Enzyme oscillation can enhance the thermodynamic efficiency of cellular metabolism: Consequence of anti-phase coupling between reaction flux and affinity

TL;DR

This study demonstrates that enzyme oscillations can improve cellular metabolic efficiency by temporally separating opposing reactions, a finding supported by a simple model and relevant to biological manipulation.

Contribution

The paper introduces a model showing enzyme oscillations can enhance thermodynamic efficiency by anti-phase coupling of reaction flux and affinity, highlighting a novel dynamic mechanism.

Findings

Enzyme oscillations improve metabolic efficiency.

Anti-phase coupling of flux and affinity is crucial.

Autonomous enzyme oscillations also enhance efficiency.

Abstract

Cells generally convert nutrient resources to useful products via energy transduction. Accordingly, the thermodynamic efficiency of this conversion process is one of the most essential characteristics of living organisms. However, although these processes occur under conditions of dynamic metabolism, most studies of cellular thermodynamic efficiency have been restricted to examining steady states; thus, the relevance of dynamics to this efficiency has not yet been elucidated. Here, we develop a simple model of metabolic reactions with anabolism-catabolism coupling catalysed by enzymes. Through application of external oscillation in the enzyme abundances, the thermodynamic efficiency of metabolism was found to be improved. This result is in strong contrast with that observed in the oscillatory input, in which the efficiency always decreased with oscillation. This improvement was effectively achieved by separating the anabolic and catabolic reactions, which tend to disequilibrate each other, and taking advantage of the temporal oscillations so that each of the antagonistic reactions could progress near equilibrium. In this case, anti-phase oscillation between the reaction flux and chemical affinity through oscillation of enzyme abundances is essential. This improvement was also confirmed in a model capable of generating autonomous oscillations in enzyme abundances. Finally, the possible relevance of the improvement in thermodynamic efficiency is discussed with respect to the potential for manipulation of metabolic oscillations in microorganisms.