Carboxysome Structural Model

Carboxysomes are bacterial microcompartments (BMCs) consisting of polyhedral protein shells filled with the enzymes ribulose-1,5-bisphosphate carboxylase/oxygenase ( RuBisCO)—the predominant enzyme in carbon fixation and the rate limiting enzyme in the Calvin cycle—and carbonic anhydrase.

Carboxysomes are thought to have evolved as a consequence of the increase in oxygen concentration in the ancient atmosphere; this is because oxygen is a competing substrate to carbon dioxide in the RuBisCO reaction. To overcome the inefficiency of RuBisCO, carboxysomes concentrate carbon dioxide inside the shell by means of co-localized carbonic anhydrase activity, which produces carbon dioxide from the bicarbonate that diffuses into the carboxysome. The resulting concentration of carbon dioxide near RuBisCO decreases the proportion of ribulose-1,5-bisphosphate oxygenation and thereby avoids costly photorespiratory reactions. The surrounding shell provides a barrier to carbon dioxide loss, helping to increase its concentration around RuBisCO.

Carboxysomes are an essential part of the broader metabolic network called the Carbon dioxide-Concentrating Mechanism (CCM), which functions in two parts: (1) Membrane transporters concentrate inorganic carbon (C_i) in the cell cytosol which is devoid of carbonic anhydrases. Carbon is primarily stored in the form of HCO₃⁻ which cannot re-cross the lipid membrane, as opposed to neutral CO₂ which can easily escape the cell. This stockpiles carbon in the cell, creating a disequilibrium between the intracellular and extracellular environments of about 30x the C_i concentration in water. (2) Cytosolic HCO₃⁻ diffuses into the carboxysome, where carboxysomal carbonic anhydrases dehydrate it back to CO₂ in the vicinity of Rubisco, allowing Rubisco to operate at its maximal rate.

Carboxysomes are the best studied example of bacterial microcompartments, the term for functionally diverse organelles that are alike in having a protein shell.

Discovery

Polyhedral bodies were discovered by transmission electron microscopy in the cyanobacterium ''Phormidium uncinatum'' in 1956. These were later observed in other cyanobacteria and in some chemotrophic bacteria that fix carbon dioxide—many of them are sulfur oxidizers or nitrogen fixers (for example, '' Halothiobacillus'', ''Acidithiobacillus'', '' Nitrobacter'' and ''Nitrococcus''; all belonging to Pseudomonadota). The polyhedral bodies were first purified from ''Thiobacillus neapolitanus'' (now ''Halothiobacillus neapolitanus'') in 1973 and shown to contain RuBisCO, held within a rigid outer covering. The authors proposed that since these appeared to be organelles involved in carbon dioxide fixation, they should be called ''carboxysomes''.

Architecture

Structurally, carboxysomes are icosahedral, or quasi- icosahedral. Electron cryo-tomography studies have confirmed the approximately icosahedral geometry of the carboxysome, and have imaged Rubisco proteins inside arranged in a few concentric layers or fibril-like structures. The non-icosahedral faceted shapes of some carboxysomes can naturally be explained within the elastic theory of heterogeneous thin shells.

Shell proteins

The carboxysome has an outer shell composed of a few thousand protein subunits, with hexameric shell proteins populating the faces and pentameric shell proteins placed at the 12 icosahedral vertices. Proteins known to form the shell have been structurally characterized by X-ray crystallography. The proteins that constitute the majority of the shell form cyclical hexamers or pseudo-hexamers and belong to the BMC protein family. Small pores perforate many different types of BMC-H hexamers, and may serve as the route for diffusion of small substrates (e.g. bicarbonate) and products (3-phosphoglycerate) into and out of the carboxysome. Positively charged amino acids in the pores presumably help promote the diffusion of the negatively charged substrates and products. Other minor structural components of the shell that have been characterized include pentameric proteins ( BMC-P proteins) which occupy the vertices of the icosahedral shell. A third building block of the carboxysome shell is a protein composed of two BMC domains in tandem ( BMC-T proteins). Structurally, these are known to form trimers which are pseudohexameric. Some members of the BMC-T protein family stack in a face-to-face fashion and form tiny cages, notably both types of carboxysomes (alpha and beta, see below) contain these stacking trimers. Based on crystal structures, these protein cages have relatively large gated pores on both sides, and it has been proposed that the opening and closing of the pore could be controlled in a manner similar to an air-lock. Such an air-lock, in contrast to BMC-H proteins with constitutively open pores, has been suggested to serve as a route for larger substrates (ribulose-1,5-bisphosphate) and products (3-phosphoglycerate) that must cross the shell.

