Carboxysomes are
bacterial microcompartment
Bacterial microcompartments (BMCs) are organelle-like structures found in bacteria. They consist of a protein shell that encloses enzymes and other proteins. BMCs are typically about 40–200 nanometers in diameter and are made entirely of protei ...
s (BMCs) consisting of polyhedral protein shells filled with the enzymes ribulose-1,5-bisphosphate carboxylase/oxygenase (
RuBisCO
Ribulose-1,5-bisphosphate carboxylase-oxygenase, commonly known by the abbreviations RuBisCo, rubisco, RuBPCase, or RuBPco, is an enzyme () involved in the first major step of carbon fixation, a process by which atmospheric carbon dioxide is con ...
)—the predominant enzyme in
carbon fixation
Biological carbon fixation or сarbon assimilation is the process by which inorganic carbon (particularly in the form of carbon dioxide) is converted to organic compounds by living organisms. The compounds are then used to store energy and as ...
and the
rate limiting enzyme in the
Calvin cycle
The Calvin cycle, light-independent reactions, bio synthetic phase, dark reactions, or photosynthetic carbon reduction (PCR) cycle of photosynthesis is a series of chemical reactions that convert carbon dioxide and hydrogen-carrier compounds into ...
—and
carbonic anhydrase
The carbonic anhydrases (or carbonate dehydratases) () form a family of enzymes that catalyze the interconversion between carbon dioxide and water and the dissociated ions of carbonic acid (i.e. bicarbonate and hydrogen ions). The active site ...
.
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
carbon dioxide-concentrating mechanism (CCM).
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
Transmission electron microscopy (TEM) is a microscopy technique in which a beam of electrons is transmitted through a specimen to form an image. The specimen is most often an ultrathin section less than 100 nm thick or a suspension on a g ...
in the
cyanobacterium
Cyanobacteria (), also known as Cyanophyta, are a phylum of gram-negative bacteria that obtain energy via photosynthesis. The name ''cyanobacteria'' refers to their color (), which similarly forms the basis of cyanobacteria's common name, blue ...
''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
''Halothiobacillus'' is a genus in the ''Gammaproteobacteria''. Both species are obligate aerobic bacteria; they require oxygen to grow. They are also halotolerant; they live in environments with high concentrations of salt or other solutes, bu ...
'', ''
Acidithiobacillus
''Acidithiobacillus'' is a genus of the ''Acidithiobacillia'' in the " Pseudomonadota". The genus includes acidophilic organisms capable of iron and/or sulfur oxidation. Like all ''"Pseudomonadota"'', ''Acidithiobacillus'' spp. are Gram-negative. ...
'', ''
Nitrobacter
''Nitrobacter'' is a genus comprising rod-shaped, gram-negative, and chemoautotrophic bacteria. The name ''Nitrobacter'' derives from the Latin neuter gender noun ''nitrum, nitri'', alkalis; the Ancient Greek noun βακτηρία'','' βακτ ...
'' and ''Nitrococcus''; all belonging to
Pseudomonadota
Pseudomonadota (synonym Proteobacteria) is a major phylum of Gram-negative bacteria. The renaming of phyla in 2021 remains controversial among microbiologists, many of whom continue to use the earlier names of long standing in the literature. The ...
).
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
![Carboxysome_structural_model](https://upload.wikimedia.org/wikipedia/commons/f/ff/Carboxysome_structural_model.jpg)
Structurally, carboxysomes are icosahedral, or quasi-
icosahedral
In geometry, an icosahedron ( or ) is a polyhedron with 20 faces. The name comes and . The plural can be either "icosahedra" () or "icosahedrons".
There are infinitely many non- similar shapes of icosahedra, some of them being more symmetrica ...
.
Electron cryo-tomography studies
have confirmed the approximately icosahedral geometry of the carboxysome, and have imaged protein molecules inside (presumed to be RuBisCO), arranged in a few concentric layers.
The non-icosahedral faceted shapes of some carboxysomes can naturally be explained within the elastic theory of heterogeneous thin shells.
The carboxysome has an outer shell composed of a few thousand protein subunits, which encapsulates a CO
2-producing enzyme (carbonic anhydrase) and a carbon-fixing enzyme (RuBisCO). Proteins known to form the shell have been structurally characterized by
X-ray crystallography
X-ray crystallography is the experimental science determining the atomic and molecular structure of a crystal, in which the crystalline structure causes a beam of incident X-rays to diffract into many specific directions. By measuring the angles ...
. 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.
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, some nitrifying bacteria, some sulfur-oxidizing bacteria (for example, ''Halothiobacillus neapolitanus''), and some
purple bacteria
Purple bacteria or purple photosynthetic bacteria are Gram-negative proteobacteria that are phototrophic, capable of producing their own food via photosynthesis. They are pigmented with bacteriochlorophyll ''a'' or ''b'', together with various ...
; these are all classified as
Pseudomonadota
Pseudomonadota (synonym Proteobacteria) is a major phylum of Gram-negative bacteria. The renaming of phyla in 2021 remains controversial among microbiologists, many of whom continue to use the earlier names of long standing in the literature. The ...
). 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 CsoS2 and CsoSCA. The CsoS2 protein has a very high
pI and a unique primary structure. The primary structure of CsoS2 appears tripartite, composed of an N-terminal, a middle- and a C-terminal region.
Repetitive motifs can be identified in the N-terminal and middle regions. Recently, it was proposed to be an intrinsically disordered protein with an essential role in alpha-carboxysome assembly. CsoSCA is a shell-associated beta-carbonic anhydrase.
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
Cyanobacteria (), also known as Cyanophyta, are a phylum of gram-negative bacteria that obtain energy via photosynthesis. The name ''cyanobacteria'' refers to their color (), which similarly forms the basis of cyanobacteria's common name, blu ...
.
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
Synthetic biology (SynBio) is a multidisciplinary area of research that seeks to create new biological parts, devices, and systems, or to redesign systems that are already found in nature.
It is a branch of science that encompasses a broad ran ...
.
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 improveme 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.
See also
*
Bacterial microcompartment
Bacterial microcompartments (BMCs) are organelle-like structures found in bacteria. They consist of a protein shell that encloses enzymes and other proteins. BMCs are typically about 40–200 nanometers in diameter and are made entirely of protei ...
*
BMC domain
In molecular biology the Bacterial Microcompartment (BMC) domain is a protein domain found in a variety of shell proteins, including CsoS1A, CsoS1B and CsoS1C of ''Thiobacillus neapolitanus'' (''Halothiobacillus neapolitanus'') and their orthologs ...
*
RuBisCO
Ribulose-1,5-bisphosphate carboxylase-oxygenase, commonly known by the abbreviations RuBisCo, rubisco, RuBPCase, or RuBPco, is an enzyme () involved in the first major step of carbon fixation, a process by which atmospheric carbon dioxide is con ...
*
Pyrenoid
Pyrenoids are sub-cellular micro-compartments found in chloroplasts of many algae,Giordano, M., Beardall, J., & Raven, J. A. (2005). CO2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. Annu. Rev. Plant Bio ...
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External links
Mysterious Bacterial Microcompartments Revealed By Biochemists
Cell anatomy
Organelles
Protein complexes