RuBisCO

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Ribulose-1,5-bisphosphate carboxylase oxygenase
SpinachRuBisCO.png
A 3d depiction of the activated RuBisCO from spinach in open form with active site accessible. The active site Lys175 residues are marked in pink, and a close-up of the residue is provided to the right for one of the monomers composing the enzyme.
Identifiers
EC no. 4.1.1.39
CAS no. 9027-23-0
Databases
IntEnz IntEnz view
BRENDA BRENDA entry
ExPASy NiceZyme view
KEGG KEGG entry
MetaCyc metabolic pathway
PRIAM profile
PDB structures RCSB PDB PDBe PDBsum
Gene Ontology AmiGO / QuickGO
Search
PMC articles
PubMed articles
NCBI proteins

Ribulose-1,5-bisphosphate carboxylase/oxygenase, commonly known by the abbreviations RuBisCo, rubisco, [1] RuBPCase, [2] or RuBPco, [3] is an enzyme (EC 4.1.1.39) involved in the light-independent (or "dark") part of photosynthesis, including the carbon fixation by which atmospheric carbon dioxide is converted by plants and other photosynthetic organisms to energy-rich molecules such as glucose. It emerged approximately four billion years ago in primordial metabolism prior to the presence of oxygen on Earth. [4] It is probably the most abundant enzyme on Earth. In chemical terms, it catalyzes the carboxylation of ribulose-1,5-bisphosphate (also known as RuBP). [5] [6] [7]

Contents

Alternative carbon fixation pathways

RuBisCO is important biologically because it catalyzes the primary chemical reaction by which inorganic carbon enters the biosphere. While many autotrophic bacteria and archaea fix carbon via the reductive acetyl CoA pathway, the 3-hydroxypropionate cycle, or the reverse Krebs cycle, these pathways are relatively small contributors to global carbon fixation compared to that catalyzed by RuBisCO. Phosphoenolpyruvate carboxylase, unlike RuBisCO, only temporarily fixes carbon. Reflecting its importance, RuBisCO is the most abundant protein in leaves, accounting for 50% of soluble leaf protein in C3 plants (20–30% of total leaf nitrogen) and 30% of soluble leaf protein in C4 plants (5–9% of total leaf nitrogen). [7] Given its important role in the biosphere, the genetic engineering of RuBisCO in crops is of continuing interest (see below).

Structure

Active site of RuBisCO of Galdieria sulphuraria with CO2: Residues involved in both the active site and stabilizing CO2 for enzyme catalysis are shown in color and labeled. Distances of the hydrogen bonding interactions are shown in angstroms. .mw-parser-output .template-chem2-su{display:inline-block;font-size:80%;line-height:1;vertical-align:-0.35em}.mw-parser-output .template-chem2-su>span{display:block;text-align:left}.mw-parser-output sub.template-chem2-sub{font-size:80%;vertical-align:-0.35em}.mw-parser-output sup.template-chem2-sup{font-size:80%;vertical-align:0.65em} Mg ion (green sphere) is shown coordinated to CO2, and is followed by three water molecules (red spheres). All other residues are placed in grayscale. RuBisCOActiveSite2.png
Active site of RuBisCO of Galdieria sulphuraria with CO2: Residues involved in both the active site and stabilizing CO2 for enzyme catalysis are shown in color and labeled. Distances of the hydrogen bonding interactions are shown in angstroms. Mg ion (green sphere) is shown coordinated to CO2, and is followed by three water molecules (red spheres). All other residues are placed in grayscale.
Location of the rbcL gene in the chloroplast genome of Arabidopsis thaliana (positions ca. 55-56.4 kb). rbcL is one of the 21 protein-coding genes involved in photosynthesis (green boxes). Plastomap of Arabidopsis thaliana.svg
Location of the rbcL gene in the chloroplast genome of Arabidopsis thaliana (positions ca. 55-56.4 kb). rbcL is one of the 21 protein-coding genes involved in photosynthesis (green boxes).

In plants, algae, cyanobacteria, and phototrophic and chemoautotrophic Pseudomonadota (formerly proteobacteria), the enzyme usually consists of two types of protein subunit, called the large chain (L, about 55,000 Da) and the small chain (S, about 13,000 Da). The large-chain gene (rbcL) is encoded by the chloroplast DNA in plants. [8] There are typically several related small-chain genes in the nucleus of plant cells, and the small chains are imported to the stromal compartment of chloroplasts from the cytosol by crossing the outer chloroplast membrane. [6] [9] The enzymatically active substrate (ribulose 1,5-bisphosphate) binding sites are located in the large chains that form dimers in which amino acids from each large chain contribute to the binding sites. A total of eight large chains (= four dimers) and eight small chains assemble into a larger complex of about 540,000 Da. [10] In some Pseudomonadota and dinoflagellates, enzymes consisting of only large subunits have been found. [lower-alpha 1]

