A Theoretical Study of the Molecular Mechanism for the Carboxylation Chemistry in Rubisco

Abstract

Stereochemical and structural aspects for the carbon dioxide fixation followed by hydration of d-ribulose 1,5-bisphosphate catalyzed by Rubisco are analyzed by using two model substrates, hydroxypropanone and 3,4-dihydroxy-2-pentanone. The molecular mechanisms for the carboxylation, C3-hydration and C2-inversion processes, are theoretically characterized and discussed with saddle points of index 1 representing transition structures (TS) and relevant (molded) intermediates mirroring the experimentally proposed mechanism. Ab initio SCF MO calculations at 3-21G and 6-31G** basis set levels of theory were used, while the correlation energy is included at the MP2/6-31G** level. The mapping starts from TS1, the carboxylation transition structure, which describes now the coupling of the carbon dioxide attack to the substrate C2-center in its dienol form with a synchronous interconversion of the C3 hydroxyl into a ketone group. Thereafter, water addition leads to a gem-diol followed by another step of intramolecular hydrogen transfer coupled with the C2−C3 bond breaking process. This TS breaks into one model of 3-d-phosphoglycerate product and an intermediate. The configuration inversion at the C2-center is found to be possible via intramolecular hydrogen transfer, as suggested by the corresponding TS relating the intermediate to the C2-inverted conformation. The complete set of steps found gives a self-contained description of the carboxylation followed by hydrolysis with proper stereochemistry. Comparisons between the transition state analogue: 2-carboxy-d-arabinitol-1,5-bisphosphate and TS1 show that both structures can be superposed with minimal root-mean-square deviation for C-atoms. All other calculated stationary TSs share the gross conformational features of TS1, and consequently, all molecular rearrangements detected in a vacuum can be accommodated without constraints into the active site of Rubisco. Transition structures invariances with respect to level of theory and molecular models are discussed.