This document provides an overview of carboxysomes, including their history, structure, function, and potential applications. Carboxysomes were first observed in cyanobacteria in the 1950s but were not fully characterized until the 1970s. They have an icosahedral protein shell that encapsulates RuBisCO and carbonic anhydrase. Carboxysomes play a key role in the carbon concentrating mechanism of cyanobacteria by compartmentalizing carbon fixation to increase CO2 levels near RuBisCO. Some researchers have proposed introducing carboxysomes into chloroplasts via genetic engineering to potentially increase photosynthetic efficiency in crops.

1. Running head: A REVIEW ON THE CARBOXYSOME: ITS HISTORY, STRUCTURE, FUNCTION AND APPLICATION 1
A Review on the Carboxysome: its History, Structure, Function, and Application
Desmond Yao
Shenzhen Foreign Languages School

2. A REVIEW ON THE CARBOXYSOME: ITS HISTORY, STRUCTURE, FUNCTION AND APPLICATION 2
Table of Contents
Abstract......................................................................................................................................3
History........................................................................................................................................4
Structure.....................................................................................................................................5
Function......................................................................................................................................8
Application...............................................................................................................................11
Other Bacterial Microcompartments........................................................................................16
Further Directions of Study......................................................................................................17
References................................................................................................................................18
Used Abbreviations..................................................................................................................21

3. A REVIEW ON THE CARBOXYSOME: ITS HISTORY, STRUCTURE, FUNCTION AND APPLICATION 3
Abstract
Carboxysomes play a crucial role in carbon fixation in cyanobacteria.
Carboxysomes typically range from 80 nanometers to 120 nanometers in diameter, and have
icosahedral protein shells that encapsulate two carbon-fixing enzymes, carbonic anhydrase
and RuBisCO. They also belong to a group of bacterial organelles prevalent in bacteria
known as bacterial microcompartments. This paper serves to offer general information on
carboxysomes: their history, their structure, their function, and their application. In addition,
this paper examines other bacterial microcompartments and provides suggestions for further
research, in an attempt to shed additional light on carboxysomes.
Keywords: carboxysome, structure, function, application, bacterial microcompartments,
further directions of study
History

4. A REVIEW ON THE CARBOXYSOME: ITS HISTORY, STRUCTURE, FUNCTION AND APPLICATION 4
In 1956, researchers first observed an intracellular structure in the cyanobacteria
Phormidium uncinatum [1, 2]. However, because of its resemblance to phage particles,
investigators were at first skeptical as to whether the inclusion was a genuine functional unit
within bacterial cells [4]. In the following years, more of the same or similar structures were
widely observed in other cyanobacteria, including Nostoc punctiforme, Synechococcus
elongates, Anabaena cylindrica and Symploca muscorum [5].
In 1973, Jessup Shively at Clemson University and his collaborators purified these
inclusions from a chemoautotrophic bacterium-Thiobacillus neapolitanus-and demonstrated
that they were packed with enzymes, not with phage DNA [2, 3, 5]. The Clemson researchers
named the intracellular inclusion carboxysomes. These newly-named bodies were mainly
around 120nm in size. Later analysis through microscopy, gel electrophoresis and other
methods showed that the carboxysome is filled with type 1 RuBisCO, the most abundant
protein in the world.
In the following years, two possible hypotheses regarding carboxysomal function were
proposed: carboxysomes are either storage units, or organelles involved in the carbon fixation
process [5]. Experiments later showed that deficient carbon fixation is strongly correlated
with defective carboxysome structure. Thus, these experiments substantiated the proposal of
carboxysomal involvement in the carbon fixation process [5].
In 1991, characterization of RuBisCO activity within the carboxysome was achieved.
Since that time, researchers have identified 16 proteins as possible constituents of
carboxysomes. Identification of these proteins as chemical sub-units os the organelle lays the

