Revisiting Trade-offs between Rubisco Kinetic Parameters

Rubisco is the primary carboxylase of the Calvin cycle, the most abundant enzyme in the biosphere, and one of the best-characterized enzymes. On the basis of correlations between Rubisco kinetic parameters, it is widely posited that constraints embedded in the catalytic mechanism enforce trade-offs between CO2 specificity, S-C/O, and maximum carboxylation rate, k(cat,C). However, the reasoning that established this view was based on data from approximate to 20 organisms. Here, we re-examine models of trade-offs in Rubisco catalysis using a data set from approximate to 300 organisms. Correlations between kinetic parameters are substantially attenuated in this larger data set, 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 addition of CO2, to the enzyme-substrate complex requires an equal increase in the O-2 addition rate. Altogether, these data suggest that Rubisco evolution is tightly constrained by the physicochemical limits of CO2/O-2 discrimination.