Opinion in Plant Biology, Vol. 31 https://doi.org/10.1016/j.pbi.2016.03.002	journal	June 2016
A Dodecameric CcmK2 Structure Suggests β-Carboxysomal Shell Facets Have a Double-Layered Organization Samborska, Bożena; Kimber, Matthew S. Structure, Vol. 20, Issue 8 https://doi.org/10.1016/j.str.2012.05.013	journal	August 2012
Elucidating Essential Role of Conserved Carboxysomal Protein CcmN Reveals Common Feature of Bacterial Microcompartment Assembly Kinney, James N.; Salmeen, Annette; Cai, Fei Journal of Biological Chemistry, Vol. 287, Issue 21 https://doi.org/10.1074/jbc.M112.355305	journal	March 2012
Biogenesis of a Bacterial Organelle: The Carboxysome Assembly Pathway Cameron, Jeffrey C.; Wilson, Steven C.; Bernstein, Susan L. Cell, Vol. 155, Issue 5 https://doi.org/10.1016/j.cell.2013.10.044	journal	November 2013
Identification and characterization of multiple rubisco activases in chemoautotrophic bacteria Tsai, Yi-Chin Candace; Lapina, Maria Claribel; Bhushan, Shashi Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms9883	journal	November 2015
A gene homologous to chloroplast carbonic anhydrase (icfA) is essential to photosynthetic carbon dioxide fixation by Synechococcus PCC7942. Fukuzawa, H.; Suzuki, E.; Komukai, Y. Proceedings of the National Academy of Sciences, Vol. 89, Issue 10 https://doi.org/10.1073/pnas.89.10.4437	journal	May 1992
Bacterial microcompartments moving into a synthetic biological world Frank, Stefanie; Lawrence, Andrew D.; Prentice, Michael B. Journal of Biotechnology, Vol. 163, Issue 2 https://doi.org/10.1016/j.jbiotec.2012.09.002	journal	January 2013
Evolution and diversity of CO2 concentrating mechanisms in cyanobacteria Badger, Murray R.; Hanson, David; Price, G. Dean Functional Plant Biology, Vol. 29, Issue 3 https://doi.org/10.1071/PP01213	journal	January 2002
Structural basis of the oxidative activation of the carboxysomal -carbonic anhydrase, CcmM Pena, K. L.; Castel, S. E.; de Araujo, C. Proceedings of the National Academy of Sciences, Vol. 107, Issue 6 https://doi.org/10.1073/pnas.0910866107	journal	January 2010
Characterization of a mutant lacking carboxysomal carbonic anhydrase from the cyanobacterium Synechocystis PCC6803 So, Anthony K.; John-McKay, Meryl; Espie, George S. Planta, Vol. 214, Issue 3 https://doi.org/10.1007/s004250100638	journal	September 2001
Analysis of Carboxysomes from Synechococcus PCC7942 Reveals Multiple Rubisco Complexes with Carboxysomal Proteins CcmM and CcaA Long, Benedict M.; Badger, Murray R.; Whitney, Spencer M. Journal of Biological Chemistry, Vol. 282, Issue 40 https://doi.org/10.1074/jbc.M703896200	journal	August 2007
Comparative analysis of carboxysome shell proteins Kinney, James N.; Axen, Seth D.; Kerfeld, Cheryl A. Photosynthesis Research, Vol. 109, Issue 1-3 https://doi.org/10.1007/s11120-011-9624-6	journal	January 2011
The Bacterial Carbon-Fixing Organelle Is Formed by Shell Envelopment of Preassembled Cargo Chen, Anna H.; Robinson-Mosher, Avi; Savage, David F. PLoS ONE, Vol. 8, Issue 9 https://doi.org/10.1371/journal.pone.0076127	journal	September 2013
The Structure of β-Carbonic Anhydrase from the Carboxysomal Shell Reveals a Distinct Subclass with One Active Site for the Price of Two Sawaya, Michael R.; Cannon, Gordon C.; Heinhorst, Sabine Journal of Biological Chemistry, Vol. 281, Issue 11 https://doi.org/10.1074/jbc.M510464200	journal	January 2006
Transgenic tobacco plants with improved cyanobacterial Rubisco expression but no extra assembly factors grow at near wild-type rates if provided with elevated CO ₂ Occhialini, Alessandro; Lin, Myat T.; Andralojc, P. John The Plant Journal, Vol. 85, Issue 1 https://doi.org/10.1111/tpj.13098	journal	December 2015
CO ₂ Fixation Kinetics of Halothiobacillus neapolitanus Mutant Carboxysomes Lacking Carbonic Anhydrase Suggest the Shell Acts as a Diffusional Barrier for CO ₂ Dou, Zhicheng; Heinhorst, Sabine; Williams, Eric B. Journal of Biological Chemistry, Vol. 283, Issue 16 https://doi.org/10.1074/jbc.M709285200	journal	February 2008