5. A REVIEW ON THE CARBOXYSOME: ITS HISTORY, STRUCTURE, FUNCTION AND APPLICATION 5
foundation for further discussion of its structure and function [5].
Structure
Carboxysomes are icosahedral, or quasi-icosahedral structures, typically 80-120 nm in
diameter [3, 5, 11, 12]. The carboxysome consists of two major parts: a protein shell ~4nm
thick and the inclusion separated from the cytosol by the protein shell.
The outer shell consists of 3000-5000 protein subunits and encapsulates two carbon
fixing enzymes: carbonic anhydrase and RuBisCO [3, 4, 5]. Because of its icosahedral
structure, the outer shell has 20 triangular faces, 30 edges and 12 vertices. The triangular
faces consist of many hexagonal building blocks formed by the CsoS1 or CcmK proteins [3,
4, 5, 6]. The vertices are formed by pentagonal proteins such as CsoS4 or CcmL [5]. Small
pores are present both at the center of the hexagonal subunits and at the crevices between the
subunits and the facets [3, 5]. The pores within each hexametric subunit have diameters
ranging from 4Å to 7Å, depending on the type of protein components [6]. Moreover, the
polarity of the carboxysomal shell may suggest that a selectivity, achieved through the
charged pores, in the diffusion of negatively charged molecules helps to account for its highly
effective carbon concentration, and helps to repel neutrally-charged O2, since the
carboxysomal inclusion is more oxidative than bacterial cytosol [7].

6. A REVIEW ON THE CARBOXYSOME: ITS HISTORY, STRUCTURE, FUNCTION AND APPLICATION 6
Figure 1 . A cyto-electron tomogram of isolated H. neapolitanus carboxysomes filled with RuBisCO [30]
The shorter bar points to the outer shell of carboxysome while the longer bar points to its inclusion.
Source: Adapted from ref. [11]

7. A REVIEW ON THE CARBOXYSOME: ITS HISTORY, STRUCTURE, FUNCTION AND APPLICATION 7
The inclusion consists of RuBisCO and carbonic anhydrase, two enzymes involved in the
carbon fixation process. The inclusion, if filled up completely, could accommodate ~250
molecules of RuBisCO, according to estimation [11]. Studies have shown through ECT and
X-ray crystallography that carboxysomal RuBisCO molecules are arranged in three or four
concentric layers which are ~11 nm apart [11, 12].
In regards to its assembly, the carboxysome also displays certain distinctive patterns.
Carboxysomes, unlike membrane-bound organelles of eukaryotes, form the inclusions first at
a distinct site within the cell [31]. Subsequently, shell proteins encapsulate these
preassembled carboxysomes, which are simultaneously relocated within the cell [31]. In
addition, the proteinaceous subunits have also displayed a pattern of self-assembly [6].
Although now we seem to understand carboxysomal structure, there are still
Figure 2 . A diagram of the icosahedral protein shell of carboxysome, with various hexagons and 12
pentagons at vertices [3].
Source: Reproduced from ref. [3]

8. A REVIEW ON THE CARBOXYSOME: ITS HISTORY, STRUCTURE, FUNCTION AND APPLICATION 8
controversies. A few recent studies have posed questions about whether pores exist on the
protein shells, since, according to Iancu et al., what has appeared as pores may actually be
artificial noises occurring due to defects in experimental set-ups [5, 11, 12]. It is even
proposed that the inclusion completely consists of RuBisCO, since CcmM, CsoSCA, and
CcaA proteins located on the protein shell may perform carbonic anhydrase activities [11].
There’s no systematic conclusion up to this point, but further progress in ECT may produce
better results.
Function
Carboxysomes are involved in a carbon fixation process called CCM (carbon
concentrating mechanism). CCM is a mechanism found in nearly all algae and many high
land plants. CCM serves to overcome the limitations to land plant growth imposed by low
Figure 3 . Identification of RuBisCO via template-matching inside a carboxysome
Densities identified as RuBisCO by template matching followed by a customized peak search are circled in red
on 6.7 nm slices through the (a) undenoised and (b) denoised carboxysome. (c) 3-D representation of the same
carboxysome in which the densities have been replaced by the RuBisCO template [11]
Source: Reproduced from ref. [11]