Production of empty carboxysome shells in E. coli enabled the first visualization of the carboxysome shell by cryo-electron microscopy.

A number of viral capsids are also icosahedral, composed of hexameric and pentameric proteins, but currently there is no evidence suggesting any evolutionary relationship between the carboxysome shell and viral capsids.

Scaffold proteins

All carboxysomes contain scaffold proteins that nucleate carboxysome components together during the assembly process. These scaffold proteins are required for carboxysome assembly; without them, carboxysomes do not form. The α-carboxysomal scaffold protein is called CsoS2, and the β-carboxysomal scaffold protein is called CcmM. Though CsoS2 and CcmM have related functions, they have no evolutionary or sequence similarity. Both proteins bind to Rubisco, thereby ensuring that Rubisco gets packaged during carboxysome biogenesis. Remarkably, both proteins bind to Rubisco at a binding site that bridges two large subunits while maintaining contact with the small subunit, ensuring that only the 16-subunit Rubisco holoenzyme is encapsulated. Both CsoS2 and CcmM have repetitive domain structures giving them multi-valent modes of binding. CcmM has three small-subutnit-like (SSUL) domains that bind to Rubisco, and CsoS2 has four N-terminal domain (NTD) repeats that bind Rubisco, making it possible for each single scaffold protein to bind up to 3-4 Rubiscos at a time. CsoS2 has also been shown to bind to shell proteins via its 7 Middle Region (MR) repeats and C-terminal domain (CTD). In α-carboxysomes, the CsoS2 MR repeats have been shown to define the size of the carboxysome.

Two types of carboxysomes

There are two types of carboxysomes. Although they may seem similar in appearance, they differ in their protein composition, including the form of RuBisCO they enclose. Furthermore, studies have revealed fundamental differences in their gene organization and possibly their assembly pathway. Based on bioinformatic studies of shell proteins, it appears that the two types of carboxysomes evolved independently.

Alpha-carboxysomes

Alpha-carboxysomes (aka α-carboxysomes) are also referred as the ''cso'' type of carboxysome. They contain Form IA RuBisCO; they are found in alpha-cyanobacteria and members of Pseudomonadota (some nitrifying bacteria, some sulfur-oxidizing bacteria such as ''Halothiobacillus neapolitanus'', and some purple bacteria). The alpha-carboxysome was the first bacterial microcompartment to be purified and characterized.

Electron microscopy studies on purified alpha-carboxysomes or cell sections containing alpha-carboxysomes revealed that they are typically 100-160 nm in diameter. Common building blocks for the shell of alpha-carboxysomes are called CsoS1A/B/C (BMC-H), CsoS4A/B (BMC-P), and CsoS1D (BMC-T). CsoS4A/B were the first BMC-P proteins to be experimentally demonstrated as minor components of the BMC shell (only 12 pentamers are required to cap the vertices of an icosahedron). CsoS1D is the first BMC-T which has been structurally characterized; it is also the first example of dimerization of two BMC building blocks in a face-to-face fashion to create a tiny cage. The CsoS1D cage has a gated pore at both ends, which is proposed to facilitate the transfer of large metabolites across the shell. In addition to the specific form of RuBisCO, other encapsulated proteins distinguish alpha-carboxysomes from beta-carboxysomes such as scaffold protein CsoS2 and carbonic anhydrase CsoSCA. CsoS2 is an intrinsically disordered protein with an essential role in alpha-carboxysome assembly. It has a very high pI and a unique primary structure with three domains: an N-terminal, a middle- and a C-terminal domain. Repetitive motifs can be identified in all three regions; the N-terminal domain repeats bind to Rubisco, the middle region domains bind to shell proteins, and the c-terminal domain repeats also bind to shell proteins. CsoSCA is a beta-carbonic anhydrase that binds to Rubisco and has been found to be allosterically regulated by the Rubisco substrate, ribulose,1-5,bisphosphate (RuBP) in alpha-cyanobacteria. Studies in ''Halothiobacillus neapolitanus'' have shown that empty shells of normal shape and composition are assembled in carboxysomal RuBisCO-lacking mutants, suggesting that alpha-carboxysome shell biogenesis and enzyme sequestration are two independent, but functionally linked processes. Intriguingly, carboxysomes of ''Halothiobacillus neapolitanus'' have been found to accommodate chimeric and heterologous species of RuBisCO. It is the large subunit of RuBisCO which determines whether the enzyme is sequestered into carboxysomes.

