Evolutionary trends in RuBisCO kinetics and their co‐evolution with CO₂ concentrating mechanisms

Abstract

Summary RuBisCO‐catalyzed CO2 fixation is the main source of organic carbon in the biosphere. This enzyme is present in all domains of life in different forms (III, II, and I) and its origin goes back to 3500 Mya, when the atmosphere was anoxygenic. However, the RuBisCO active site also catalyzes oxygenation of ribulose 1,5‐bisphosphate, therefore, the development of oxygenic photosynthesis and the subsequent oxygen‐rich atmosphere promoted the appearance of CO2 concentrating mechanisms (CCMs) and/or the evolution of a more CO2‐specific RuBisCO enzyme. The wide variability in RuBisCO kinetic traits of extant organisms reveals a history of adaptation to the prevailing CO2/O2 concentrations and the thermal environment throughout evolution. Notable differences in the kinetic parameters are found among the different forms of RuBisCO, but the differences are also associated with the presence and type of CCMs within each form, indicative of co‐evolution of RuBisCO and CCMs. Trade‐offs between RuBisCO kinetic traits vary among the RuBisCO forms and also among phylogenetic groups within the same form. These results suggest that different biochemical and structural constraints have operated on each type of RuBisCO during evolution, probably reflecting different environmental selective pressures. In a similar way, variations in carbon isotopic fractionation of the enzyme point to significant differences in its relationship to the CO2 specificity among different RuBisCO forms. A deeper knowledge of the natural variability of RuBisCO catalytic traits and the chemical mechanism of RuBisCO carboxylation and oxygenation reactions raises the possibility of finding unrevealed landscapes in RuBisCO evolution.

Photosynthesis and photosynthetic efficiencies along the terrestrial plant’s phylogeny: lessons for improving crop photosynthesis

“…Additionally, it is likely that some facilitating biochemical elements are also involved in the dynamic regulation of g m , including some aquaporins (Hanba et al, 2004;Flexas et al, 2006Flexas et al, , 2008 and carbonic anhydrases (Momayyezi and Guy, 2017;Guy et al, 2019). Finally, although the different components of photosynthetic photochemistry and biochemistry are sufficiently well known, their complexityinvolving many electron transporters, redox molecules, and soluble enzymes, among other biochemical factors (Anderson, 1975), together with the fact that they are regulate at the transcription and post-transcriptional levels by both nuclear and chloroplastic genes (Fankhausen and Aubry, 2017;Wang et al, 2017;Galm es et al, 2019) overall severely restricts easy manipulation to achieve photosynthetic improvements, although a few successful attempts have been reported (Lefebvre et al, 2005;Raines, 2011;Driever et al, 2017;Simkin et al, 2019).…”

Recent Advances in Developing Artificial Autotrophic Microorganism for Reinforcing CO2 Fixation

“…Rubisco is a well-studied enzyme in photosynthetic organism since it provides organic carbon for life (Iniguez et al, 2020). Crystal structures of Rubisco from several origins have been analyzed by X-ray, including Rhodospirillum rubrum, Synechococcus PCC6301, Chlorobium tepidum, Thermococcus kodakaraensis KOD1, and so on (Iniguez et al, 2020). Two forms of Rubisco participate in the CBB cycle.…”

“…As the key enzyme in the CBB cycle, Rubisco is the most abundant protein in the biosphere, which fixes ∼10 11 tons of CO 2 from the atmosphere per year ( Hayer-Hartl and Hartl, 2020 ). Rubisco is a well-studied enzyme in photosynthetic organism since it provides organic carbon for life ( Iniguez et al, 2020 ). Crystal structures of Rubisco from several origins have been analyzed by X-ray, including Rhodospirillum rubrum , Synechococcus PCC6301, Chlorobium tepidum , Thermococcus kodakaraensis KOD1, and so on ( Iniguez et al, 2020 ).…”

Rubisco adaptation is more limited by phylogenetic constraint than by catalytic trade-off

“…This is because prior analyses which did not account for the evolutionary relationships among (and non-independence of) species may have suffered from over-estimated correlation coefficients as a consequence of the phylogenetic co-variation which is observed in kinetic traits (Figure 3A). In order to evaluate the severity by which phylogenetic co-variation may have influenced previous results (Tcherkez, Farquhar and Andrews, 2006; Savir et al , 2010; Flamholz et al , 2019; Iñiguez et al , 2020), the correlations observed in the kinetic trait data using both phylogenetic and non-phylogenetic regression methods were compared (Figure 3B and 3C).…”