9. A REVIEW ON THE CARBOXYSOME: ITS HISTORY, STRUCTURE, FUNCTION AND APPLICATION 9
atmospheric CO2 concentration and high O2 concentration. CCM has three steps in total, and
carboxysomal activity is its last step [14].
The first step is for the cell to uptake bicarbonate (HCO3
-
) or CO2 that is later transformed
to bicarbonate in the cytoplasm, via a group of light-dependent pumps, to reach a
concentration 1000 times that of the outside environment [8]. Then, in the second step, as the
RuBisCO requires CO2 as its substrate, the carboxysomal carbonic anhydrases CsoSCA,
CcaA and CcmM, convert bicarbonate to CO2 in the vicinity of RuBisCO, inside the
carboxysome [5]. In the third step, RuBisCO catalyzes the combination of ribulose-1, 5-
bisphosphate (RuBP) and CO2 to produce 3-phosphoglycerate (3-PGA), an intermittent sugar.
The 3-PGA produced ultimately leaves the carboxysome and enters the Calvin-Benson-
Bassham cycle to produce G3P, which can be later used in metabolism and other cellular
Figure 4 . Cyanobacterial carbon concentrating mechanism (CCM)
a: The bacterial CCM starts with uptake of inorganic carbon into the cell as bicarbonate and CO2. Bicarbonate
that enters through pores on the protein shell then is converted to CO2 by carboxysomal carbonic anhydrase(CA)
within the microcompartment lumen. Consequently, CO2 can accumulate in the immediate vicinity of RuBisCO
while diffusive loss of CO2 through the cell membrane is minimized. Elevated CO2 proximal to RuBisCO
increases carbon fixation and suppresses photorespiration [26].
b: A preliminary atomic model of the carboxysome shell based on crystal structures of the component shell
proteins [3]. The positively charged pores through the sheet of hexagonal proteins are indicated. These have
been postulated to enhance the diffusion of negatively charged molecules such as bicarbonate (thick arrow)
across the shell, compared to uncharged molecules such as CO2 and O2 (thin arrows) [26].
Source: Reproduced from ref. [26]

10. A REVIEW ON THE CARBOXYSOME: ITS HISTORY, STRUCTURE, FUNCTION AND APPLICATION 10
activities [9].
CCM is in general relatively sensitive to the outer environment [15]. Moreover,
considering the unusually active correlation between the two carboxysomal encoding genes
and the outer environment, researchers have suggested that carboxysomes are more sensitive
than others parts involved in CCM to the change in pCO2 and temperature levels [15]. Thus,
it is possible that within CCM, the carboxysome is most directly related to the outside
environment in responses to other outer factors [15].
The advantage offered by CCM lies in the unusually high efficiency of carbon fixation,
and this high efficiency is largely due to the carboxysome. RuBisCO is a bi-functional
enzyme; thus, it reacts with two kinds of substrate, O2 and CO2, in a competitive manner.
Moreover, RuBisCO is noted as a notoriously inefficient enzyme, because its primary
substrate is O2,and its secondary substrate is CO2 [11]. Since O2 is evidently more abundant
than CO2 in natural environments, cyanobacteria waste a lot of energy in reacting with O2
through photorespiration instead of going through carbon fixation by catalyzing CO2. Thus, in
order to increase the fitness of the species, cyanobacteria increase their carbon fixing
efficiency by developing a special way of introducing a CO2-rich environment in proximity to
the RuBisCO [5]. As a result, the organisms evolved the current mechanism, in which the
carbonic anhydrase successfully creates an abundance of CO2 in the vicinity of the RuBisCO
in the inclusion, and makes the efficiency much higher as the cell doesn’t have to waste
energy in photorespiration. This arrangement greatly increases cyanobacteria’s fitness. The
fact that most of the RuBisCO protein located in cells may be found in carboxysomes, while

11. A REVIEW ON THE CARBOXYSOME: ITS HISTORY, STRUCTURE, FUNCTION AND APPLICATION 11
RuBisCO is the most abundant protein on earth, shows the prevalence of the carboxysome,
which indicates its importance in cyanobacterial survival [9].
Application
The world now faces a serious crisis regarding food security and food shortages,
especially with an increasing world population. Thus, increasing food production is becoming
an important task [19]. One possible way to improve food production is to improve the
efficiency of photosynthetic carbon fixation [19]. However, one of the greatest impediments
to photosynthesis is the low efficiency of RuBisCO inside chloroplasts [20]. Meanwhile,
cyanobacteria have unusually high affinity for CO2 and high efficiency in carbon fixation
because carboxysomes involved in the carbon fixation process can create an oxygen-free
inner-environment that favors photosynthesis [17, 32]. Moreover, because cyanobacteria and
chloroplasts share a common ancestor and carboxysomes are organelles inside cyanobacteria,
carboxysomes are likely to function properly after genetic modification and can help to
improve efficiency of photosynthesis by improving the carbon fixation efficiency of
RuBisCO. Consequently, researchers asked: what if we can enhance photosynthesis by
assembling functional carboxysomes inside chloroplasts?
Thus, some researchers have proposed using cyanobacterial CCM, which includes
carboxysomes, as a way of improving photosynthesis in crops [19]. Their proposed method is
to build a carbon fixation system similar to CCM inside crops. In this method, researchers
propose to assemble carboxysomes in chloroplasts via genome transformation inside
chloroplasts, which is likely to succeed because similar experiments have created structurally

