DOI: 10.1073/pnas.0600605103. Despite slow catalysis and confused substrate specificity, all ribulose bisphosphate carboxylases may be nearly perfectly optimized

Despite slow catalysis and confused substrate specificity, all ribulose bisphosphate carboxylases may be nearly perfectly optimized

10.1073/pnas.0600605103

Crossref journal-article

Proceedings of the National Academy of Sciences

Proceedings of the National Academy of Sciences (341)

Abstract

The cornerstone of autotrophy, the CO 2 -fixing enzyme, d -ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco), is hamstrung by slow catalysis and confusion between CO 2 and O 2 as substrates, an “abominably perplexing” puzzle, in Darwin's parlance. Here we argue that these characteristics stem from difficulty in binding the featureless CO 2 molecule, which forces specificity for the gaseous substrate to be determined largely or completely in the transition state. We hypothesize that natural selection for greater CO 2 /O 2 specificity, in response to reducing atmospheric CO 2 :O 2 ratios, has resulted in a transition state for CO 2 addition in which the CO 2 moiety closely resembles a carboxylate group. This maximizes the structural difference between the transition states for carboxylation and the competing oxygenation, allowing better differentiation between them. However, increasing structural similarity between the carboxylation transition state and its carboxyketone product exposes the carboxyketone to the strong binding required to stabilize the transition state and causes the carboxyketone intermediate to bind so tightly that its cleavage to products is slowed. We assert that all Rubiscos may be nearly perfectly adapted to the differing CO 2 , O 2 , and thermal conditions in their subcellular environments, optimizing this compromise between CO 2 /O 2 specificity and the maximum rate of catalytic turnover. Our hypothesis explains the feeble rate enhancement displayed by Rubisco in processing the exogenously supplied carboxyketone intermediate, compared with its nonenzymatic hydrolysis, and the positive correlation between CO 2 /O 2 specificity and 12 C/ 13 C fractionation. It further predicts that, because a more product-like transition state is more ordered (decreased entropy), the effectiveness of this strategy will deteriorate with increasing temperature.

Bibliography

Tcherkez, G. G. B., Farquhar, G. D., & Andrews, T. J. (2006). Despite slow catalysis and confused substrate specificity, all ribulose bisphosphate carboxylases may be nearly perfectly optimized. Proceedings of the National Academy of Sciences, 103(19), 7246â7251.

Authors 3

Guillaume G. B. Tcherkez (first)
Graham D. Farquhar (additional)
T. John Andrews (additional)

References 58 Referenced 652

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Dates

Type	When
Created	19 years, 4 months ago (April 26, 2006, 8:39 p.m.)
Deposited	3 years, 4 months ago (April 12, 2022, 3:17 p.m.)
Indexed	1 week ago (Aug. 19, 2025, 6:31 a.m.)
Issued	19 years, 3 months ago (May 9, 2006)
Published	19 years, 3 months ago (May 9, 2006)
Published Online	19 years, 3 months ago (May 9, 2006)
Published Print	19 years, 3 months ago (May 9, 2006)

Funders 0

None

BibTeX

@article{Tcherkez_2006, title={Despite slow catalysis and confused substrate specificity, all ribulose bisphosphate carboxylases may be nearly perfectly optimized}, volume={103}, ISSN={1091-6490}, url={http://dx.doi.org/10.1073/pnas.0600605103}, DOI={10.1073/pnas.0600605103}, number={19}, journal={Proceedings of the National Academy of Sciences}, publisher={Proceedings of the National Academy of Sciences}, author={Tcherkez, Guillaume G. B. and Farquhar, Graham D. and Andrews, T. John}, year={2006}, month=may, pages={7246–7251} }

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