Magnesium ions (Mg2+) are needed for enzymatic activity. Correct positioning of Mg2+ in the active site of the enzyme involves addition of an "activating" carbon dioxide molecule (CO2) to a lysine in the active site (forming a carbamate). [12] Mg2+ operates by driving deprotonation of the Lys210 residue, causing the Lys residue to rotate by 120 degrees to the trans conformer, decreasing the distance between the nitrogen of Lys and the carbon of CO2. The close proximity allows for the formation of a covalent bond, resulting in the carbamate. [13] Mg2+ is first enabled to bind to the active site by the rotation of His335 to an alternate conformation. Mg2+ is then coordinated by the His residues of the active site (His300, His302, His335), and is partially neutralized by the coordination of three water molecules and their conversion to −OH. [13] This coordination results in an unstable complex, but produces a favorable environment for the binding of Mg2+. Formation of the carbamate is favored by an alkaline pH. The pH and the concentration of magnesium ions in the fluid compartment (in plants, the stroma of the chloroplast) increases in the light. The role of changing pH and magnesium ion levels in the regulation of RuBisCO enzyme activity is discussed below. Once the carbamate is formed, His335 finalizes the activation by returning to its initial position through thermal fluctuation. [13]

RuBisCO large chain,
catalytic domain
Identifiers
SymbolRuBisCO_large
Pfam PF00016
InterPro IPR000685
PROSITE PDOC00142
SCOP2 3rub / SCOPe / SUPFAM
CDD cd08148
Available protein structures:
Pfam   structures / ECOD  
PDB RCSB PDB; PDBe; PDBj
PDBsum structure summary
PDB 1aa1 ​, 1aus ​, 1bwv ​, 1bxn ​, 1ej7 ​, 1geh ​, 1gk8 ​, 1ir1 ​, 1ir2 ​, 1iwa ​, 1rba ​, 1rbl ​, 1rbo ​, 1rco ​, 1rcx ​, 1rld ​, 1rsc ​, 1rus ​, 1rxo ​, 1svd ​, 1tel ​, 1upm ​, 1upp ​, 1uw9 ​, 1uwa ​, 1uzd ​, 1uzh ​, 1wdd ​, 1ykw ​, 2cwx ​, 2cxe ​, 2d69 ​, 2qyg ​, 2rus ​, 2v63 ​, 2v67 ​, 2v68 ​, 2v69 ​, 2v6a ​, 3rub ​, 4rub ​, 5rub ​, 8ruc ​, 9rub ​
RuBisCO, N-terminal domain
Identifiers
SymbolRuBisCO_large_N
Pfam PF02788
InterPro IPR017444
SCOP2 3rub / SCOPe / SUPFAM
Available protein structures:
Pfam   structures / ECOD  
PDB RCSB PDB; PDBe; PDBj
PDBsum structure summary
PDB 1aa1 ​, 1aus ​, 1bwv ​, 1bxn ​, 1ej7 ​, 1geh ​, 1gk8 ​, 1ir1 ​, 1ir2 ​, 1iwa ​, 1rba ​, 1rbl ​, 1rbo ​, 1rco ​, 1rcx ​, 1rld ​, 1rsc ​, 1rus ​, 1rxo ​, 1svd ​, 1tel ​, 1upm ​, 1upp ​, 1uw9 ​, 1uwa ​, 1uzd ​, 1uzh ​, 1wdd ​, 1ykw ​, 2cwx ​, 2cxe ​, 2d69 ​, 2qyg ​, 2rus ​, 2v63 ​, 2v67 ​, 2v68 ​, 2v69 ​, 2v6a ​, 3rub ​, 4rub ​, 5rub ​, 8ruc ​, 9rub ​
RuBisCO, small chain
Identifiers
SymbolRuBisCO_small
Pfam PF00101
InterPro IPR000894
SCOP2 3rub / SCOPe / SUPFAM
CDD cd03527
Available protein structures:
Pfam   structures / ECOD  
PDB RCSB PDB; PDBe; PDBj
PDBsum structure summary
PDB 1aa1 ​, 1aus ​, 1bwv ​, 1bxn ​, 1ej7 ​, 1gk8 ​, 1ir1 ​, 1ir2 ​, 1iwa ​, 1rbl ​, 1rbo ​, 1rco ​, 1rcx ​, 1rlc ​, 1rld ​, 1rsc ​, 1rxo ​, 1svd ​, 1upm ​, 1upp ​, 1uw9 ​, 1uwa ​, 1uzd ​, 1uzh ​, 1wdd ​, 2v63 ​, 2v67 ​, 2v68 ​, 2v69 ​, 2v6a ​, 3rub ​, 4rub ​, 8ruc ​

Enzymatic activity

Two main reactions of RuBisCo: CO2 fixation and oxygenation. RuBisCO reaction CO2 or O2.svg
Two main reactions of RuBisCo: CO2 fixation and oxygenation.