Beta-carboxysomes

Beta-carboxysomes (aka β-carboxysomes) are found in cyanobacteria, specifically the "beta-cyanobacteria".

The signature proteins of the beta-carboxysome are Form IB RuBisCO and a gamma carbonic anhydrase homolog. Beta-carboxysomes are typically larger than alpha-carboxysomes: the observed diameters vary from 200 to 400 nm. The structural proteins that are essential for beta-carboxysome formation are encoded in the conserved carboxysome locus known as the ''ccm'' locus. The ''ccm'' locus includes genes for core proteins CcmM and CcmN and the shell proteins CcmK (a BMC-H protein), CcmL (a BMC-P protein) and CcmO (a BMC-T protein).

A full length CcmM protein consists of a gamma-carbonic anhydrase domain and three to five RubisCO small subunit-like domains (SSLDs) on its C-terminus. The ccmM gene contains an internal translation site that produces a short form of CcmM which only consists of SSLDs; both long and short forms of CcmM are required for beta-carboxysome assembly. CcmN contains multiple hexapeptide-repeat domains on its N-terminus and a short α-helical encapsulation peptide on the C-terminus.

Other structural components of beta-carboxysomes are encoded outside of the ''ccm'' locus. CcmP is a BMC-T protein that is absolutely conserved among organisms that form beta-carboxysomes. Two CcmP pseudohexamers stack to form a nanocompartment—an example of an air-lock forming protein. Likewise, in some cyanobacterial strains the beta-carboxysomes contain a beta-carbonic anhydrase that is not encoded in the ''ccm'' locus.

Shell proteins of beta carboxysomes are relatively diverse compared to their counterparts in the alpha carboxysomes, and this has been proposed to reflect variable permeability requirements of beta carboxysomes, which are found in cyanobacteria that occupy ecophysiologically dynamic environments.

The beta-carboxysome assembles from the inside out. First an enzymatic core forms that is subsequently encapsulated by the protein shell. Carboxysome assembly occurs through a series of protein-protein interactions: the enzyme RuBisCO and the two isoforms (full length and short form) of the CcmM protein interact by means of the SSLDs; in strains containing CcaA the beta-carbonic anhydrase is brought into the carboxysome core by interaction with the N-terminus of the full length CcmM. Once the procarboxysome (the carboxysome core) is formed, the N-terminus of the adapter protein CcmN interacts with the N-terminus of CcmM, while the C-terminus of CcmN recruits the shell proteins CcmK (BMC-H) and CcmO (BMC-T), utilizing a 15-20 amino acids long peptide. This encapsulation peptide forms an amphipathic a-helix that interacts with the shell components and its role is essential, given that in its absence, carboxysomes cannot be formed. The final step is the addition of the vertices formed by the BMC-P protein CcmL, which then cap the enzymatic core and facets. Elucidation of the assembly pathway of beta carboxysomes enabled the design of a single synthetic protein that replaced four other proteins in carboxysome assembly.

Potential uses of the carboxysome in biotechnology

As is the case with other BMCs, the carboxysome is attracting significant attention by researchers for applications in plant synthetic biology. The transfer of a genetic module coding for an alpha-carboxysome has been shown to produce carboxysome-like structures in ''E. coli''. Bioengineering of carboxysome shells has been shown to be feasible, and beta-carboxysomes constructed with chimeric proteins or with chimeric shells have been reported. The introduction of carboxysomes into plant chloroplasts as part of a concentrating mechanism such as that found in cyanobacteria is predicted to significantly improve net fixation and yield. Expression of beta-carboxysomal shell proteins and Form IB Rubisco-CcmM complexes in tobacco chloroplasts has been achieved, but did not result in compartments containing RuBisCO. A further advance has been the construction of minimal alpha-carboxysomes containing Form IA Rubisco and the CsoS1A and CsoS2 proteins from the cyanobacterium Cyanobium PCC7001 in tobacco chloroplasts. As yet, identifiably functional carboxysomes have not been constructed in plant chloroplasts. Improvement of photosynthesis in plants using this approach is ultimately dependent on the operation of transporter proteins in the chloroplast inner envelope membrane to help generate a high concentration of bicarbonate inside the chloroplast.

