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, SC/O, and maximum carboxylation rate, kcat,C. However, the reasoning that established this view
was based on data from ≈20 organisms. Here, we re-examine models
of trade-offs in Rubisco catalysis using a data set from ≈300
organisms. Correlations between kinetic parameters are substantially
attenuated in this larger data set, with the inverse relationship
between kcat,C and SC/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 kcat,C values are between 1 and 10 s–1, and no measured kcat,C exceeds 15 s–1. Similarly, SC/O varies
by only 30% among Form I Rubiscos and <10% among C3 plant
enzymes. Limited variation in SC/O forces
a strong positive correlation between the catalytic efficiencies (kcat/KM) 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 O2 addition rate.
Altogether, these data suggest that Rubisco evolution is tightly constrained
by the physicochemical limits of CO2/O2 discrimination.