RuBisCO is one of many enzymes in the Calvin cycle. When Rubisco facilitates the attack of CO2 at the C2 carbon of RuBP and subsequent bond cleavage between the C3 and C2 carbon, 2 molecules of glycerate-3-phosphate are formed. The conversion involves these steps: enolisation, carboxylation, hydration, C-C bond cleavage, and protonation. [14] [15] [16]

Substrates

Substrates for RuBisCO are ribulose-1,5-bisphosphate and carbon dioxide (distinct from the "activating" carbon dioxide). RuBisCO also catalyses a reaction of ribulose-1,5-bisphosphate and molecular oxygen (O2) instead of carbon dioxide (CO2). [17] Discriminating between the substrates CO2 and O2 is attributed to the differing interactions of the substrate's quadrupole moments and a high electrostatic field gradient. [13] This gradient is established by the dimer form of the minimally active RuBisCO, which with its two components provides a combination of oppositely charged domains required for the enzyme's interaction with O2 and CO2. These conditions help explain the low turnover rate found in RuBisCO: In order to increase the strength of the electric field necessary for sufficient interaction with the substrates’ quadrupole moments, the C- and N- terminal segments of the enzyme must be closed off, allowing the active site to be isolated from the solvent and lowering the dielectric constant. [18] This isolation has a significant entropic cost, and results in the poor turnover rate.

Binding RuBP

Carbamylation of the ε-amino group of Lys210 is stabilized by coordination with the Mg2+. [19] This reaction involves binding of the carboxylate termini of Asp203 and Glu204 to the Mg2+ ion. The substrate RuBP binds Mg2+ displacing two of the three aquo ligands. [14] [20] [21]

Enolisation

Enolisation of RuBP is the conversion of the keto tautomer of RuBP to an enediol(ate). Enolisation is initiated by deprotonation at C3. The enzyme base in this step has been debated, [20] [22] but the steric constraints observed in crystal structures have made Lys210 the most likely candidate. [14] Specifically, the carbamate oxygen on Lys210 that is not coordinated with the Mg ion deprotonates the C3 carbon of RuBP to form a 2,3-enediolate. [20] [21]

Carboxylation

A 3D image of the active site of spinach RuBisCO complexed with the inhibitor 2-carboxyarabinitol-1,5-bisphosphate, CO2, and Mg. (PDB: 1IR1; Ligand View [CAP]501:A) Crystal structure of active site of RuBisCO bound to 2-Carboxyarabinitol-1,5-Bisphosphate.png
A 3D image of the active site of spinach RuBisCO complexed with the inhibitor 2-carboxyarabinitol-1,5-bisphosphate, CO2, and Mg. (PDB: 1IR1; Ligand View [CAP]501:A)

Carboxylation of the 2,3-enediolate results in the intermediate 3-keto-2-carboxyarabinitol-1,5-bisphosphate and Lys334 is positioned to facilitate the addition of the CO2 substrate as it replaces the third Mg2+-coordinated water molecule and add directly to the enediol. No Michaelis complex is formed in this process. [14] [22] Hydration of this ketone results in an additional hydroxy group on C3, forming a gem-diol intermediate. [20] [23] Carboxylation and hydration have been proposed as either a single concerted step [20] or as two sequential steps. [23] Concerted mechanism is supported by the proximity of the water molecule to C3 of RuBP in multiple crystal structures. Within the spinach structure, other residues are well placed to aid in the hydration step as they are within hydrogen bonding distance of the water molecule. [14]

C-C bond cleavage

The gem-diol intermediate cleaves at the C2-C3 bond to form one molecule of glycerate-3-phosphate and a negatively charged carboxylate. [14] Stereo specific protonation of C2 of this carbanion results in another molecule of glycerate-3-phosphate. This step is thought to be facilitated by Lys175 or potentially the carbamylated Lys210. [14]

Products

When carbon dioxide is the substrate, the product of the carboxylase reaction is an unstable six-carbon phosphorylated intermediate known as 3-keto-2-carboxyarabinitol-1,5-bisphosphate, which decays rapidly into two molecules of glycerate-3-phosphate. This product, also known as 3-phosphoglycerate, can be used to produce larger molecules such as glucose.

When molecular oxygen is the substrate, the products of the oxygenase reaction are phosphoglycolate and 3-phosphoglycerate. Phosphoglycolate is recycled through a sequence of reactions called photorespiration, which involves enzymes and cytochromes located in the mitochondria and peroxisomes (this is a case of metabolite repair). In this process, two molecules of phosphoglycolate are converted to one molecule of carbon dioxide and one molecule of 3-phosphoglycerate, which can reenter the Calvin cycle. Some of the phosphoglycolate entering this pathway can be retained by plants to produce other molecules such as glycine. At ambient levels of carbon dioxide and oxygen, the ratio of the reactions is about 4 to 1, which results in a net carbon dioxide fixation of only 3.5. Thus, the inability of the enzyme to prevent the reaction with oxygen greatly reduces the photosynthetic capacity of many plants. Some plants, many algae, and photosynthetic bacteria have overcome this limitation by devising means to increase the concentration of carbon dioxide around the enzyme, including C4 carbon fixation, crassulacean acid metabolism, and the use of pyrenoid.

Rubisco side activities can lead to useless or inhibitory by-products. Important inhibitory by-products include xylulose 1,5-bisphosphate and glycero-2,3-pentodiulose 1,5-bisphosphate, both caused by "misfires" halfway in the enolisation-carboxylation reaction. In higher plants, this process causes RuBisCO self-inhibition, which can be triggered by saturating CO2 and RuBP concentrations and solved by Rubisco activase (see below). [24]

Rate of enzymatic activity

Overview of the Calvin cycle and carbon fixation. Calvin-cycle4.svg
Overview of the Calvin cycle and carbon fixation.

