Experimental evidence for extra proton exchange in ribulose 1,5-bisphosphate carboxylase/oxygenase catalysis

Commun Integr Biol. 2022 Feb 15;15(1):68-74. doi: 10.1080/19420889.2022.2039431. eCollection 2022.

Abstract

Despite considerable advances in the past 50 y, the mechanism of ribulose 1,5-bisphosphate carboxylase/oxygenase (Rubisco) catalysis is still not well understood. In particular, the movement and exchange of protons within the active site is not well documented: typically, kinetics of H exchange during the first steps of catalysis, i.e. abstraction of the H3 atom of ribulose 1,5-bisphosphate (RuBP) and enolization, are not clearly established. Here, we took advantage of reaction assays run in heavy water (2H2O) to monitor the appearance of deuterated RuBP and deuterated products (3-phosphoglycerate and 2-phosphoglycolate) with exact mass LC-MS. Enolization was reversible such that de-enolization generated not only monodeuterated RuBP (2H-[H-3]-ribulose 1,5-bisphosphate) but also dideuterated RuBP (2H2-[H-3,O-3]-ribulose 1,5-bisphosphate). Carboxylation yielded about one half deuterated 3-phosphoglycerate (2H-[H-2]-3-phosphoglycerate) and also a small proportion of dideuterated 3-phosphoglycerate (2H2-[H-2,O-2]-3-phosphoglycerate). Oxygenation generated a small amount of monodeuterated, but no dideuterated, products. (Di)deuterated isotopologue abundance depended negatively on gas concentration. We conclude that in addition to the first step of proton exchange at H3 occurring before gas addition (and thus influenced by the competition between de-enolization and gas addition), there is another proton exchange step between solvent water, active site residues, and the 2,3-enediol(ate) leading to deuterated OH groups in products.

Keywords: Rubisco; carboxylation; catalysis; isotope; kinetics; oxygenation.

Grants and funding

This work was supported by the Conseil Régional des Pays de la Loire [Connect Talent Isoseed].