Cyanobacterial carboxysomes contain an unique rubisco-activase-like protein

Lechno‐Yossef, Sigal; Rohnke, Brandon A.; Belza, Ana O.; Melnicki, Matthew R.; Montgomery, Beronda L.; Kerfeld, Cheryl A.

doi:10.1111/nph.16195

Title: Cyanobacterial carboxysomes contain an unique rubisco-activase-like protein

Journal Article · 25 October 2019 · New Phytologist

DOI: https://doi.org/10.1111/nph.16195 · OSTI ID:1735821

^[1];

^[1]; Belza, Ana O. ^[1]; Melnicki, Matthew R. ^[1];

^[1];

^[2]

Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory
Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)

In plants, rubisco activase (Rca) regulates rubisco by removing inhibitory molecules such as ribulose–1,5–bisphosphate (RuBP). In cyanobacteria, a homologous protein (activase–like cyanobacterial protein, ALC), contains a distinctive C–terminal fusion resembling the small–subunit of rubisco. Although cyanobacterial rubisco is believed to be less sensitive to RuBP inhibition, the ALC is widely distributed among diverse cyanobacteria. Using microscopy, biochemistry and molecular biology, the cellular localization of the ALC, its effect on carboxysome/cell ultrastructure in Fremyella diplosiphon, and its function in vitro were studied. Bioinformatic analysis uncovered evolutionary relationships between the ALC and rubisco. ALC localizes to carboxysomes and exhibits ATPase activity. Furthermore, the ALC induces rubisco aggregation in a manner similar to that of another carboxysomal protein, M35, and this activity is affected by ATP. An alc deletion mutant showed modified cell morphology when grown under enriched CO₂ and impaired regulation of carboxysome biogenesis, without affecting growth rate. Carbamylation of Fremyella recombinant rubisco was inhibited by RuBP, but this inhibition was not relieved by the ALC. Here, the ALC does not appear to function like a canonical Rca; instead, it exerts an effect on the response to CO₂ availability at the level of a metabolic module, the carboxysome, through rubisco network formation, and carboxysome organization.

View Accepted Manuscript (DOE)

View Accepted Manuscript (Publisher)

Cite

Export

Save

Research Organization:: Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory

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

Grant/Contract Number:: FG02-91ER20021; FG02‐91ER20021

OSTI ID:: 1735821

Alternate ID(s):: OSTI ID: 1572105; OSTI ID: 1671328

Journal Information:: New Phytologist, Vol. 225, Issue 2; ISSN 0028-646X

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 20 works

Citation information provided by
Web of Science

References (89)