Some enzymes can carry out thousands of chemical reactions each second. However, RuBisCO is slow, fixing only 3-10 carbon dioxide molecules each second per molecule of enzyme. [25] The reaction catalyzed by RuBisCO is, thus, the primary rate-limiting factor of the Calvin cycle during the day. Nevertheless, under most conditions, and when light is not otherwise limiting photosynthesis, the speed of RuBisCO responds positively to increasing carbon dioxide concentration.

RuBisCO is usually only active during the day, as ribulose 1,5-bisphosphate is not regenerated in the dark. This is due to the regulation of several other enzymes in the Calvin cycle. In addition, the activity of RuBisCO is coordinated with that of the other enzymes of the Calvin cycle in several other ways:

By ions

Upon illumination of the chloroplasts, the pH of the stroma rises from 7.0 to 8.0 because of the proton (hydrogen ion, H+) gradient created across the thylakoid membrane. The movement of protons into thylakoids is driven by light and is fundamental to ATP synthesis in chloroplasts (Further reading: Photosynthetic reaction centre; Light-dependent reactions). To balance ion potential across the membrane, magnesium ions (Mg2+) move out of the thylakoids in response, increasing the concentration of magnesium in the stroma of the chloroplasts. RuBisCO has a high optimal pH (can be >9.0, depending on the magnesium ion concentration) and, thus, becomes "activated" by the introduction of carbon dioxide and magnesium to the active sites as described above.

By RuBisCO activase

In plants and some algae, another enzyme, RuBisCO activase (Rca, GO:0046863, P10896 ), is required to allow the rapid formation of the critical carbamate in the active site of RuBisCO. [26] [27] This is required because ribulose 1,5-bisphosphate (RuBP) binds more strongly to the active sites of RuBisCO when excess carbamate is present, preventing processes from moving forward. In the light, RuBisCO activase promotes the release of the inhibitory (or — in some views — storage) RuBP from the catalytic sites of RuBisCO. Activase is also required in some plants (e.g., tobacco and many beans) because, in darkness, RuBisCO is inhibited (or protected from hydrolysis) by a competitive inhibitor synthesized by these plants, a substrate analog 2-carboxy-D-arabitinol 1-phosphate (CA1P). [28] CA1P binds tightly to the active site of carbamylated RuBisCO and inhibits catalytic activity to an even greater extent. CA1P has also been shown to keep RuBisCO in a conformation that is protected from proteolysis. [29] In the light, RuBisCO activase also promotes the release of CA1P from the catalytic sites. After the CA1P is released from RuBisCO, it is rapidly converted to a non-inhibitory form by a light-activated CA1P-phosphatase. Even without these strong inhibitors, once every several hundred reactions, the normal reactions with carbon dioxide or oxygen are not completed; other inhibitory substrate analogs are still formed in the active site. Once again, RuBisCO activase can promote the release of these analogs from the catalytic sites and maintain the enzyme in a catalytically active form. However, at high temperatures, RuBisCO activase aggregates and can no longer activate RuBisCO. This contributes to the decreased carboxylating capacity observed during heat stress. [30] [31]

By activase

The removal of the inhibitory RuBP, CA1P, and the other inhibitory substrate analogs by activase requires the consumption of ATP. This reaction is inhibited by the presence of ADP, and, thus, activase activity depends on the ratio of these compounds in the chloroplast stroma. Furthermore, in most plants, the sensitivity of activase to the ratio of ATP/ADP is modified by the stromal reduction/oxidation (redox) state through another small regulatory protein, thioredoxin. In this manner, the activity of activase and the activation state of RuBisCO can be modulated in response to light intensity and, thus, the rate of formation of the ribulose 1,5-bisphosphate substrate. [32]

By phosphate

In cyanobacteria, inorganic phosphate (Pi) also participates in the co-ordinated regulation of photosynthesis: Pi binds to the RuBisCO active site and to another site on the large chain where it can influence transitions between activated and less active conformations of the enzyme. In this way, activation of bacterial RuBisCO might be particularly sensitive to Pi levels, which might cause it to act in a similar way to how RuBisCO activase functions in higher plants. [33]

By carbon dioxide

Since carbon dioxide and oxygen compete at the active site of RuBisCO, carbon fixation by RuBisCO can be enhanced by increasing the carbon dioxide level in the compartment containing RuBisCO (chloroplast stroma). Several times during the evolution of plants, mechanisms have evolved for increasing the level of carbon dioxide in the stroma (see C4 carbon fixation). The use of oxygen as a substrate appears to be a puzzling process, since it seems to throw away captured energy. However, it may be a mechanism for preventing carbohydrate overload during periods of high light flux. This weakness in the enzyme is the cause of photorespiration, such that healthy leaves in bright light may have zero net carbon fixation when the ratio of O2 to CO2 available to RuBisCO shifts too far towards oxygen. This phenomenon is primarily temperature-dependent: high temperatures can decrease the concentration of CO2 dissolved in the moisture of leaf tissues. This phenomenon is also related to water stress: since plant leaves are evaporatively cooled, limited water causes high leaf temperatures. C4 plants use the enzyme PEP carboxylase initially, which has a higher affinity for CO2. The process first makes a 4-carbon intermediate compound, hence the name C4 plants, which is shuttled into a site of C3 photosynthesis then decarboxylated, releasing CO2 to boost the concentration of CO2.