Potential applications of carboxysomes (list format):

# Engineer the carbon dioxide-concentrating mechanism (CCM) and carboxysomes into industrially relevant microbes, potentially converting heterotrophic organisms into mixotrophs or autotrophs that capture CO₂ while producing high value products.
# Engineer the carbon dioxide-concentrating mechanism (CCM) and carboxysomes into plants for increased CO₂ capture and enhanced growth.
# Engineer faster Rubiscos. The fastest form I prokaryotic Rubiscos are mostly found in α-carboxysomes.
# Engineer a minimal carboxysome gene set (Rubisco, carbonic anhydrase, scaffold protein, hexameric shell, pentameric shell) to facilitate facile engineering into alternative host organisms.
# Design ''in vitro'' carboxysomes for cell-free CO₂ fixation.
# Engineer carboxysomes to have alternative metabolisms.

Carboxysome reviews (by year)

Carboxysome research expands every year. Published reviews chart the rapid pace of discovery across the broad field of "carboxysomics".

See also

* Bacterial microcompartment
* BMC domain
* RuBisCO
* Pyrenoid

References

{{Reflist,
refs=

{{cite journal , vauthors = Yeates TO, Kerfeld CA, Heinhorst S, Cannon GC, Shively JM , title = Protein-based organelles in bacteria: carboxysomes and related microcompartments , journal = Nature Reviews. Microbiology , volume = 6 , issue = 9 , pages = 681–691 , date = September 2008 , pmid = 18679172 , doi = 10.1038/nrmicro1913 , s2cid = 22666203

{{cite journal , vauthors = Badger MR, Price GD , title = CO2 concentrating mechanisms in cyanobacteria: molecular components, their diversity and evolution , journal = Journal of Experimental Botany , volume = 54 , issue = 383 , pages = 609–622 , date = February 2003 , pmid = 12554704 , doi = 10.1093/jxb/erg076 , doi-access = free

{{cite journal , vauthors = Cai F, Menon BB, Cannon GC, Curry KJ, Shively JM, Heinhorst S , title = The pentameric vertex proteins are necessary for the icosahedral carboxysome shell to function as a CO2 leakage barrier , journal = PLOS ONE , volume = 4 , issue = 10 , pages = e7521 , date = October 2009 , pmid = 19844578 , pmc = 2760150 , doi = 10.1371/journal.pone.0007521 , doi-access = free , bibcode = 2009PLoSO...4.7521C

{{cite journal , vauthors = Dou Z, Heinhorst S, Williams EB, Murin CD, Shively JM, Cannon GC , title = CO2 fixation kinetics of Halothiobacillus neapolitanus mutant carboxysomes lacking carbonic anhydrase suggest the shell acts as a diffusional barrier for CO2 , journal = The Journal of Biological Chemistry , volume = 283 , issue = 16 , pages = 10377–10384 , date = April 2008 , pmid = 18258595 , doi = 10.1074/jbc.M709285200 , doi-access = free

{{cite journal , vauthors = Kerfeld CA, Erbilgin O , title = Bacterial microcompartments and the modular construction of microbial metabolism , journal = Trends in Microbiology , volume = 23 , issue = 1 , pages = 22–34 , date = January 2015 , pmid = 25455419 , doi = 10.1016/j.tim.2014.10.003 , doi-access = free

{{cite journal , vauthors = Axen SD, Erbilgin O, Kerfeld CA , title = A taxonomy of bacterial microcompartment loci constructed by a novel scoring method , journal = PLOS Computational Biology , volume = 10 , issue = 10 , pages = e1003898 , date = October 2014 , pmid = 25340524 , pmc = 4207490 , doi = 10.1371/journal.pcbi.1003898 , bibcode = 2014PLSCB..10E3898A , doi-access = free