12. A REVIEW ON THE CARBOXYSOME: ITS HISTORY, STRUCTURE, FUNCTION AND APPLICATION 12
correct carboxysomes in E. coli [20]. Then, through the addition of bicarbonate pumps on
chloroplast membranes and removal of chloroplast carbonic anhydrase, an effective CCM can
be constructed inside the chloroplast [19]. In the next step, carbonic anhydrase needs to be
added to the cell cytosol.
The photosynthesis of this new structure, from now on referred to as the enhanced
chloroplast, is still divided into two parts: the light-dependent reactions and the light-
independent reactions. Light-dependent reactions are reactions in photosynthesis that help to
convert light energy into chemical energy, and there is no difference in light-dependent
reactions between these enhanced chloroplasts and wild-types. In the light-dependent
reactions, light is first absorbed by a pigment called chlorophyll a inside Photosystem II,
located on the thylakoid membrane. Then, through a series of redox reactions, the light
energy absorbed helps to convert NADP into NADPH, produce ATP, and split H2O into O2
and H+
. Light-independent reactions are reactions that convert CO2 into glucose or other
sugars. These reactions are also referred to as the Calvin-Benson-Bassham cycle. Enhanced
chloroplasts perform the light-independent reactions differently in the first few steps of the
Calvin-Benson-Bassham cycle. Firstly, CO2, absorbed by the plant, is transformed to
bicarbonate in the cytosol by carbonic anhydrase, in order to prevent gaseous-state CO2 from
escaping the cell. Then, bicarbonate enters chloroplasts via the bicarbonate pumps added.
Thirdly, bicarbonate, now inside the chloroplast, enters the carboxysome and is transformed
to 3-PGA by carboxysomal carbonic anhydrase and RuBisCO, and the 3-PGA produced
enters the Calvin-Benson-Bassham cycle that ultimately leads to sugar production, using the

13. A REVIEW ON THE CARBOXYSOME: ITS HISTORY, STRUCTURE, FUNCTION AND APPLICATION 13
products of light-dependent reactions, NADPH and ATP, as oxidizing agents and energy
sources. In short, the main alteration here is in the first step of the cycle: instead of having
RuBisCO inside the stroma, this method uses an extra compartment, the carboxysome, to
enclose RuBisCO, thereby increasing the RuBisCO efficiency by blocking O2 to approach
RuBisCO.
There are many advantages to this method. Firstly, it can help to increase the net CO2
fixation by greatly improving the efficiency of RuBisCO in the Calvin-Benson-Bassham
cycle because the CO2-rich environment, created by the carboxysome, will ensure the entire
Calvin-Benson-Bassham cycle to work more efficiently without the energetically wasteful
photorespiration. Secondly, because of their close evolutionary relationship, cyanobacteria
and chloroplasts have very similar structures and inner environments; thus, the assembly of a
CCM inside chloroplasts may not be challenging. Although no systematically conclusive
evidence that such a plan can be achieved exists, it still presents an interesting angle of
research and a promising future.

14. A REVIEW ON THE CARBOXYSOME: ITS HISTORY, STRUCTURE, FUNCTION AND APPLICATION 14
Figure 5 . An illustration of the Calvin-Benson-Bassham cycle in C3 plants [33]
Here the first step is the fixation of CO2, catalyzed by RuBisCO. The method proposed will instead use
carboxysomes to fix CO2 into ribulose-1, 5-bisphosphate (RuBP).
Source: Reproduced from ref. [33]
Figure 6 . An illustration of a cyanobacteria with a carboxysome [19]
Here the circles on the membranes are either CO2 transporters or bicarbonate transporters, and CO2 leakage
means the undesirable loss of CO2 due to permeation. The cyanobacteria illustrated here is carbonic anhydrase
absent within its cytosol.
Source: Reproduced from ref. [19]