Crassulacean acid metabolism (CAM) plants keep their stomata closed during the day, which conserves water but prevents the light-independent reactions (a.k.a. the Calvin Cycle) from taking place, since these reactions require CO2 to pass by gas exchange through these openings. Evaporation through the upper side of a leaf is prevented by a layer of wax.

Genetic engineering

Since RuBisCO is often rate-limiting for photosynthesis in plants, it may be possible to improve photosynthetic efficiency by modifying RuBisCO genes in plants to increase catalytic activity and/or decrease oxygenation rates. [34] [35] [36] [37] This could improve sequestration of CO2 and be a strategy to increase crop yields. [38] Approaches under investigation include transferring RuBisCO genes from one organism into another organism, engineering Rubisco activase from thermophilic cyanobacteria into temperature sensitive plants, increasing the level of expression of RuBisCO subunits, expressing RuBisCO small chains from the chloroplast DNA, and altering RuBisCO genes to increase specificity for carbon dioxide or otherwise increase the rate of carbon fixation. [39] [40]

Mutagenesis in plants

In general, site-directed mutagenesis of RuBisCO has been mostly unsuccessful, [38] though mutated forms of the protein have been achieved in tobacco plants with subunit C4 species, [41] and a RuBisCO with more C4-like kinetic characteristics have been attained in rice via nuclear transformation. [42] Robust and reliable engineering for yield of RuBisCO and other enzymes in the C3 cycle was shown to be possible, [43] and it was first achieved in 2019 through a synthetic biology approach. [37]

One avenue is to introduce RuBisCO variants with naturally high specificity values such as the ones from the red alga Galdieria partita into plants. This may improve the photosynthetic efficiency of crop plants, although possible negative impacts have yet to be studied. [44] Advances in this area include the replacement of the tobacco enzyme with that of the purple photosynthetic bacterium Rhodospirillum rubrum . [45] In 2014, two transplastomic tobacco lines with functional RuBisCO from the cyanobacterium Synechococcus elongatus PCC7942 (Se7942) were created by replacing the RuBisCO with the large and small subunit genes of the Se7942 enzyme, in combination with either the corresponding Se7942 assembly chaperone, RbcX, or an internal carboxysomal protein, CcmM35. Both mutants had increased CO2 fixation rates when measured as carbon molecules per RuBisCO. However, the mutant plants grew more slowly than wild-type. [46]

A recent theory explores the trade-off between the relative specificity (i.e., ability to favour CO2 fixation over O2 incorporation, which leads to the energy-wasteful process of photorespiration) and the rate at which product is formed. The authors conclude that RuBisCO may actually have evolved to reach a point of 'near-perfection' in many plants (with widely varying substrate availabilities and environmental conditions), reaching a compromise between specificity and reaction rate. [47] It has been also suggested that the oxygenase reaction of RuBisCO prevents CO2 depletion near its active sites and provides the maintenance of the chloroplast redox state. [48]

Since photosynthesis is the single most effective natural regulator of carbon dioxide in the Earth's atmosphere, [49] a biochemical model of RuBisCO reaction is used as the core module of climate change models. Thus, a correct model of this reaction is essential to the basic understanding of the relations and interactions of environmental models.

Expression in bacterial hosts

There currently are very few effective methods for expressing functional plant Rubisco in bacterial hosts for genetic manipulation studies. This is largely due to Rubisco's requirement of complex cellular machinery for its biogenesis and metabolic maintenance including the nuclear-encoded RbcS subunits, which are typically imported into chloroplasts as unfolded proteins. [50] [51] Furthermore, sufficient expression and interaction with Rubisco activase are major challenges as well. [39] One successful method for expression of Rubisco in E. coli involves the co-expression of multiple chloroplast chaperones, though this has only been shown for Arabidopsis thaliana Rubisco. [52]

Depletion in proteomic studies

Due to its high abundance in plants (generally 40% of the total protein content), RuBisCO often impedes analysis of important signaling proteins such as transcription factors, kinases, and regulatory proteins found in lower abundance (10-100 molecules per cell) within plants. [53] For example, using mass spectrometry on plant protein mixtures would result in multiple intense RuBisCO subunit peaks that interfere and hide those of other proteins.

