The energy spilling reactions of bacteria and other organisms

Abstract

For many years it was assumed that living organisms always utilized ATP in a highly efficient manner, but simple growth studies with bacteria indicated that the efficiency of biomass production was often at least 3-fold lower than the amount that would be predicted from standard biosynthetic pathways. The utilization of energy for maintenance could only explain a small portion of this discrepancy particularly when the growth rate was high. These ideas and thermodynamic arguments indicated that cells might have another avenue of energy utilization. This phenomenon has also been called 'uncoupling', 'spillage' and 'overflow metabolism', but 'energy spilling' is probably the most descriptive term. It appears that many bacteria spill energy, and the few that do not can be killed (large and often rapid decrease in viability), if the growth medium is nitrogen-limited and the energy source is in 'excess'. The lactic acid bacterium, Streptococcus bovis, is an ideal bacterium for the study of energy spilling. Because it only uses substrate level phosphorylation to generate ATP, ATP generation can be calculated with a high degree of certainty. It does not store glucose as glycogen, and its cell membrane can be easily accessed. Comparative analysis of heat production, membrane voltage, ATP production and Ohm's law indicated that the energy spilling reaction of S. bovis is mediated by a futile cycle of protons through the cell membrane. Less is known about Escherichia coli, but in this bacterium energy spilling could be mediated by a futile cycle of potassium or ammonium ions. Energy spilling is not restricted to prokaryotes and appears to occur in yeasts and in higher organisms. In man, energy spilling may be related to cancer, ageing, ischemia and cardiac failure.