Additional families of orange carotenoid proteins in the photoprotective system of cyanobacteria Bao, Han; Melnicki, Matthew R.; Pawlowski, Emily G. Nature Plants, Vol. 3, Issue 8 https://doi.org/10.1038/nplants.2017.89	journal	July 2017
Light Modulates the Biosynthesis and Organization of Cyanobacterial Carbon Fixation Machinery through Photosynthetic Electron Flow Sun, Yaqi; Casella, Selene; Fang, Yi Plant Physiology, Vol. 171, Issue 1 https://doi.org/10.1104/pp.16.00107	journal	March 2016
A synthetic RNA editing factor edits its target site in chloroplasts and bacteria Royan, Santana; Gutmann, Bernard; Colas des Francs-Small, Catherine Communications Biology, Vol. 4, Issue 1 https://doi.org/10.1038/s42003-021-02062-9	journal	May 2021
The Rubisco activase (rca) gene is located downstream from rbcS in Anabaena sp. strain CA and is detected in other Anabaena/Nostoc strains Li, Lih-Ann; Janet, L. Plant Molecular Biology, Vol. 21, Issue 5 https://doi.org/10.1007/BF00027109	journal	March 1993
Transport as the basis of the kok effect. Levels of some photosynthetic intermediates and activation of light-regulated enzymes during photosynthesis of chloroplasts and green leaf protoplasts Heber, U.; Takahama, U.; Neimanis, S. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 679, Issue 2 https://doi.org/10.1016/0005-2728(82)90299-7	journal	February 1982
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
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
Spatial expression and autoregulation of hetR, a gene involved in the control of heterocyst development in Anabaena Black, Todd A.; Cai, Yuping; Wolk, C. Peter Molecular Microbiology, Vol. 10, Issue 5 https://doi.org/10.1111/j.1365-2958.1993.tb00985.x	journal	December 1993
Strong and regulated promoters in the cyanobacterium Anabaena PCC 7120 Elhai, Jeff FEMS Microbiology Letters, Vol. 114, Issue 2 https://doi.org/10.1111/j.1574-6968.1993.tb06570.x	journal	December 1993
New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0 Guindon, Stéphane; Dufayard, Jean-François; Lefort, Vincent Systematic Biology, Vol. 59, Issue 3 https://doi.org/10.1093/sysbio/syq010	journal	March 2010
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
Biogenesis and Metabolic Maintenance of Rubisco Bracher, Andreas; Whitney, Spencer M.; Hartl, F. Ulrich Annual Review of Plant Biology, Vol. 68, Issue 1 https://doi.org/10.1146/annurev-arplant-043015-111633	journal	April 2017
A Mutant of Arabidopsis thaliana Which Lacks Activation of RuBP Carboxylase In Vivo Somerville, C. R.; Portis, Archie R.; Ogren, William L. Plant Physiology, Vol. 70, Issue 2 https://doi.org/10.1104/pp.70.2.381	journal	August 1982
The mechanism of Rubisco activase: Insights from studies of the properties and structure of the enzyme Salvucci, Michael E.; Ogren, William L. Photosynthesis Research, Vol. 47, Issue 1 https://doi.org/10.1007/BF00017748	journal	January 1996
Rubisco Activase Activity Assays Barta, Csengele; Carmo-Silva, A. Elizabete; Salvucci, Michael E. Photosynthesis Research Protocols, p. 375-382 https://doi.org/10.1007/978-1-60761-925-3_29	book	January 2010
Structure of Arabidopsis thaliana Rubisco activase Hasse, Dirk; Larsson, Anna M.; Andersson, Inger Acta Crystallographica Section D Biological Crystallography, Vol. 71, Issue 4 https://doi.org/10.1107/S1399004715001182	journal	March 2015
The Diverse AAA+ Machines that Repair Inhibited Rubisco Active Sites Mueller-Cajar, Oliver Frontiers in Molecular Biosciences, Vol. 4 https://doi.org/10.3389/fmolb.2017.00031	journal	May 2017
Inhibition of ribulose bisphosphate carboxylase by substrate ribulose 1,5-bisphosphate. Jordan, D. B.; Chollet, R. Journal of Biological Chemistry, Vol. 258, Issue 22 https://doi.org/10.1016/S0021-9258(17)43982-2	journal	November 1983
