Diffusion and interactions of carbon dioxide and oxygen in the vicinity of the active site of Rubisco: Molecular dynamics and quantum chemical studies

Abstract

Molecular dynamics (MD) at the molecular mechanical level and geometry optimisation at the quantum mechanical level have been performed to investigate the transport and fixation of oxygen and carbon dioxide in the cavity of ribulose-1,5-bisphosphate carboxylase/oxygenase, or Rubisco. Multiple MD simulations have been carried out to study the diffusive behaviour of O(2) and CO(2) molecules from the Mg(2+) cation in Rubisco at 298 K and 1 bar, being one step in the overall process of carboxylation/oxygenation in Rubisco. In addition to this work, in order to gain additional perspective on the role of chemical reaction rates and thermodynamics, oxygen, and carbon dioxide uptake mechanisms have also been investigated by the aid of quantum chemical calculations. The results indicate that the activation barrier for carboxylation is slightly lower than that of oxygenation. This agrees qualitatively with experimental findings, and rationalises the observed competition between both catalytic processes in nature. Finally, the longer-lived persistence of CO(2) in the vicinity of the active centre (i.e., slower self-diffusion) may serve to explain, in part, why carboxylation is the more kinetically favoured on an overall basis compared to oxygenation.

The mechanism of Rubisco‐catalysed oxygenation

“…Other quantum chemical calculations have also suggested that carboxylation is favoured over oxygenation because of a slower internal self‐diffusion for CO 2 (higher residence time within the active site) than for O 2 (El‐Hendawy et al . ). Henry's law and solubility data also indicate that CO 2 is up to 850 times more soluble in a proteinaceous medium than in water (reviewed in Tcherkez ) while O 2 is less soluble in a proteinaceous medium or a protein aqueous solution.…”

Possible Steps of the Carboxylation of Ribulose-1,5-biphosphate from Intermediates: 2,3-Enediol versus 1,2-Enol

“…In the case of the attachment of CO 2 to enediolate, an intermediate 6-carbon compound is formed, which is named 3-keto-2-carboxy- d -arabinitol 1,5-bisphosphate (3kCABP). In the literature, one can find a number of works devoted to the modeling of the steps of the carboxylation of RuBP by quantum–chemical methods [ 7 , 8 , 9 , 10 ], as well as a combination of quantum–chemical and molecular modeling methods [ 11 , 12 , 13 , 14 ]. When modeling the RuBP enolization reaction, some authors consider the reaction product to be the 2,3-enediol compound [ 11 ] or its deprotonated form, 2,3-enediolate [ 7 , 8 , 9 , 10 , 11 , 12 , 13 , 14 ].…”

“…In the literature, one can find a number of works devoted to the modeling of the steps of the carboxylation of RuBP by quantum–chemical methods [ 7 , 8 , 9 , 10 ], as well as a combination of quantum–chemical and molecular modeling methods [ 11 , 12 , 13 , 14 ]. When modeling the RuBP enolization reaction, some authors consider the reaction product to be the 2,3-enediol compound [ 11 ] or its deprotonated form, 2,3-enediolate [ 7 , 8 , 9 , 10 , 11 , 12 , 13 , 14 ]. In this study, we assume that 1,2-enol or its deprotonated form can be formed during the enolization step.…”

“…To determine the kinetics, most authors use an enzyme model in which the 2,3-enediolate forms a complex with the magnesium ion Mg 2+ . In previous studies [ 7 , 8 , 9 , 12 , 13 ] it was shown that the formation of 3kCABP is energetically favorable; when the 2,3-enediolate interacts with the CO 2 molecule the equilibrium shifts towards the reaction products. Kannappan and Grady point out that Rubisco is a very ineffective enzyme with a low catalytic rate of CO 2 fixation [ 7 ].…”

Quantum chemical investigation of thermochemistry in Calvin cycle

“…The first step is the fixation of CO 2 from inorganic forms such as the solvated CO 2 molecule and the bicarbonate and carbonate ions to organic molecule such as Ribulose-1,5-bisphosphate (RuBP) in presence of enzyme RuBisco, thereby generating 3-Phosphoglyceraldehyde (3-PG). The mechanism of CO 2 fixation, that is, the conversion of RuBP to 3-PG, was studied in detail by English et al 2 In the second step, ATP and * For correspondence NADPH reduce 3-PG into Glyceraldehyde-3-phosphate (G3P). Simultaneously, ATP converts into ADP and NADPH into NADP + .…”