  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.