Single-molecule diffusometry reveals the nucleotide-dependent oligomerization pathways of Nicotiana tabacum Rubisco activase Wang, Quan; Serban, Andrew J.; Wachter, Rebekka M. The Journal of Chemical Physics, Vol. 148, Issue 12 https://doi.org/10.1063/1.5005930	journal	March 2018
A hybrid ribulose bisphosphate carboxylase/oxygenase enzyme exhibiting a substantial increase in substrate specificity factor Read, Betsy A.; Tabita, F. Robert Biochemistry, Vol. 31, Issue 24 https://doi.org/10.1021/bi00139a018	journal	June 1992
Plant RuBisCo assembly in E. coli with five chloroplast chaperones including BSD2 Aigner, H.; Wilson, R. H.; Bracher, A. Science, Vol. 358, Issue 6368 https://doi.org/10.1126/science.aap9221	journal	December 2017
Generic Assignments, Strain Histories and Properties of Pure Cultures of Cyanobacteria Stanier, Roger Y.; Deruelles, Josette; Rippka, Rosmarie Microbiology, Vol. 111, Issue 1, p. 1-61 https://doi.org/10.1099/00221287-111-1-1	journal	March 1979
RuBisCo activase is present in the pyrenoid of green algae McKay, R. M. L.; Gibbs, Sarah P.; Vaughn, K. C. Protoplasma, Vol. 162, Issue 1 https://doi.org/10.1007/BF01403899	journal	February 1991
Mechanism of Enzyme Repair by the AAA+ Chaperone Rubisco Activase Bhat, Javaid Y.; Miličić, Goran; Thieulin-Pardo, Gabriel Molecular Cell, Vol. 67, Issue 5 https://doi.org/10.1016/j.molcel.2017.07.004	journal	September 2017
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
Structure of green-type Rubisco activase from tobacco Stotz, Mathias; Mueller-Cajar, Oliver; Ciniawsky, Susanne Nature Structural & Molecular Biology, Vol. 18, Issue 12 https://doi.org/10.1038/nsmb.2171	journal	November 2011
Maximum activity of recombinant ribulose 1,5-bisphosphate carboxylase/oxygenase of Anabaena sp. strain CA requires the product of the rbcX gene. Li, L. A.; Tabita, F. R. Journal of Bacteriology, Vol. 179, Issue 11 https://doi.org/10.1128/jb.179.11.3793-3796.1997	journal	June 1997
Ethylene-induced stomatal closure in Arabidopsis occurs via AtrbohF-mediated hydrogen peroxide synthesis Desikan, Radhika; Last, Kathryn; Harrett-Williams, Rhian The Plant Journal, Vol. 47, Issue 6 https://doi.org/10.1111/j.1365-313X.2006.02842.x	journal	September 2006
Kinetics and subunit interactions of ribulose bisphosphate carboxylase-oxygenase from the cyanobacterium, Synechococcus sp. Andrews, T. J.; Abel, K. M. Journal of Biological Chemistry, Vol. 256, Issue 16 https://doi.org/10.1016/S0021-9258(19)68863-0	journal	August 1981
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
Heterohexamers Formed by CcmK3 and CcmK4 Increase the Complexity of Beta Carboxysome Shells Sommer, Manuel; Sutter, Markus; Gupta, Sayan Plant Physiology, Vol. 179, Issue 1 https://doi.org/10.1104/pp.18.01190	journal	November 2018
Alterations in Global Patterns of Gene Expression in Synechocystis sp. PCC 6803 in Response to Inorganic Carbon Limitation and the Inactivation of ndhR , a LysR Family Regulator Wang, Hong-Liang; Postier, Bradley L.; Burnap, Robert L. Journal of Biological Chemistry, Vol. 279, Issue 7 https://doi.org/10.1074/jbc.M311336200	journal	November 2003
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
ATP and Magnesium Promote Cotton Short-Form Ribulose-1,5-bisphosphate Carboxylase/Oxygenase (Rubisco) Activase Hexamer Formation at Low Micromolar Concentrations Kuriata, Agnieszka M.; Chakraborty, Manas; Henderson, J. Nathan Biochemistry, Vol. 53, Issue 46 https://doi.org/10.1021/bi500968h	journal	November 2014
Activation of Ribulosebisphosphate Carboxylase/Oxygenase at Physiological CO ₂ and Ribulosebisphosphate Concentrations by Rubisco Activase Portis, Archie R.; Salvucci, Michael E.; Ogren, William L. Plant Physiology, Vol. 82, Issue 4 https://doi.org/10.1104/pp.82.4.967	journal	December 1986
New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0 Guindon, Stéphane; Dufayard, Jean-François; Lefort, Vincent Oxford University Press https://doi.org/10.5167/uzh-155669	text	January 2010
