The Mechanism of Rubisco Catalyzed Carboxylation Reaction: Chemical Aspects Involving Acid-Base Chemistry and Functioning of the Molecular Machine

Immacolata C Tommasi

doi:10.3390/catal11070813

Abstract

In recent years, a great deal of attention has been paid by the scientific community to improving the efficiency of photosynthetic carbon assimilation, plant growth and biomass production in order to achieve a higher crop productivity. Therefore, the primary carboxylase enzyme of the photosynthetic process Rubisco has received considerable attention focused on many aspects of the enzyme function including protein structure, protein engineering and assembly, enzyme activation and kinetics. Based on its fundamental role in carbon assimilation Rubisco is also targeted by the CO2-fertilization effect, which is the increased rate of photosynthesis due to increasing atmospheric CO2-concentration. The aim of this review is to provide a framework, as complete as possible, of the mechanism of the RuBP carboxylation/hydration reaction including description of chemical events occurring at the enzyme “activating” and “catalytic” sites (which involve Broensted acid-base reactions) and the functioning of the complex molecular machine. Important research results achieved over the last few years providing substantial advancement in understanding the enzyme functioning will be discussed.

Highlights

The increased amount of anthropogenic CO2 emissions since the beginning of the industrial era has significantly affected the natural biogeochemical carbon cycle
An analysis of the components of the anthropogenic “CO2 budget”, as defined in Reports released by the Intergovernmental Panel on Climate Change (IPCC) [1] and the Global Carbon Budget Project [2] (GCB Project, Table S1), show that, since 1750, global CO2-emissions amounted to about 700 GtC compared to 400 GtC fixed by CO2-natural sinks (Table S1)
Estimates of carbon fluxes between different compartments of terrestrial ecosystems (Figure S1, Table S2, Supplementary Materials) evidence that, during the last six decades, oceans and land have adapted to such “CO2 pressure”, increasing CO2 natural sink [2].There is a consensus that terrestrial carbon sink (SLAND, see Section S1) has constantly increased in the Northern Hemisphere largely due to the “CO2-fertilization effect”

Summary

Introduction

The increased amount of anthropogenic CO2 emissions since the beginning of the industrial era (starting around 1750) has significantly affected the natural biogeochemical carbon cycle. The carboxylase activity of the enzyme (Scheme 1a) allows for CO2 fixation in photosynthetic organisms by converting D-ribulose-1,5-bisphosphate (RuBP) into two molecules of 3-phospho-D-glycerate (3PGA). Stec [15] proposes that the two gaseous molecules “bind” to the same region of the active site, at the mouth of the TIM barrel, covered as a lid by the N-terminal domain of the adjacent L subunit (see Figure 3), where a high electrostatic field gradient is set up by the closeness of negative and positive surfaces potential. Crystal structures assigned the PBD ID5MAC, 1BXN and 4FOK are related to G-II, G-IC and GID Rubisco respectively, and belong to proteins progressively adapted to increasing O2 concentration Comparison of these crystal structures evidenced the presence of higher surface charge potential proximal to the active site and solvent accessible channels connecting the protein surface to the active site. Increasing extension of the positive charged areas within the three proteins parallels increased SC/O selectivity

Structure of the Rubisco “Catalytic Active Site”

Mechanism of the Rubisco Carboxylation Reaction

Rubisco Kinetics

10. Photorespiration

Findings

11. Conclusions