Cited By (14)

Structures of maintenance of carboxysome distribution Walker-box McdA and McdB adaptor homologs Schumacher, Maria A.; Henderson, Max; Zhang, Hengshan Nucleic Acids Research, Vol. 47, Issue 11 https://doi.org/10.1093/nar/gkz314	journal	May 2019
Photobioreactor cultivation strategies for microalgae and cyanobacteria Johnson, Tylor J.; Katuwal, Sarmila; Anderson, Gary A. Biotechnology Progress, Vol. 34, Issue 4 https://doi.org/10.1002/btpr.2628	journal	March 2018
Nanoreactor Design Based on Self-Assembling Protein Nanocages Ren, Huimei; Zhu, Shaozhou; Zheng, Guojun International Journal of Molecular Sciences, Vol. 20, Issue 3 https://doi.org/10.3390/ijms20030592	journal	January 2019
Comparative Genomic Analysis Reveals Novel Microcompartment-Associated Metabolic Pathways in the Human Gut Microbiome Ravcheev, Dmitry A.; Moussu, Lubin; Smajic, Semra Frontiers in Genetics, Vol. 10 https://doi.org/10.3389/fgene.2019.00636	journal	July 2019
Bacterial microcompartments Kerfeld, Cheryl A.; Aussignargues, Clement; Zarzycki, Jan Nature Reviews Microbiology, Vol. 16, Issue 5 https://doi.org/10.1038/nrmicro.2018.10	journal	March 2018
Bacterial Microcompartments Kerfeld, Cheryl A.; Heinhorst, Sabine; Cannon, Gordon C. Annual Review of Microbiology, Vol. 64, Issue 1 https://doi.org/10.1146/annurev.micro.112408.134211	journal	October 2010
Bacterial Microcompartments Bobik, Thomas A. Microbe Magazine, Vol. 2, Issue 1 https://doi.org/10.1128/microbe.2.25.1	journal	January 2007
Minimalist Protocell Design: A Molecular System Based Solely on Proteins that Form Dynamic Vesicular Membranes Embedding Enzymatic Functions Huber, Matthias C.; Schreiber, Andreas; Schiller, Stefan M. ChemBioChem, Vol. 20, Issue 20 https://doi.org/10.1002/cbic.201900283	journal	August 2019
Encapsulation mechanisms and structural studies of GRM2 bacterial microcompartment particles Kalnins, Gints; Cesle, Eva-Emilija; Jansons, Juris Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-019-14205-y	journal	January 2020
Deciphering molecular details in the assembly of alpha-type carboxysome Liu, Yilan; He, Xinyuan; Lim, Weiping Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-33074-x	journal	October 2018
The Phenix software for automated determination of macromolecular structures Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Methods, Vol. 55, Issue 1 https://doi.org/10.1016/j.ymeth.2011.07.005	journal	September 2011
Encapsulation mechanisms and structural studies of GRM2 bacterial microcompartment particles Kalnins, Gints; Cesle, Eva-Emilija; Jansons, Juris Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-019-14205-y	journal	January 2020
Deciphering molecular details in the assembly of alpha-type carboxysome Liu, Yilan; He, Xinyuan; Lim, Weiping Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-33074-x	journal	October 2018
Nanoreactor Design Based on Self-Assembling Protein Nanocages Ren, Huimei; Zhu, Shaozhou; Zheng, Guojun International Journal of Molecular Sciences, Vol. 20, Issue 3 https://doi.org/10.3390/ijms20030592	journal	January 2019

Similar Records

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

Journal Article · 2015 · Scientific Reports · OSTI ID:1256062

Sutter, Markus; Roberts, Evan W.; Gonzalez, Raul C.; +6 more

Heterohexamers Formed by CcmK₃ and CcmK₄ Increase the Complexity of Beta Carboxysome Shells

Journal Article · 2019 · Plant Physiology (Bethesda) · OSTI ID:1480559

Sommer, Manuel; Sutter, Markus; Gupta, Sayan; +12 more

Bacterial microcompartments as metabolic modules for plant synthetic biology

Journal Article · 2016 · The Plant Journal · OSTI ID:1400750

Gonzalez‐Esquer, C. Raul; Newnham, Sarah E.; Kerfeld, Cheryl A.

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
cyanobacteria
carbon fixation
carboxysome
modularity
protein domains
synthetic biology
09 BIOMASS FUELS

Title: Carboxysomes: metabolic modules for CO2 fixation

Citation Formats

References (92)

Cited By (14)

Similar Records

Related Subjects

Title: Carboxysomes: metabolic modules for CO₂ fixation