{{cite journal , vauthors = Drews G, Niklowitz W , title = ytology of Cyanophycea. II. Centroplasm and granular inclusions of Phormidium uncinatum, journal = Archiv für Mikrobiologie , volume = 24 , issue = 2 , pages = 147–162 , year = 1956 , pmid = 13327992 , doi = 10.1007/BF00408629 , s2cid = 46171409

{{cite journal , vauthors = Gantt E, Conti SF , title = Ultrastructure of blue-green algae , journal = Journal of Bacteriology , volume = 97 , issue = 3 , pages = 1486–1493 , date = March 1969 , pmid = 5776533 , pmc = 249872 , doi = 10.1128/JB.97.3.1486-1493.1969

{{cite journal , vauthors = Shively JM , title = Inclusion bodies of prokaryotes , journal = Annual Review of Microbiology , date = 1974 , volume = 28 , pages = 167–187 , pmid = 4372937 , doi = 10.1146/annurev.mi.28.100174.001123

{{cite journal , vauthors = Shively JM, Ball F, Brown DH, Saunders RE , title = Functional organelles in prokaryotes: polyhedral inclusions (carboxysomes) of Thiobacillus neapolitanus , journal = Science , volume = 182 , issue = 4112 , pages = 584–586 , date = November 1973 , pmid = 4355679 , doi = 10.1126/science.182.4112.584 , s2cid = 10097616 , bibcode = 1973Sci...182..584S

{{cite journal , vauthors = Iancu CV, Ding HJ, Morris DM, Dias DP, Gonzales AD, Martino A, Jensen GJ , title = The structure of isolated Synechococcus strain WH8102 carboxysomes as revealed by electron cryotomography , journal = Journal of Molecular Biology , volume = 372 , issue = 3 , pages = 764–773 , date = September 2007 , pmid = 17669419 , pmc = 2453779 , doi = 10.1016/j.jmb.2007.06.059

{{cite journal , vauthors = Iancu CV, Morris DM, Dou Z, Heinhorst S, Cannon GC, Jensen GJ , title = Organization, structure, and assembly of alpha-carboxysomes determined by electron cryotomography of intact cells , journal = Journal of Molecular Biology , volume = 396 , issue = 1 , pages = 105–117 , date = February 2010 , pmid = 19925807 , pmc = 2853366 , doi = 10.1016/j.jmb.2009.11.019

{{cite journal , vauthors = Schmid MF, Paredes AM, Khant HA, Soyer F, Aldrich HC, Chiu W, Shively JM , title = Structure of Halothiobacillus neapolitanus carboxysomes by cryo-electron tomography , journal = Journal of Molecular Biology , volume = 364 , issue = 3 , pages = 526–535 , date = December 2006 , pmid = 17028023 , pmc = 1839851 , doi = 10.1016/j.jmb.2006.09.024 , hdl = 11147/2128

{{cite journal , vauthors = Vernizzi G, Sknepnek R, Olvera de la Cruz M , title = Platonic and Archimedean geometries in multicomponent elastic membranes , journal = Proceedings of the National Academy of Sciences of the United States of America , volume = 108 , issue = 11 , pages = 4292–4296 , date = March 2011 , pmid = 21368184 , pmc = 3060260 , doi = 10.1073/pnas.1012872108 , doi-access = free

{{cite journal , vauthors = Kerfeld CA, Sawaya MR, Tanaka S, Nguyen CV, Phillips M, Beeby M, Yeates TO , title = Protein structures forming the shell of primitive bacterial organelles , journal = Science , volume = 309 , issue = 5736 , pages = 936–938 , date = August 2005 , pmid = 16081736 , doi = 10.1126/science.1113397 , s2cid = 24561197 , citeseerx = 10.1.1.1026.896 , bibcode = 2005Sci...309..936K

{{cite journal , vauthors = Tanaka S, Kerfeld CA, Sawaya MR, Cai F, Heinhorst S, Cannon GC, Yeates TO , title = Atomic-level models of the bacterial carboxysome shell , journal = Science , volume = 319 , issue = 5866 , pages = 1083–1086 , date = February 2008 , pmid = 18292340 , doi = 10.1126/science.1151458 , s2cid = 5734731 , bibcode = 2008Sci...319.1083T