HMMER web server: 2018 update Potter, Simon C.; Luciani, Aurélien; Eddy, Sean R. Nucleic Acids Research, Vol. 46, Issue W1 https://doi.org/10.1093/nar/gky448	journal	June 2018
High Substrate Specificity Factor Ribulose Bisphosphate Carboxylase/Oxygenase from Eukaryotic Marine Algae and Properties of Recombinant Cyanobacterial Rubisco Containing "Algal" Residue Modifications Read, B. A.; Tabita, F. R. Archives of Biochemistry and Biophysics, Vol. 312, Issue 1 https://doi.org/10.1006/abbi.1994.1301	journal	July 1994
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
NIH Image to ImageJ: 25 years of image analysis Schneider, Caroline A.; Rasband, Wayne S.; Eliceiri, Kevin W. Nature Methods, Vol. 9, Issue 7 https://doi.org/10.1038/nmeth.2089	journal	June 2012
Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing Shih, P. M.; Wu, D.; Latifi, A. Proceedings of the National Academy of Sciences, Vol. 110, Issue 3, p. 1053-1058 https://doi.org/10.1073/pnas.1217107110	journal	December 2012
A Cytosolic Bypass and G6P Shunt in Plants Lacking Peroxisomal Hydroxypyruvate Reductase Li, Jiying; Weraduwage, Sarathi M.; Preiser, Alyssa L. Plant Physiology, Vol. 180, Issue 2 https://doi.org/10.1104/pp.19.00256	journal	March 2019
Evolution of Rubisco activase gene in plants Nagarajan, Ragupathi; Gill, Kulvinder S. Plant Molecular Biology, Vol. 96, Issue 1-2 https://doi.org/10.1007/s11103-017-0680-y	journal	November 2017
Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. Guzman, L. M.; Belin, D.; Carson, M. J. Journal of Bacteriology, Vol. 177, Issue 14, p. 4121-4130 https://doi.org/10.1128/jb.177.14.4121-4130.1995	journal	July 1995
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
A versatile class of positive-selection vectors based on the nonviability of palindrome-containing plasmids that allows cloning into long polylinkers Elhai, Jeff; Wolk, C. Peter Gene, Vol. 68, Issue 1 https://doi.org/10.1016/0378-1119(88)90605-1	journal	August 1988
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies Stamatakis, Alexandros Bioinformatics, Vol. 30, Issue 9 https://doi.org/10.1093/bioinformatics/btu033	journal	January 2014
New and versatile cloning vectors with kanamycin-resistance marker Pridmore, Raymond David Gene, Vol. 56, Issue 2-3 https://doi.org/10.1016/0378-1119(87)90149-1	journal	January 1987
Paired cloning vectors for complementation of mutations in the cyanobacterium Anabaena sp. strain PCC 7120 Wolk, C. Peter; Fan, Qing; Zhou, Ruanbao Archives of Microbiology, Vol. 188, Issue 6 https://doi.org/10.1007/s00203-007-0276-z	journal	July 2007
Adenosine triphosphate hydrolysis by purified rubisco activase Robinson, Simon P.; Portis, Archie R. Archives of Biochemistry and Biophysics, Vol. 268, Issue 1 https://doi.org/10.1016/0003-9861(89)90568-7	journal	January 1989
Light modulation of Rubisco in Arabidopsis requires a capacity for redox regulation of the larger Rubisco activase isoform Zhang, N.; Kallis, R. P.; Ewy, R. G. Proceedings of the National Academy of Sciences, Vol. 99, Issue 5 https://doi.org/10.1073/pnas.042529999	journal	February 2002
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
Chaperone Coexpression Plasmids: Differential and Synergistic Roles of DnaK-DnaJ-GrpE and GroEL-GroES in Assisting Folding of an Allergen of Japanese Cedar Pollen, Cryj2, inEscherichia coli Nishihara, Kazuyo; Kanemori, Masaaki; Kitagawa, Masanari Applied and Environmental Microbiology, Vol. 64, Issue 5 https://doi.org/10.1128/AEM.64.5.1694-1699.1998	journal	May 1998
Evolution of the Animal Apoptosis Network Zmasek, C. M.; Godzik, A. Cold Spring Harbor Perspectives in Biology, Vol. 5, Issue 3 https://doi.org/10.1101/cshperspect.a008649	journal	March 2013
Despite slow catalysis and confused substrate specificity, all ribulose bisphosphate carboxylases may be nearly perfectly optimized Tcherkez, G. G. B.; Farquhar, G. D.; Andrews, T. J. Proceedings of the National Academy of Sciences, Vol. 103, Issue 19 https://doi.org/10.1073/pnas.0600605103	journal	April 2006
