Revisiting tradeoffs in Rubisco kinetic parameters

Abstract

Rubisco is the primary carboxylase of the Calvin cycle, the most abundant enzyme in the biosphere, and one of the best-characterized enzymes. Based on correlations between Rubisco kinetic parameters, it is widely posited that constraints embedded in the catalytic mechanism enforce tradeoffs between CO 2 -specificity, S C/O , and maximum carboxylation rate, k cat,C .However, the reasoning that established this view was based on data from ≈20 organisms.Here, we re-examine models of tradeoffs in Rubisco catalysis using a dataset from ≈300 organisms. Correlations between kinetic parameters are substantially attenuated in this larger dataset, with the inverse relationship between k cat,C and S C/O being a key example. Nonetheless, measured kinetic parameters display extremely limited variation, consistent with a view of Rubisco as a highly-constrained enzyme. More than 95% of k cat,C values are between 1 and 10 s -1 and no measured k cat,C exceeds 15 s -1 . Similarly, S C/O varies by only 30% among Form I Rubiscos and < 10% among C 3 plant enzymes. Limited variation in S C/O forces a strong positive correlation between the catalytic efficiencies (k cat /K M ) for carboxylation and oxygenation, consistent with a model of Rubisco catalysis in which increasing the rate of CO 2 addition to the enzyme-substrate complex requires an equal increase to the O 2 addition rate. Altogether, these data suggest that Rubisco evolution is tightly constrained by the physicochemical limits of CO 2 /O 2 discrimination. * !,! − * !,! and so changes to the conformation of the RuBP enediolate might explain characteristic differences between S C/O of C 3 plant and cyanobacterial Rubiscos. 5,8 See SI for a derivation of this model and further discussion of its implications.

Response: Commentary: Directions for Optimization of Photosynthetic Carbon Fixation: RuBisCO’s Efficiency May Not Be So Constrained After All

“…Moreover, it appears that higher plants are not so constrained, as the trade-off is not clearly evident from a much broader sample ( Figure 1 ). This conclusion is supported more broadly by a comprehensive statistical analysis of all the kinetic data (Flamholz et al, 2018, Flamholz et al, 2019). However, there are currently insufficient data for all non-plant Rubiscos to be able to judge whether these findings can be generalized.…”

The global mass and average rate of rubisco

“…Thus, the effective catalytic rate of Rubisco in wild terrestrial environments is ≈1% of its maximal rate. The characteristic k cat of marine autotrophs is not significantly different from that of terrestrial plants, even though that of cyanobacterial Rubisco is usually faster ( 42 ), and we estimate it at ≈4 s −1 ( https://bit.ly/2CNq6j2 ). As such, the effective catalytic rate of Rubisco in the marine environment is ≈15% of its maximal rate at 25 °C.…”

“…How does this rate compare with the maximal catalytic rate of Rubisco in plants? Using a collection of kinetic parameters of Rubiscos ( 42 ), we estimate the characteristic k cat of terrestrial plants is ≈3 s −1 at 25 °C ( https://bit.ly/2CNq6j2 ). Thus, the effective catalytic rate of Rubisco in wild terrestrial environments is ≈1% of its maximal rate.…”

Phosphoglycolate salvage in a chemolithoautotroph using the Calvin cycle

“…GSE141999 ) ( 58 ) and are available in Dataset S1 . Bioinformatic genome analysis of Rubisco and malate synthase are available in Dataset S2 and at GitHub ( https://github.com/flamholz/malate_synthase/tree/master/pipeline ) ( 59 ).…”