{{cite journal , vauthors = Cai F, Sutter M, Cameron JC, Stanley DN, Kinney JN, Kerfeld CA , title = The structure of CcmP, a tandem bacterial microcompartment domain protein from the β-carboxysome, forms a subcompartment within a microcompartment , journal = The Journal of Biological Chemistry , volume = 288 , issue = 22 , pages = 16055–16063 , date = May 2013 , pmid = 23572529 , pmc = 3668761 , doi = 10.1074/jbc.M113.456897 , doi-access = free

{{cite journal , vauthors = Klein MG, Zwart P, Bagby SC, Cai F, Chisholm SW, Heinhorst S, Cannon GC, Kerfeld CA , display-authors = 6 , title = Identification and structural analysis of a novel carboxysome shell protein with implications for metabolite transport , journal = Journal of Molecular Biology , volume = 392 , issue = 2 , pages = 319–333 , date = September 2009 , pmid = 19328811 , doi = 10.1016/j.jmb.2009.03.056 , hdl-access = free , s2cid = 42771660 , hdl = 1721.1/61355

{{cite journal , vauthors = Zarzycki J, Axen SD, Kinney JN, Kerfeld CA , title = Cyanobacterial-based approaches to improving photosynthesis in plants , journal = Journal of Experimental Botany , volume = 64 , issue = 3 , pages = 787–798 , date = January 2013 , pmid = 23095996 , doi = 10.1093/jxb/ers294 , doi-access = free

{{cite journal , vauthors = Rae BD, Long BM, Badger MR, Price GD , title = Functions, compositions, and evolution of the two types of carboxysomes: polyhedral microcompartments that facilitate CO2 fixation in cyanobacteria and some proteobacteria , journal = Microbiology and Molecular Biology Reviews , volume = 77 , issue = 3 , pages = 357–379 , date = September 2013 , pmid = 24006469 , pmc = 3811607 , doi = 10.1128/MMBR.00061-12

{{cite journal , vauthors = Shively JM, Bock E, Westphal K, Cannon GC , title = Icosahedral inclusions (carboxysomes) of Nitrobacter agilis , journal = Journal of Bacteriology , volume = 132 , issue = 2 , pages = 673–675 , date = November 1977 , pmid = 199579 , pmc = 221910 , doi = 10.1128/JB.132.2.673-675.1977

{{cite journal, vauthors = Cannon GC, Shively JM , title=Characterization of a homogenous preparation of carboxysomes from Thiobacillus neapolitanus, journal=Archives of Microbiology, volume=134, issue=1, year=1983, pages=52–59, issn=0302-8933, doi=10.1007/BF00429407, bibcode=1983ArMic.134...52C , s2cid=22329896

{{Cite book, vauthors = Heinhorst S, Cannon GC, Shively JM , chapter=Carboxysomes and Their Structural Organization in Prokaryotes, year=2014, pages=75–101, doi=10.1007/978-1-4939-1667-2_4, title =Nanomicrobiology, isbn=978-1-4939-1666-5

{{cite journal , vauthors = Cai F, Dou Z, Bernstein SL, Leverenz R, Williams EB, Heinhorst S, Shively J, Cannon GC, Kerfeld CA , display-authors = 6 , title = Advances in Understanding Carboxysome Assembly in Prochlorococcus and Synechococcus Implicate CsoS2 as a Critical Component , journal = Life , volume = 5 , issue = 2 , pages = 1141–1171 , date = March 2015 , pmid = 25826651 , pmc = 4499774 , doi = 10.3390/life5021141 , bibcode = 2015Life....5.1141C , doi-access = free

{{cite journal , vauthors = Sawaya MR, Cannon GC, Heinhorst S, Tanaka S, Williams EB, Yeates TO, Kerfeld CA , title = The structure of beta-carbonic anhydrase from the carboxysomal shell reveals a distinct subclass with one active site for the price of two , journal = The Journal of Biological Chemistry , volume = 281 , issue = 11 , pages = 7546–7555 , date = March 2006 , pmid = 16407248 , doi = 10.1074/jbc.M510464200 , doi-access = free

