Revisiting Trade-offs between Rubisco Kinetic Parameters
This article has been Reviewed by the following groups
Listed in
- Evaluated articles (PREreview)
Abstract
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.
Article activity feed
-
-
This Zenodo record is a permanently preserved version of a PREreview. You can view the complete PREreview at https://prereview.org/reviews/7624527.
UIUC Plant Physiology JC (2018/12/3): Revisiting tradeoffs in Rubisco kinetic parameters
The preprint "Revisiting tradeoffs in Rubisco kinetic parameters" by Flamholz et al. 2018 (https://doi.org/10.1101/470021) investigates the tradeoffs between catalytic efficiency and rate, of the central enzyme in carbon fixation, Ribulose-1,6-bisphosphate Carboxylase/Oxygenase (RuBisCO), using kinetic modeling based on biochemical data. The manuscript builds on previous work from the group (Savir et al. 2010; doi: 10.1073/pnas.0911663107), including an expanded dataset of kinetic parameters of ~250 RuBisCOs from 286 different species extracted from the literature. We thought it was an important …
This Zenodo record is a permanently preserved version of a PREreview. You can view the complete PREreview at https://prereview.org/reviews/7624527.
UIUC Plant Physiology JC (2018/12/3): Revisiting tradeoffs in Rubisco kinetic parameters
The preprint "Revisiting tradeoffs in Rubisco kinetic parameters" by Flamholz et al. 2018 (https://doi.org/10.1101/470021) investigates the tradeoffs between catalytic efficiency and rate, of the central enzyme in carbon fixation, Ribulose-1,6-bisphosphate Carboxylase/Oxygenase (RuBisCO), using kinetic modeling based on biochemical data. The manuscript builds on previous work from the group (Savir et al. 2010; doi: 10.1073/pnas.0911663107), including an expanded dataset of kinetic parameters of ~250 RuBisCOs from 286 different species extracted from the literature. We thought it was an important topic with potential interest for a wide range of researchers working on photosynthesis and evolution.
The main questions the paper seeks to address are:
- Which trade-offs are inherent in Rubisco kinetics.
- Has evolution resulted in optimal kinetics within the constraints of those inherent trade-offs.
The preprint challenges the theory that increasing RuBisCO activity reduces enzyme specificity as described by Tcherkez et al. (2006), which was based on a model of enzyme activity the discriminates between CO2 and O2 in a transition state. Data supporting this theory has been reported widely in the literature. However, the authors propose that there is little/no correlation between specificity and activity, and most previously-found correlations (KcatC and SC/O etc) are smaller for the new dataset, except for KcatC/KC and KcatO/KO.
We really enjoyed reading the manuscript and as it challenged our preconceptions about RuBisCO activity. We found it interesting (and surprising!) that the data contradicts a well-established theory, and it increased our awareness out current models of enzyme activity. We also thought it was interesting that they were able to collect data from so many species across many previous studies and also break down trends/relationships between different clades or physiologies. It was also interesting that given that they were using data from studies that showed the opposite, they were able to come to the conclusion they found. We particularly liked the authors' suggestions about how to move the field forward and the call for an improved understanding of RuBisCO kinetic mechanism.
There were a few areas we thought it would be useful to clarify:
- Providing a cartoon model of the proposed mechanism would help readers unfamiliar with the nuances of the models being assessed.
- More information about how the authors selected and filtered data collecting from the literature and how the different datasets were taken into account in the statistical analysis. i.e. how many measurements per species, types of values (mean/median) etc.
- Figure 4 and 5: how was the conclusion reached that there was no correlation between parameters?
- Organization, it would make things stronger to layout the arguments clearly between what came before and after, for those not familiar with the academic argument.
- As the paper argues against what most people are reading it might expect, additional text theorizing why this is the case would be useful to guide readers.
Minor comments
- Figure 2A y-axis labels
- Put a key at the top as the symbols can get buried in the text
-
