A short history of RubisCO: the rise and fall (?) of Nature's predominant CO2 fixing enzyme

Abstract

Ribulose-1,5-bisphosphate carboxylase/oxygenase (RubisCO) is arguably one of the most abundant proteins in the biosphere and a key enzyme in the global carbon cycle. Although RubisCO has been intensively studied, its evolutionary origins and rise as Nature's most dominant carbon dioxide (CO₂)-fixing enzyme still remain in the dark. In this review we will bring together biochemical, structural, physiological, microbiological, as well as phylogenetic data to speculate on the evolutionary roots of the CO₂-fixation reaction of RubisCO, the emergence of RubisCO-based autotrophic CO₂-fixation in the context of the Calvin-Benson-Bassham cycle, and the further evolution of RubisCO into the 'RubisCOsome', a complex of various proteins assembling and interacting with the enzyme to improve its operational capacity (functionality) under different biological and environmental conditions.

Graphical abstract

Figure 1. Evolution of the carboxylation function in the RLP/RubisCO superfamily of enzymes.

The left panel shows a phylogenetic tree of the RLP/RubisCO superfamily, with RubisCOs depicted in red and RLPs of the 1,3-isomerase and tautomerase family shown in blue. The different reaction mechanisms postulated for these enzymes are shown on the right panel. All reactions proceed through a central enolate intermediate that is formed by the initial abstraction of a proton from the respective substrate (highlighted in green). Compared to RubisCO, the reactions of the 1,3-isomerase and tautomerase are mechanistically simpler, indicating that the more complex CO₂-fixing reaction of RubisCO emerged in the scaffold of a RLP ancestor. The phylogenetic tree was adapted with changes from Schada et al. [26]. Ribulose-1,5-bisphosphate (Ru-1,5-BP), methylthioribulose-1-phosphate (MT-Ru-1P), methylthioribulose-5-phosphate (MT-Ru-5P), methylthioxylulose-5-phosphate (MT-Xu-5P), 2,3-diketo methylthiopentyl-1-phsphate (DK-MT-pentyl-1P), 2-hydroxy-3-keto-5-methylthiopentenyl-1-phosphate (HK-MT-pentenyl-1P).

Figure 2. Hypothetical timeline of the emergence and evolution of RubisCO.

The figure summarizes the individual events in the emergence of RubisCO from a non-CO₂-fixing ancestor to complex, modern-day RubisCO (Form I) which operates in chloroplasts and cyanobacterial carboxysomes. The postulated events are based on the main steps during evolution that are discussed in the main text. Note that timeline is only relative and that the order of some of the events might differ, which is highlighted by a question mark.