15. A REVIEW ON THE CARBOXYSOME: ITS HISTORY, STRUCTURE, FUNCTION AND APPLICATION 15
ba
c d
Figure 7 . Method for biulding a carbon concentrating mechanism inside chloroplast
a: Addition of bicarbonate pumps and enhancement of Na+
/H+
transport [19]
b: Construction of cyanobacterial carboxysomes in the stroma [19]
c: Removal of stromal carbonic anhydrase to decrease stromal RuBisCO content [19]
d: Introduction of a cyanobacterial CO2 pump [19]
Sources: Reproduced from Ref. [19]

16. A REVIEW ON THE CARBOXYSOME: ITS HISTORY, STRUCTURE, FUNCTION AND APPLICATION 16
Other Bacterial Microcompartments
Carboxysomes belong to a group of inner-cell structures referred to as bacterial
microcompartments (BMC), which can be found in many kinds of bacteria. These bacterial
microcompartments generally help the cell with metabolism and fixation of chemical
compounds.
For many years, the carboxysome was the only known polyhedral microcompartment [5].
In 1994, however, a structure formed conditionally by S. enterica during B12-dependant
growth on 1, 2-propanediol was discovered [26]. The structure was named the Pdu
microcompartment. The Pdu microcompartment is generally similar to the carboxysome both
in size and appearance. It has a diameter ranging from 100nm-150nm, and has a ~4nm
protein shell. It is composed of 14-18 different polypeptides [26]. The proposed function for
the Pdu microcompartment is to isolate a by-product of 1, 2-propanediol degradation in order
to prevent toxicity and diffusive loss [26, 27]. Thus, a functional similarity between the Pdu
compartment and the carboxysome is that they both serve to retain intermediate products of
degradation that may not be fully confined or properly coped with by lipid bilayers.
Similar structures to the carboxysome have also been discovered in S. enterica, a bacteria
that can use ethanolamine as its sole source of carbon under certain conditions [28]. These
bacteria maintain operons that enable them to form carboxysome-like large protein
complexes that are involved in the ethanolamine degradation and metabolism [29]. This new
structure is named Eut microcompartments. The Eut microcompartment, when viewed under
traditional TEM, actually lacks the icosahedral structure attributed to the carboxysome, but

17. A REVIEW ON THE CARBOXYSOME: ITS HISTORY, STRUCTURE, FUNCTION AND APPLICATION 17
the proteinaceous outer shell still is composed of regular repeating patterns of BMC domain
proteins [29]. Similar to the diffusion of CO2 through the outer shell of carboxysome,
ethanolamine enters the lumen of the Eut microcompartment through pores found on the
outer shell. A functional analogy seen between the Eut microcompartment and the
carboxysome is that they are both involved in retaining certain metabolic intermediates and in
the enhancement of metabolism and of energy production [28].
Further Directions of Study
Although our knowledge about carboxysomes has greatly increased in recent years, we
now possess only the general picture, and there are certainly a few pieces missing. Firstly, we
don’t yet understand the distribution of the variety of similar proteins in the outer shell, nor
do we understand the factors behind the evolution of several similar proteins carrying similar
tasks [5]. Secondly, we need further experimentation to confirm the proposed models for
diffusion across the shell [5]. Thirdly, we don’t yet completely understand the functions and
structures of some of the proteins inside carboxysomes [5]. Finally, more experimentation on
the possible future utilization needs to be conducted, both through bioengineering and
through structural studies.
References
1. Stockel, J., Elvitigala, T., Liberton, M., and Pakrasi, H. (2013). Carbon Availability Affects Diurnally
Controlled Processes and Cell Morphology of Cyanothece 51142. PLoS one 8, 1-10
2. Cannon, G., Bradburne, C., Aldrich, H., Baker, S., Heinhorst, S., and Shively, J. (2001).

