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

Biochemistry, vol. 59, pp. 3562–3569

Abstract

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 ( T inf ) 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, T inf 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.

Authors 7

1. Erica J. Prentice

   University of Waikato

   Affiliation as printed

   School of Science - Te Aka Ma̅tuatua, University of Waikato, Hamilton 3216, New Zealand

2. Joanna Hicks

   University of Waikato

   Affiliation as printed

   School of Science - Te Aka Ma̅tuatua, University of Waikato, Hamilton 3216, New Zealand

3. Hendrik Ballerstedt Aachen Institute of Applied Microbiology

   RWTH Aachen University

   Affiliation as printed

   Institute of Applied Microbiology (iAMB), Aachen Biology and Biotechnology (ABBt), RWTH Aachen University, Worringerweg 1, D-52074 Aachen, Germany

4. Lars M. Blank Aachen Institute of Applied Microbiology

   RWTH Aachen University

   Affiliation as printed

   Institute of Applied Microbiology (iAMB), Aachen Biology and Biotechnology (ABBt), RWTH Aachen University, Worringerweg 1, D-52074 Aachen, Germany

5. Liyin L. Liang

   Manaaki Whenua – Landcare Research

   Affiliation as printed

   Manaaki Whenua-Landcare Research, Private Bag 11052, Palmerston North 4442, New Zealand

6. Louis A. Schipper

   University of Waikato

   Affiliation as printed

   School of Science - Te Aka Ma̅tuatua, University of Waikato, Hamilton 3216, New Zealand

7. Vickery L. Arcus corresponding

   University of Waikato

   Affiliation as printed

   School of Science - Te Aka Ma̅tuatua, University of Waikato, Hamilton 3216, New Zealand