Recently, one efficient method for precipitating out RuBisCO involves the usage of protamine sulfate solution. [54] Other existing methods for depleting RuBisCO and studying lower abundance proteins include fractionation techniques with calcium and phytate, [55] gel electrophoresis with polyethylene glycol, [56] [57] affinity chromatography, [58] [59] and aggregation using DTT, [60] though these methods are more time-consuming and less efficient when compared to protamine sulfate precipitation. [53]

Evolution of RuBisCO

Phylogenetic studies

The chloroplast gene rbcL, which codes for the large subunit of RuBisCO has been widely used as an appropriate locus for analysis of phylogenetics in plant taxonomy. [61]

Origin

Non-carbon-fixing proteins similar to RuBisCO, termed RuBisCO-like proteins (RLPs), are also found in the wild in organisms as common as Bacillus subtilis . This bacterium has a rbcL-like protein with a 2,3-diketo-5-methylthiopentyl-1-phosphate enolase function, part of the methionine salvage pathway. [62] Later identifications found functionally divergent examples dispersed all over bacteria and archaea, as well as transitionary enzymes performing both RLP-type enolase and RuBisCO functions. It is now believed that the current RuBisCO evolved from a dimeric RLP ancestor, acquiring its carboxylase function first before further oligomerizing and then recruiting the small subunit to form the familiar modern enzyme. [15] The small subunit probably first evolved in anaerobic and thermophilic organisms, where it enabled RuBisCO to catalyze its reaction at higher temperatures. [63] In addition to its effect on stabilizing catalysis, it enabled the evolution of higher specificities for CO2 over O2 by modulating the effect that substitutions within RuBisCO have on enzymatic function. Substitutions that do not have an effect without the small subunit suddenly become beneficial when it is bound. Furthermore, the small subunit enabled the accumulation of substitutions that are only tolerated in its presence. Accumulation of such substitutions leads to a strict dependence on the small subunit, which is observed in extant Rubiscos that bind a small subunit.

C4

With the mass convergent evolution of the C4-fixation pathway in a diversity of plant lineages, ancestral C3-type RuBisCO evolved to have faster turnover of CO2 in exchange for lower specificity as a result of the greater localization of CO2 from the mesophyll cells into the bundle sheath cells. [64] This was achieved through enhancement of conformational flexibility of the “open-closed” transition in the Calvin cycle. Laboratory-based phylogenetic studies have shown that this evolution was constrained by the trade-off between stability and activity brought about by the series of necessary mutations for C4 RuBisCO. [65] Moreover, in order to sustain the destabilizing mutations, the evolution to C4 RuBisCO was preceded by a period in which mutations granted the enzyme increased stability, establishing a buffer to sustain and maintain the mutations required for C4 RuBisCO. To assist with this buffering process, the newly-evolved enzyme was found to have further developed a series of stabilizing mutations. While RuBisCO has always been accumulating new mutations, most of these mutations that have survived have not had significant effects on protein stability. The destabilizing C4 mutations on RuBisCO has been sustained by environmental pressures such as low CO2 concentrations, requiring a sacrifice of stability for new adaptive functions. [65]

History of the term

The term "RuBisCO" was coined humorously in 1979, by David Eisenberg at a seminar honouring the retirement of the early, prominent RuBisCO researcher, Sam Wildman, and also alluded to the snack food trade name "Nabisco" in reference to Wildman's attempts to create an edible protein supplement from tobacco leaves. [66] [67]

The capitalization of the name has been long debated. It can be capitalized for each letter of the full name (Ribulose-1,5 bisphosphate carboxylase/oxygenase), but it has also been argued that is should all be in lower case (rubisco), similar to other terms like scuba or laser. [1]

See also

Related Research Articles

<span class="mw-page-title-main">Photosynthesis</span> Biological process to convert light into chemical energy

Photosynthesis is a system of biological processes by which photosynthetic organisms, such as most plants, algae, and cyanobacteria, convert light energy, typically from sunlight, into the chemical energy necessary to fuel their metabolism. Photosynthesis usually refers to oxygenic photosynthesis, a process that produces oxygen.
Photosynthetic organisms store the chemical energy so produced within intracellular organic compounds like sugars, glycogen, cellulose and starches. To use this stored chemical energy, an organism's cells metabolize the organic compounds through cellular respiration. Photosynthesis plays a critical role in producing and maintaining the oxygen content of the Earth's atmosphere, and it supplies most of the biological energy necessary for complex life on Earth.

<span class="mw-page-title-main">Pyrenoid</span> Organelle found within the chloroplasts of algae and hornworts

Pyrenoids are sub-cellular micro-compartments found in chloroplasts of many algae, and in a single group of land plants, the hornworts. Pyrenoids are associated with the operation of a carbon-concentrating mechanism (CCM). Their main function is to act as centres of carbon dioxide (CO2) fixation, by generating and maintaining a CO2 rich environment around the photosynthetic enzyme ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO). Pyrenoids therefore seem to have a role analogous to that of carboxysomes in cyanobacteria.

C<sub>4</sub> carbon fixation Photosynthetic process in some plants

C4 carbon fixation or the Hatch–Slack pathway is one of three known photosynthetic processes of carbon fixation in plants. It owes the names to the 1960s discovery by Marshall Davidson Hatch and Charles Roger Slack.