18. A REVIEW ON THE CARBOXYSOME: ITS HISTORY, STRUCTURE, FUNCTION AND APPLICATION 18
Microcompartments in Prokaryotes: Carboxysomes and Related Polyhedra. Applied and Environmental
Biology 67, 12.
3. Tanaka, S., Kerfeld, C., Sawaya, M., Heinhorst, S., Cannon, G., and Yeates, T. (2008). Atomic-Level
Models of the Bacterial Carboxysome Shell. Science 319, 1083-1086.
4. Kerfeld, C., Greenleaf, W., and Kinney, J. (2010). The Carboxysome and Other Bacterial
Microcompartments. Microbe 5, 257-263
5. Cannon, G., Kerfeld, C., Aldrich, H., Yeates, T., Heinhorst, S., and Shively, J. (2001). Protein-based
organelles in bacteria: carboxysomes and related microcompartments. Nature 6, 681-691.
6. Kerfeld, C., Sawaya, M., Tanaka, S., Nguyen, C., Phillips, M., Beeby, M., and Yeates, T. (2005). Protein
Structures Forming the Shell of Primitive Bacterial Organelles. Science 309, 936–938.
7. Chen, A., Robinson-Mosher, A., Savage, D., Silver, P., and Polka, J. (2013). The Bacterial Carbon-Fixing
Organelle Is Formed by Shell Envelopment of Preassembled Cargo. PLoS one 8, 1-13
8. Peña, K., Castel, S., Araujo, C., Espie, G., and Kimber, M. (2010). Structural basis of the oxidative
activation of the carboxysomal gamma-carbonic anhydrase, CcmM. Proceedings of the National Academy
of Sciences of the United States of America 107, 2455–60.
9. Badger, M., and Price, G. (2003). CO2 concentrating mechanisms in cyanobacteria: molecular components,
their diversity and evolution. Journal of Experimental Botany 54, 609–622.
10. Savage, D., Afonso, B., Chen, A., and Silver, P. (2010). Spatially ordered dynamics of the bacterial carbon
fixation machinery. Science 327, 1258–61.
11. Iancu, C. V., Ding, J. H., Morris, D. M., Dias, P. D., Gonzales, A. D., Martino, A., and Jensen, G. J. (2007).
The Structure of Isolated Synechococcus Strain WH8102 Carboxysomes as Revealed by Electron
Cryotomography. Journal of Molecular Biology 372, 764–773.
12. Schmid, M., Paredes, A., Khant, h., Soyer, F., Aldrich, H., Chiu, W., and Shively, J. (2006). "Structure of
Halothiobacillus neapolitanus Carboxysomes by Cryo-electron Tomography." Journal of Molecular
Biology 364, 526-535.
13. Iancu, C., Morris, D., Dou, Z., Heinhorst, S., Cannon, G., and Jensen, G. (2010). Organization, structure,
and assembly of alpha-carboxysomes determined by electron cryotomography of intact cells. Journal of
molecular biology 396, 105–17
14. Reinfelder, J. R. (2011). Carbon Concentrating Mechanisms in Eukaryotic Marine Phytoplankton. Annual

19. A REVIEW ON THE CARBOXYSOME: ITS HISTORY, STRUCTURE, FUNCTION AND APPLICATION 19
Review of Marine Science 3, 291-315.
15. Levitan, O., Sudhaus, S., LaRoche, J., and Berman-Frank, I. (2010). The influence of pCO2 and temperature
on gene expression of carbon and nitrogen pathways in Trichodesmium IMS101. PloS one 5, 1-11
16. Price, G., Badger, M., Woodger, F., and Long, B. (2008). Advances in understanding the cyanobacterial
CO2-concentrating-mechanism (CCM): functional components, Ci transporters, diversity, genetic regulation
and prospects for engineering into plants. Journal of Experimental Botany 59, 1441–1461.
17. Fukuzawa, H., Suzuki, E., Komukai, Y., and Miyachi, S. (1992). A gene homologous to chloroplast
carbonic anhydrase (icfA) is essential to photosynthetic carbon dioxide fixation by Synechococcus
PCC7942. Proceedings of the National Academy of Sciences 89, 4437–4441.
18. Mitra, M., Lato, S., Ynalvez, R., Xiao, Y., and Moroney, J. (2004). Identification of a New Chloroplast
Carbonic Anhydrase in Chlamydomonas reinhardtii. Plant Physiology 135, 173–182.
19. Price, G. D., Pengelly, J. J., Forster, B., Du, J., Whitney, S. M., von Caemmerer, S., Badger, M. R., Howitt,
S. M., and Evans, J. R. (2013). The cyanobacterial CCM as a source of genes for improving photosynthetic
CO2 fixation in crop species. Journal of experimental botany 64, 753–768.
20. Bonacci, W., Teng, P., Afonso, B., Niederholtmeyer, H., Grob, P., Silver, P., and Savage, D. (2012).
Modularity of a carbon-fixing protein organelle. Proceedings of the National Academy of Sciences of the
United States of America 109, 478–483.
21. Riding, R. (2006). Cyanobacterial calcification, carbon dioxide concentrating mechanisms, and Proterozoic
Cambrian changes in atmospheric composition. Geobiology 4, 299-316.
22. Lal, R. (2008). Carbon sequestration. Philosophical Transactions of the Royal Society B: Biological
Sciences 363, 815-830.
23. Nogia, P., Sidhu, G., Mehrotra, R., and Mehrotra, S. (2013). Capturing atmospheric carbon: biological and
nonbiological methods. International Journal of Low-Carbon Technologies, 1-9
24. Yamasaki, A. An Overview of CO2 Mitigation Options for Global Warming-Emphasizing CO2 Sequestration
Options. Journal of Chemical Engineering of Japan, 361-375.
25. Heffelfinger, G., Martino, A., Gorin, A., Xu, Y., Rintoul, M., Geist, A., Al-Hashimi, H., Davidson, G.,
Faulon, J., Frink, L., Haaland, D., Hart, W., Jakobsson, E., Lane, T., Li, M., Locascio, P., Olken, F., Olman,
V., Palenik, B., Plimpton, S., Roe, D., Samatova, N., Shah, M., Shoshoni, A., Strauss, C., Thomas, E.,
Timlin, J., and Xu, D. (2002). Carbon sequestration in Synechococcus Sp.: from molecular machines to

