The Inflection Point Hypothesis: The Relationship between the Temperature Dependence of Enzyme-Catalyzed Reaction Rates and Microbial Growth Rates.

Erica J Prentice, Joanna Hicks, Hendrik Ballerstedt, Lars M Blank, Liyı N L Liáng, Louis A Schipper, Vickery L Arcus

Biochemistry 2020 Sep 29

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The temperature dependence of biological rates at different scales (from individual enzymes to isolated organisms to ecosystem processes such as soil respiration and photosynthesis) is the subject of much historical and contemporary research. The precise relationship between the temperature dependence of enzyme rates and those at larger scales is not well understood. We have developed macromolecular rate theory (MMRT) to describe the temperature dependence of biological processes at all scales. Here we formalize the scaling relationship by investigating MMRT both at the molecular scale (constituent enzymes) and for growth of the parent organism. We demonstrate that the inflection point (Tinf) for the temperature dependence of individual metabolic enzymes coincides with the optimal growth temperature for the parent organism, and we rationalize this concordance in terms of the necessity for linearly correlated rates for metabolic enzymes over fluctuating environmental temperatures to maintain homeostasis. Indeed, Tinf is likely to be under strong selection pressure to maintain coordinated rates across environmental temperature ranges. At temperatures at which rates become uncorrelated, we postulate a regulatory catastrophe and organism growth rates precipitously decline at temperatures where this occurs. We show that the curvature in the plots of the natural log of the rate versus temperature for individual enzymes determines the curvature for the metabolic process overall and the curvature for the temperature dependence of the growth of the organism. We have called this "the inflection point hypothesis", and this hypothesis suggests many avenues for future investigation, including avenues for engineering the thermal tolerance of organisms.

Citation

Erica J Prentice, Joanna Hicks, Hendrik Ballerstedt, Lars M Blank, Liyı N L Liáng, Louis A Schipper, Vickery L Arcus. The Inflection Point Hypothesis: The Relationship between the Temperature Dependence of Enzyme-Catalyzed Reaction Rates and Microbial Growth Rates. Biochemistry. 2020 Sep 29;59(38):3562-3569