Construction of Shuttle Plasmids Which Can Be Efficiently Mobilized from Escherichia coli into the Chromatically Adapting Cyanobacterium, Fremyella diplosiphon Cobley, John G.; Zerweck, Edward; Reyes, Richard Plasmid, Vol. 30, Issue 2 https://doi.org/10.1006/plas.1993.1037	journal	September 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
Rubisco condensate formation by CcmM in β-carboxysome biogenesis Wang, H.; Yan, X.; Aigner, H. Nature, Vol. 566, Issue 7742 https://doi.org/10.1038/s41586-019-0880-5	journal	January 2019
Rubisco Activase Is Required for Optimal Photosynthesis in the Green Alga Chlamydomonas reinhardtii in a Low-CO ₂ Atmosphere Pollock, Steve V.; Colombo, Sergio L.; Prout, Davey L. Plant Physiology, Vol. 133, Issue 4 https://doi.org/10.1104/pp.103.032078	journal	November 2003
The small RbcS-like domains of the β-carboxysome structural protein CcmM bind RubisCO at a site distinct from that binding the RbcS subunit Ryan, Patrick; Forrester, Taylor J. B.; Wroblewski, Charles Journal of Biological Chemistry, Vol. 294, Issue 8 https://doi.org/10.1074/jbc.RA118.006330	journal	December 2018
Isolation and characterization of the ccmM gene required by the cyanobacterium Synechocystis PCC6803 for inorganic carbon utilization Ogawa, Teruo; Amichay, Doron; Gurevitz, Michael Photosynthesis Research, Vol. 39, Issue 2 https://doi.org/10.1007/BF00029385	journal	February 1994
Control of electron flow in intact chloroplasts by the intrathylakoid pH, not by the phosphorylation potential Kobayashi, Yoshichika; Inoue, Yorinao; Shibata, Kazuo Planta, Vol. 146, Issue 4 https://doi.org/10.1007/BF00380864	journal	September 1979
Plasmids from two morphologically distinct cyanobacterial strains share a novel replication origin. Schaefer, M. R.; Chiang, G. G.; Cobley, J. G. Journal of Bacteriology, Vol. 175, Issue 17 https://doi.org/10.1128/jb.175.17.5701-5705.1993	journal	September 1993
Ribulose-1,5-Bis-Phosphate Carboxylase/Oxygenase Accumulation Factor1 Is Required for Holoenzyme Assembly in Maize Feiz, Leila; Williams-Carrier, Rosalind; Wostrikoff, Katia The Plant Cell, Vol. 24, Issue 8 https://doi.org/10.1105/tpc.112.102012	journal	August 2012
Nucleotide Dependence of Subunit Rearrangements in Short-Form Rubisco Activase from Spinach Peterson-Forbrook, Dayna S.; Hilton, Matthew T.; Tichacek, Laura Biochemistry, Vol. 56, Issue 36 https://doi.org/10.1021/acs.biochem.7b00574	journal	August 2017
Rubisco regulation: a role for inhibitors Parry, M. A. J.; Keys, A. J.; Madgwick, P. J. Journal of Experimental Botany, Vol. 59, Issue 7 https://doi.org/10.1093/jxb/ern084	journal	June 2007
Spatial expression and autoregulation of hetR, a gene involved in the control of heterocyst development in Anabaena Black, Todd A.; Cai, Yuping; Wolk, C. Peter Molecular Microbiology, Vol. 9, Issue 1 https://doi.org/10.1111/j.1365-2958.1993.tb01670.x	journal	July 1993
Reduction of conjugal transfer efficiency by three restriction activities of Anabaena sp. strain PCC 7120. Elhai, J.; Vepritskiy, A.; Muro-Pastor, A. M. Journal of Bacteriology, Vol. 179, Issue 6 https://doi.org/10.1128/jb.179.6.1998-2005.1997	journal	March 1997
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
A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally-located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants Hoang, Tung T.; Karkhoff-Schweizer, RoxAnn R.; Kutchma, Alecksandr J. Gene, Vol. 212, Issue 1 https://doi.org/10.1016/S0378-1119(98)00130-9	journal	May 1998
New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0 Guindon, Stéphane; Dufayard, Jean-François; Lefort, Vincent ETH Zurich https://doi.org/10.3929/ethz-b-000025281	text	January 2010