20. A REVIEW ON THE CARBOXYSOME: ITS HISTORY, STRUCTURE, FUNCTION AND APPLICATION 20
hierarchical modeling. Omics : A Journal of Integrative Biology 6, 305–330.
26. Cheng, S., Liu, Y., Crowley, C., Yeates, T., and Bobik, T. (2008). Bacterial microcompartments: their
properties and paradoxes. BioEssays : News and Reviews in Molecular, Cellular and Developmental
Biology 30, 1084–1095.
27. Havemann, G. D., Sampson, E. M., and Bobik, T. A. (2002). PduA is a shell protein of polyhedral
organelles involved in coenzyme B12-dependent degradation of 1, 2-propanediol in Salmonella enterica
serovar typhimurium LT2. Journal of bacteriology 184, 1253–1261.
28. Penrod, J., and Roth, J. (2006). Conserving a Volatile Metabolite: a Role for Carboxysome-Like Organelles
in Salmonella enterica. Journal of Bacteriology 188, 2865-2874.
29. Held, M., Quin, M., and Schmidt-Dannert, C. (2013). Eut Bacterial Microcompartments: Insights into Their
Function, Structure, and Bioengineering Applications. Journal of Molecular Microbiology and
Biotechnology 23, 308-320.
30. Bustin, E. (2013). Cloning and Expression of the cbbO (0910) Gene from Halothiobacillus neapolitanus
and Its Potential to Code for RuBisCO Activase. Honors Theses 156, 1-35
31. Cameron, J., Wilson, S., Bernstein, S., and Kerfeld, C. (2013). Biogenesis of a Bacterial Organelle: The
Carboxysome Assembly Pathway. Cell 155, 1131-1140.
32. Zarzycki, J., Axen, S., Kinney, J., and Kerfeld, C. (2013). Cyanobacterial-based approaches to improving
photosynthesis in plants. Journal of Experimental Botany 64, 787-798.
33. Raines, C., Lloyd, J., and Dyer, T. (1997). Molecular biology of the C3 photosynthetic carbon reduction
cycle. Photosynthesis Research 27, 1-14.
Used Abbreviations:
RuBisCO - Ribulose-1, 5-bisphosphate carboxylase/oxygenase
BMC - Bacterial Microcompartment
ECT - Electron Cryotomography
CCM - Carbon Concentrating Mechanism
RuBP - Ribulose-1, 5-bisphosphate
3-PGA - 3-phosphoglycerate
G3P - Glyceraldehyde 3-phosphate

21. A REVIEW ON THE CARBOXYSOME: ITS HISTORY, STRUCTURE, FUNCTION AND APPLICATION 21
E. coli - Escherichia coli
pCO2 - Partial Pressure of CO2
S. enterica - Salmonella enterica
TEM - Transmission Electron Microscopy
NADP - Nicotinamide adenine dinucleotide phosphate
NADPH - Reduced nicotinamide adenine dinucleotide phosphate