<span class="mw-page-title-main">Photorespiration</span> Process in plant metabolism

Photorespiration (also known as the oxidative photosynthetic carbon cycle or C2 cycle) refers to a process in plant metabolism where the enzyme RuBisCO oxygenates RuBP, wasting some of the energy produced by photosynthesis. The desired reaction is the addition of carbon dioxide to RuBP (carboxylation), a key step in the Calvin–Benson cycle, but approximately 25% of reactions by RuBisCO instead add oxygen to RuBP (oxygenation), creating a product that cannot be used within the Calvin–Benson cycle. This process lowers the efficiency of photosynthesis, potentially lowering photosynthetic output by 25% in C3 plants. Photorespiration involves a complex network of enzyme reactions that exchange metabolites between chloroplasts, leaf peroxisomes and mitochondria.

<span class="mw-page-title-main">Ribulose 1,5-bisphosphate</span> Chemical compound

Ribulose 1,5-bisphosphate (RuBP) is an organic substance that is involved in photosynthesis, notably as the principal CO2 acceptor in plants. It is a colourless anion, a double phosphate ester of the ketopentose called ribulose. Salts of RuBP can be isolated, but its crucial biological function happens in solution. RuBP occurs not only in plants but in all domains of life, including Archaea, Bacteria, and Eukarya.

C<sub>3</sub> carbon fixation Series of interconnected biochemical reactions

C3 carbon fixation is the most common of three metabolic pathways for carbon fixation in photosynthesis, the other two being C4 and CAM. This process converts carbon dioxide and ribulose bisphosphate (RuBP, a 5-carbon sugar) into two molecules of 3-phosphoglycerate through the following reaction:

<span class="mw-page-title-main">Calvin cycle</span> Light-independent reactions in photosynthesis

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 glucose. The Calvin cycle is present in all photosynthetic eukaryotes and also many photosynthetic bacteria. In plants, these reactions occur in the stroma, the fluid-filled region of a chloroplast outside the thylakoid membranes. These reactions take the products of light-dependent reactions and perform further chemical processes on them. The Calvin cycle uses the chemical energy of ATP and reducing power of NADPH from the light dependent reactions to produce sugars for the plant to use. These substrates are used in a series of reduction-oxidation (redox) reactions to produce sugars in a step-wise process; there is no direct reaction that converts several molecules of CO2 to a sugar. There are three phases to the light-independent reactions, collectively called the Calvin cycle: carboxylation, reduction reactions, and ribulose 1,5-bisphosphate (RuBP) regeneration.

Methylotrophs are a diverse group of microorganisms that can use reduced one-carbon compounds, such as methanol or methane, as the carbon source for their growth; and multi-carbon compounds that contain no carbon-carbon bonds, such as dimethyl ether and dimethylamine. This group of microorganisms also includes those capable of assimilating reduced one-carbon compounds by way of carbon dioxide using the ribulose bisphosphate pathway. These organisms should not be confused with methanogens which on the contrary produce methane as a by-product from various one-carbon compounds such as carbon dioxide. Some methylotrophs can degrade the greenhouse gas methane, and in this case they are called methanotrophs. The abundance, purity, and low price of methanol compared to commonly used sugars make methylotrophs competent organisms for production of amino acids, vitamins, recombinant proteins, single-cell proteins, co-enzymes and cytochromes.

<span class="mw-page-title-main">Carboxysome</span> Bacterial microcompartment containing the enzyme RuBisCo

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.

<span class="mw-page-title-main">Phosphoenolpyruvate carboxylase</span> Class of enzymes

Phosphoenolpyruvate carboxylase (also known as PEP carboxylase, PEPCase, or PEPC; EC 4.1.1.31, PDB ID: 3ZGE) is an enzyme in the family of carboxy-lyases found in plants and some bacteria that catalyzes the addition of bicarbonate (HCO3−) to phosphoenolpyruvate (PEP) to form the four-carbon compound oxaloacetate and inorganic phosphate:

Carboxylation is a chemical reaction in which a carboxylic acid is produced by treating a substrate with carbon dioxide. The opposite reaction is decarboxylation. In chemistry, the term carbonation is sometimes used synonymously with carboxylation, especially when applied to the reaction of carbanionic reagents with CO2. More generally, carbonation usually describes the production of carbonates.

In enzymology, a [ribulose-bisphosphate carboxylase]-lysine N-methyltransferase (EC 2.1.1.127) is an enzyme that catalyzes the chemical reaction

<span class="mw-page-title-main">Phosphoribulokinase</span>

Phosphoribulokinase (PRK) (EC 2.7.1.19) is an essential photosynthetic enzyme that catalyzes the ATP-dependent phosphorylation of ribulose 5-phosphate (RuP) into ribulose 1,5-bisphosphate (RuBP), both intermediates in the Calvin Cycle. Its main function is to regenerate RuBP, which is the initial substrate and CO2-acceptor molecule of the Calvin Cycle. PRK belongs to the family of transferase enzymes, specifically those transferring phosphorus-containing groups (phosphotransferases) to an alcohol group acceptor. Along with ribulose 1,5-bisphosphate carboxylase/oxygenase (RuBisCo), phosphoribulokinase is unique to the Calvin Cycle. Therefore, PRK activity often determines the metabolic rate in organisms for which carbon fixation is key to survival. Much initial work on PRK was done with spinach leaf extracts in the 1950s; subsequent studies of PRK in other photosynthetic prokaryotic and eukaryotic organisms have followed. The possibility that PRK might exist was first recognized by Weissbach et al. in 1954; for example, the group noted that carbon dioxide fixation in crude spinach extracts was enhanced by the addition of ATP. The first purification of PRK was conducted by Hurwitz and colleagues in 1956.