{{cite journal , vauthors = Menon BB, Dou Z, Heinhorst S, Shively JM, Cannon GC , title = Halothiobacillus neapolitanus carboxysomes sequester heterologous and chimeric RubisCO species , journal = PLOS ONE , volume = 3 , issue = 10 , pages = e3570 , year = 2008 , pmid = 18974784 , pmc = 2570492 , doi = 10.1371/journal.pone.0003570 , doi-access = free , bibcode = 2008PLoSO...3.3570M

{{cite journal , vauthors = Long BM, Badger MR, Whitney SM, Price GD , title = Analysis of carboxysomes from Synechococcus PCC7942 reveals multiple Rubisco complexes with carboxysomal proteins CcmM and CcaA , journal = The Journal of Biological Chemistry , volume = 282 , issue = 40 , pages = 29323–29335 , date = October 2007 , pmid = 17675289 , doi = 10.1074/jbc.M703896200 , doi-access = free

{{cite journal , vauthors = Long BM, Tucker L, Badger MR, Price GD , title = Functional cyanobacterial beta-carboxysomes have an absolute requirement for both long and short forms of the CcmM protein , journal = Plant Physiology , volume = 153 , issue = 1 , pages = 285–293 , date = May 2010 , pmid = 20304968 , pmc = 2862411 , doi = 10.1104/pp.110.154948

{{cite journal , vauthors = Kinney JN, Salmeen A, Cai F, Kerfeld CA , title = Elucidating essential role of conserved carboxysomal protein CcmN reveals common feature of bacterial microcompartment assembly , journal = The Journal of Biological Chemistry , volume = 287 , issue = 21 , pages = 17729–17736 , date = May 2012 , pmid = 22461622 , pmc = 3366800 , doi = 10.1074/jbc.M112.355305 , doi-access = free

{{cite journal , vauthors = Cannon GC, Heinhorst S, Kerfeld CA , title = Carboxysomal carbonic anhydrases: Structure and role in microbial CO2 fixation , journal = Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics , volume = 1804 , issue = 2 , pages = 382–392 , date = February 2010 , pmid = 19818881 , doi = 10.1016/j.bbapap.2009.09.026 , s2cid = 3712407 , url = https://digital.library.unt.edu/ark:/67531/metadc840980/

{{cite journal , vauthors = Cameron JC, Wilson SC, Bernstein SL, Kerfeld CA , title = Biogenesis of a bacterial organelle: the carboxysome assembly pathway , journal = Cell , volume = 155 , issue = 5 , pages = 1131–1140 , date = November 2013 , pmid = 24267892 , doi = 10.1016/j.cell.2013.10.044 , doi-access = free

{{cite journal , vauthors = Cot SS, So AK, Espie GS , title = A multiprotein bicarbonate dehydration complex essential to carboxysome function in cyanobacteria , journal = Journal of Bacteriology , volume = 190 , issue = 3 , pages = 936–945 , date = February 2008 , pmid = 17993516 , pmc = 2223583 , doi = 10.1128/JB.01283-07

{{cite journal , vauthors = Long BM, Rae BD, Badger MR, Price GD , title = Over-expression of the β-carboxysomal CcmM protein in Synechococcus PCC7942 reveals a tight co-regulation of carboxysomal carbonic anhydrase (CcaA) and M58 content , journal = Photosynthesis Research , volume = 109 , issue = 1–3 , pages = 33–45 , date = September 2011 , pmid = 21597987 , doi = 10.1007/s11120-011-9659-8 , bibcode = 2011PhoRe.109...33L , s2cid = 20716799

{{cite journal , vauthors = Bonacci W, Teng PK, Afonso B, Niederholtmeyer H, Grob P, Silver PA, Savage DF , title = Modularity of a carbon-fixing protein organelle , journal = Proceedings of the National Academy of Sciences of the United States of America , volume = 109 , issue = 2 , pages = 478–483 , date = January 2012 , pmid = 22184212 , pmc = 3258634 , doi = 10.1073/pnas.1108557109 , doi-access = free

