Abstract
The ubiquitous enzyme Ribulose 1,5-bisphosphate carboxylase-oxygenase (RuBisCO) fixes atmospheric carbon dioxide within the Calvin-Benson cycle that is utilized by most photosynthetic organisms. Despite this central role, RuBisCO's efficiency surprisingly struggles, with both a very slow turnover rate to products and also impaired substrate specificity, features that have long been an enigma as it would be assumed that its efficiency was under strong evolutionary pressure. RuBisCO's substrate specificity is compromised as it catalyzes a side-fixation reaction with atmospheric oxygen; empirical kinetic results show a trend to tradeoff between relative specificity and low catalytic turnover rate. Although the dominant hypothesis has been that the active-site chemistry constrains the enzyme's evolution, a more recent study on RuBisCO stability and adaptability has implicated competing selection pressures. Elucidating these constraints is crucial for directing future research on improving photosynthesis, as the current literature casts doubt on the potential effectiveness of site-directed mutagenesis to improve RuBisCO's efficiency. Here we use regression analysis to quantify the relationships between kinetic parameters obtained from empirical data sets spanning a wide evolutionary range of RuBisCOs. Most significantly we found that the rate constant for dissociation of CO2 from the enzyme complex was much higher than previous estimates and comparable with the corresponding catalytic rate constant. Observed trends between relative specificity and turnover rate can be expressed as the product of negative and positive correlation factors. This provides an explanation in simple kinetic terms of both the natural variation of relative specificity as well as that obtained by reported site-directed mutagenesis results. We demonstrate that the kinetic behaviour shows a lesser rather than more constrained RuBisCO, consistent with growing empirical evidence of higher variability in relative specificity. In summary our analysis supports an explanation for the origin of the tradeoff between specificity and turnover as due to competition between protein stability and activity, rather than constraints between rate constants imposed by the underlying chemistry. Our analysis suggests that simultaneous improvement in both specificity and turnover rate of RuBisCO is possible.
Highlights
Ribulose 1,5-bisphosphate carboxylase-oxygenase (RuBisCO) is the enzyme responsible for the fixation of carbon derived from atmospheric CO2 as part of the Calvin-Benson cycle that leads to production of the glucose essential for growth in most photosynthetic organisms
RuBisCO has a low turnover rate in higher plants (∼3 s−1) and the efficiency of carbon fixation by the enzyme is compromised by a competing reaction with atmospheric O2 that leads to photorespiration at high cost to the organism in terms of both energy and loss of carbon
A later analysis (Bar-Even et al, 2015) showed that enzyme-substate encounters for the “average” enzyme are not productive(“futile”), again for various reasons. The insights from these analyses are useful in placing RuBisCO’s catalytic rate and efficiency in the context of all enzymes, especially the significant dissociation rate for CO2 we find in this work, but puzzles remain as RuBisCO has been subject to very strong evolutionary pressure
Summary
Ribulose 1,5-bisphosphate carboxylase-oxygenase (RuBisCO) is the enzyme responsible for the fixation of carbon derived from atmospheric CO2 as part of the Calvin-Benson cycle that leads to production of the glucose essential for growth in most photosynthetic organisms. A later analysis (Bar-Even et al, 2015) showed that enzyme-substate encounters for the “average” enzyme are not productive(“futile”), again for various reasons The insights from these analyses are useful in placing RuBisCO’s catalytic rate and efficiency in the context of all enzymes, especially the significant dissociation rate for CO2 we find in this work, but puzzles remain as RuBisCO has been subject to very strong evolutionary pressure. To mitigate this apparent torpidity of the enzyme, organisms have co-evolved other strategies for maintaining levels of photosynthesis. The observed large variations in RuBisCO kinetic parameters from photosynthetic organisms in different kingdoms down to different species (Jordan and Ogren, 1981, 1983) is a consequence of co-evolution with resource allocation into other strategies that lead to enhanced photosynthesis (largely by way of more efficient CO2 and nitrogen utilization) and suppressed photorespiration (Badger and Andrews, 1987; Badger et al, 1998)
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