2′-Carboxy-D-arabitinol 1-phosphate protects ribulose 1,5-bisphosphate carboxylase/oxygenase against proteolytic breakdown: CA1P protects Rubisco against proteolysis Khan, Shahnaz; Andralojc, P. John; Lea, Peter J. European Journal of Biochemistry, Vol. 266, Issue 3 https://doi.org/10.1046/j.1432-1327.1999.00913.x	journal	December 1999
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
The most abundant protein in the world Ellis, R. John Trends in Biochemical Sciences, Vol. 4, Issue 11 https://doi.org/10.1016/0968-0004(79)90212-3	journal	November 1979
A Spatial Interactome Reveals the Protein Organization of the Algal CO2-Concentrating Mechanism Mackinder, Luke C. M.; Chen, Chris; Leib, Ryan D. Cell, Vol. 171, Issue 1 https://doi.org/10.1016/j.cell.2017.08.044	journal	September 2017
Specific Glucoside Transporters Influence Septal Structure and Function in the Filamentous, Heterocyst-Forming Cyanobacterium Anabaena sp. Strain PCC 7120 Nieves-Morión, Mercedes; Lechno-Yossef, Sigal; López-Igual, Rocío Journal of Bacteriology, Vol. 199, Issue 7 https://doi.org/10.1128/JB.00876-16	journal	January 2017
MAFFT version 5: improvement in accuracy of multiple sequence alignment Katoh, K. Nucleic Acids Research, Vol. 33, Issue 2 https://doi.org/10.1093/nar/gki198	journal	January 2005
Effects of light, temperature, pH, and inhibitors on the ATP level of the blue-green alga Anacystic nidulans Bornefeld, T.; Simonis, W. Planta, Vol. 115, Issue 4 https://doi.org/10.1007/BF00388613	journal	January 1974
RcaE-Dependent Regulation of Carboxysome Structural Proteins Has a Central Role in Environmental Determination of Carboxysome Morphology and Abundance in Fremyella diplosiphon Rohnke, Brandon A.; Singh, Shailendra P.; Pattanaik, Bagmi mSphere, Vol. 3, Issue 1 https://doi.org/10.1128/mSphere.00617-17	journal	January 2018
Catalytic by-product formation and ligand binding by ribulose bisphosphate carboxylases from different phylogenies Pearce, F. Grant Biochemical Journal, Vol. 399, Issue 3 https://doi.org/10.1042/BJ20060430	journal	October 2006
ATP pools and transients in the blue-green alga, Anabaena cylindrica Bottomley, P. J.; Stewart, W. D. P. Archives of Microbiology, Vol. 108, Issue 3 https://doi.org/10.1007/BF00454849	journal	January 1976
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies Stamatakis, A. Karlsruhe https://doi.org/10.5445/ir/1000045818	text	January 2014
β-Carboxysome bioinformatics: identification and evolution of new bacterial microcompartment protein gene classes and core locus constraints Sommer, Manuel; Cai, Fei; Melnicki, Matthew Journal of Experimental Botany, Vol. 68, Issue 14 https://doi.org/10.1093/jxb/erx115	journal	April 2017
Single-Organelle Quantification Reveals Stoichiometric and Structural Variability of Carboxysomes Dependent on the Environment Sun, Yaqi; Wollman, Adam J. M.; Huang, Fang The Plant Cell, Vol. 31, Issue 7 https://doi.org/10.1105/tpc.18.00787	journal	May 2019
Skylign: a tool for creating informative, interactive logos representing sequence alignments and profile hidden Markov models Wheeler, Travis J.; Clements, Jody; Finn, Robert D. BMC Bioinformatics, Vol. 15, Issue 1 https://doi.org/10.1186/1471-2105-15-7	journal	January 2014
Kinetic properties of ribulose 1,5-bisphosphate carboxylase/oxygenase from Anabaena variabilis Badger, Murray R. Archives of Biochemistry and Biophysics, Vol. 201, Issue 1 https://doi.org/10.1016/0003-9861(80)90509-3	journal	April 1980
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
AAA⁺: A Class of Chaperone-Like ATPases Associated with the Assembly, Operation, and Disassembly of Protein Complexes Neuwald, Andrew F.; Aravind, L.; Spouge, John L. Genome Research, Vol. 9, Issue 1 https://doi.org/10.1101/gr.9.1.27	journal	January 1999

Cited By (1)

Binding Options for the Small Subunit-Like Domain of Cyanobacteria to Rubisco Rohnke, Brandon A.; Kerfeld, Cheryl A.; Montgomery, Beronda L. Frontiers in Microbiology, Vol. 11 https://doi.org/10.3389/fmicb.2020.00187	journal	February 2020