ATP + Mg2+ - D-ribulose 5-phosphate  ADP + D-ribulose 1,5-bisphosphate
<i>Vaucheria litorea</i> Species of alga

Vaucheria litorea is a species of yellow-green algae (Xanthophyceae). It grows in a filamentous fashion. V. litorea is a common intertidal species of coastal brackish waters and salt marshes of the Northern Atlantic, along the coasts of Europe, North America and New Zealand. It is also found in the Eastern Pacific coasts of Washington state. It is found to be able to tolerate a large range of salinities, making it euryhaline.

[Fructose-bisphosphate aldolase]-lysine N-methyltransferase is an enzyme that catalyses the following chemical reaction:

2-Carboxy-<small>D</small>-arabitinol 1-phosphate Chemical compound

2-Carboxy-D-arabitinol 1-phosphate is a molecule produced in plants that inhibits RuBisCO, a key enzyme in the Calvin cycle and carbon fixation. In dark conditions, this molecule binds to RuBisCO, preventing it from participating in chemical reactions. As the amount of light present increases, CA1P levels decrease, freeing RuBisCO's reactive ends, allowing more of the molecules to participate in chemical reactions. It can be broken down by the enzyme 2-carboxy-D-arabinitol-1-phosphatase into 2-carboxy-D-arabinitol.

<span class="mw-page-title-main">Fractionation of carbon isotopes in oxygenic photosynthesis</span>

Photosynthesis converts carbon dioxide to carbohydrates via several metabolic pathways that provide energy to an organism and preferentially react with certain stable isotopes of carbon. The selective enrichment of one stable isotope over another creates distinct isotopic fractionations that can be measured and correlated among oxygenic phototrophs. The degree of carbon isotope fractionation is influenced by several factors, including the metabolism, anatomy, growth rate, and environmental conditions of the organism. Understanding these variations in carbon fractionation across species is useful for biogeochemical studies, including the reconstruction of paleoecology, plant evolution, and the characterization of food chains.

<span class="mw-page-title-main">Kinetic isotope effects of RuBisCO</span>

The kinetic isotope effect (KIE) of ribulose-1,5-bisphosphate carboxylase oxygenase (RuBisCO) is the isotopic fractionation associated solely with the step in the Calvin-Benson cycle where a molecule of carbon dioxide is attached to the 5-carbon sugar ribulose-1,5-bisphosphate (RuBP) to produce two 3-carbon sugars called 3-phosphoglycerate. This chemical reaction is catalyzed by the enzyme RuBisCO, and this enzyme-catalyzed reaction creates the primary kinetic isotope effect of photosynthesis. It is also largely responsible for the isotopic compositions of photosynthetic organisms and the heterotrophs that eat them. Understanding the intrinsic KIE of RuBisCO is of interest to earth scientists, botanists, and ecologists because this isotopic biosignature can be used to reconstruct the evolution of photosynthesis and the rise of oxygen in the geologic record, reconstruct past evolutionary relationships and environmental conditions, and infer plant relationships and productivity in modern environments.

<span class="mw-page-title-main">Anthony Cashmore</span> New Zealand molecular biologist

Anthony R. Cashmore is a biochemist and plant molecular biologist, best known for identifying cryptochrome photoreceptor proteins. These specialized proteins are critical for plant development and play an essential role in circadian rhythms of plants and animals. A Professor emeritus in the Department of Biology at the University of Pennsylvania, Cashmore led the Plant Science Institute from the time of his appointment in 1986 until his retirement in 2011. He was elected to the National Academy of Sciences in 2003.

<span class="mw-page-title-main">2-Phosphoglycolate</span> Chemical compound

2-Phosphoglycolate (chemical formula C2H2O6P3-; also known as phosphoglycolate, 2-PG, or PG) is a natural metabolic product of the oxygenase reaction mediated by the enzyme ribulose 1,5-bisphosphate carboxylase (RuBisCo).

References

  1. ↑ The structure of RuBisCO from the photosynthetic bacterium Rhodospirillum rubrum has been determined by X-ray crystallography, see: PDB: 9RUB ​. A comparison of the structures of eukaryotic and bacterial RuBisCO is shown in the Protein Data Bank "Molecule of the Month" #11. [11]
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  67. ↑ Portis AR, Parry MA (October 2007). "Discoveries in Rubisco (Ribulose 1,5-bisphosphate carboxylase/oxygenase): a historical perspective". Photosynthesis Research. 94 (1): 121–143. Bibcode:2007PhoRe..94..121P. doi:10.1007/s11120-007-9225-6. PMID   17665149. S2CID   39767233.
Figure 3. In this figure, each protein chain in the (LS)2 complex is given its own color for easy identification. RuBisCOL2S2.png
Figure 3. In this figure, each protein chain in the (LS)2 complex is given its own color for easy identification.

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