Coupling of ATP and PMF in Escherichia coli is determined by growth conditions

The ATP molecule is the universal energy currency across all living organisms. There are two fundamental pathways of ATP synthesis: substrate-level and oxidative phosphorylation. While substrate-level phosphorylation generates ATP directly, in oxidative phosphorylation, proton motive force (PMF) is required to power ATP synthesis via the F1Fo ATP synthase. Using Escherichia coli, we show that due to simultaneous use of both pathways, the strength of coupling between ATP and PMF strongly depends on growth conditions: coupling is weak when requirements for independent generation of ATP and PMF are met, and becomes essential when not. We determine the conditions, under which PMF-ATP coupling becomes essential and show that PMF is required for bacterial growth irrespective of its ATP synthesis function. We propose that the main role of F1Fo in Escherichia coli, contrary to the canonical view, is not to generate ATP but to provide an auxiliary pathway that allows both, ATP and PMF, to be produced.