{{cite journal , vauthors = Cai F, Sutter M, Bernstein SL, Kinney JN, Kerfeld CA , title = Engineering bacterial microcompartment shells: chimeric shell proteins and chimeric carboxysome shells , journal = ACS Synthetic Biology , volume = 4 , issue = 4 , pages = 444–453 , date = April 2015 , pmid = 25117559 , doi = 10.1021/sb500226j

{{cite journal , vauthors = Price GD, Badger MR, Woodger FJ, Long BM , title = Advances in understanding the cyanobacterial CO2-concentrating-mechanism (CCM): functional components, Ci transporters, diversity, genetic regulation and prospects for engineering into plants , journal = Journal of Experimental Botany , volume = 59 , issue = 7 , pages = 1441–1461 , date = 2008 , pmid = 17578868 , doi = 10.1093/jxb/erm112 , doi-access = free

{{cite journal , vauthors = Price GD, Pengelly JJ, Forster B, Du J, Whitney SM, von Caemmerer S, Badger MR, Howitt SM, Evans JR , display-authors = 6 , title = The cyanobacterial CCM as a source of genes for improving photosynthetic CO2 fixation in crop species , journal = Journal of Experimental Botany , volume = 64 , issue = 3 , pages = 753–768 , date = January 2013 , pmid = 23028015 , doi = 10.1093/jxb/ers257 , doi-access = free , hdl = 1885/53387 , hdl-access = free

{{cite journal , vauthors = McGrath JM, Long SP , title = Can the cyanobacterial carbon-concentrating mechanism increase photosynthesis in crop species? A theoretical analysis , journal = Plant Physiology , volume = 164 , issue = 4 , pages = 2247–2261 , date = April 2014 , pmid = 24550242 , pmc = 3982776 , doi = 10.1104/pp.113.232611

{{cite journal , vauthors = Yin X, Struik PC , title = Can increased leaf photosynthesis be converted into higher crop mass production? A simulation study for rice using the crop model GECROS , journal = Journal of Experimental Botany , volume = 68 , issue = 9 , pages = 2345–2360 , date = April 2017 , pmid = 28379522 , pmc = 5447886 , doi = 10.1093/jxb/erx085

{{cite journal , vauthors = Lin MT, Occhialini A, Andralojc PJ, Devonshire J, Hines KM, Parry MA, Hanson MR , title = β-Carboxysomal proteins assemble into highly organized structures in Nicotiana chloroplasts , journal = The Plant Journal , volume = 79 , issue = 1 , pages = 1–12 , date = July 2014 , pmid = 24810513 , pmc = 4080790 , doi = 10.1111/tpj.12536

{{cite journal , vauthors = Lin MT, Occhialini A, Andralojc PJ, Parry MA, Hanson MR , title = A faster Rubisco with potential to increase photosynthesis in crops , journal = Nature , volume = 513 , issue = 7519 , pages = 547–550 , date = September 2014 , pmid = 25231869 , pmc = 4176977 , doi = 10.1038/nature13776 , bibcode = 2014Natur.513..547L

{{cite journal , vauthors = Long BM, Hee WY, Sharwood RE, Rae BD, Kaines S, Lim YL, Nguyen ND, Massey B, Bala S, von Caemmerer S, Badger MR, Price GD , display-authors = 6 , title = Carboxysome encapsulation of the CO₂-fixing enzyme Rubisco in tobacco chloroplasts , journal = Nature Communications , volume = 9 , issue = 1 , pages = 3570 , date = September 2018 , pmid = 30177711 , pmc = 6120970 , doi = 10.1038/s41467-018-06044-0 , bibcode = 2018NatCo...9.3570L

{{cite journal , vauthors = Rae BD, Long BM, Förster B, Nguyen ND, Velanis CN, Atkinson N, Hee WY, Mukherjee B, Price GD, McCormick AJ , display-authors = 6 , title = Progress and challenges of engineering a biophysical CO2-concentrating mechanism into higher plants , journal = Journal of Experimental Botany , volume = 68 , issue = 14 , pages = 3717–3737 , date = June 2017 , pmid = 28444330 , doi = 10.1093/jxb/erx133 , doi-access = free , hdl = 20.500.11820/42c5bfb2-691e-4a61-91b1-8efffbe31383 , hdl-access = free .

External links

Mysterious Bacterial Microcompartments Revealed By Biochemists



Cell anatomy
Organelles
Protein complexes