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Cold temperature is prevalent across the biosphere and slows the rates of chemical reactions. Increased catalysis has been predicted to be a dominant adaptive trait of enzymes to reduced temperature, and this expectation has informed physical models for enzyme catalysis and influenced bioprospecting strategies. To systematically test rate enhancement as an adaptive trait to cold, we paired kinetic constants of 2223 enzyme reactions with their organism’s optimal growth temperature ( T Growth ) and analyzed trends of rate constants as a function of T Growth . These data do not support a general increase in rate enhancement in cold adaptation. In the model enzyme ketosteroid isomerase (KSI), there is prior evidence for temperature adaptation from a change in an active site residue that results in a tradeoff between activity and stability. Nevertheless, we found that little of the rate constant variation for 20 KSI variants was accounted for by T Growth . In contrast, and consistent with prior expectations, we observed a correlation between stability and T Growth across 433 proteins. These results suggest that temperature exerts a weaker selection pressure on enzyme rate constants than stability and that evolutionary forces other than temperature are responsible for the majority of enzymatic rate constant variation.
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Parallel molecular mechanisms for enzyme temperature adaptation
The mechanisms that underly the adaptation of enzyme activities and stabilities to temperature are fundamental to our understanding of molecular evolution and how enzymes work. Here, we investigate the molecular and evolutionary mechanisms of enzyme temperature adaption, combining deep mechanistic studies with comprehensive sequence analyses of thousands of enzymes. We show that temperature adaptation in ketosteroid isomerase (KSI) arises primarily from one residue change with limited, local epistasis, and we establish the underlying physical mechanisms. This residue change occurs in diverse KSI backgrounds, suggesting parallel adaptation to temperature. We identify residues associated with organismal growth temperature across 1005 diverse bacterial enzyme families, suggesting widespread parallel adaptation to temperature. We assess the residue properties, molecular interactions, and interaction networks that appear to underly temperature adaptation.
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- Award ID(s):
- 1714723
- PAR ID:
- 10216459
- Publisher / Repository:
- American Association for the Advancement of Science (AAAS)
- Date Published:
- Journal Name:
- Science
- Volume:
- 371
- Issue:
- 6533
- ISSN:
- 0036-8075
- Page Range / eLocation ID:
- Article No. eaay2784
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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