Promiscuous archaeal ATP synthase concurrently coupled to Na + and H + translocation
- 4 January 2012
- journal article
- Published by Proceedings of the National Academy of Sciences in Proceedings of the National Academy of Sciences of the United States of America
- Vol. 109 (3), 947-952
- https://doi.org/10.1073/pnas.1115796109
Abstract
ATP synthases are the primary source of ATP in all living cells. To catalyze ATP synthesis, these membrane-associated complexes use a rotary mechanism powered by the transmembrane diffusion of ions down a concentration gradient. ATP synthases are assumed to be driven either by H(+) or Na(+), reflecting distinct structural motifs in their membrane domains, and distinct metabolisms of the host organisms. Here, we study the methanogenic archaeon Methanosarcina acetivorans using assays of ATP hydrolysis and ion transport in inverted membrane vesicles, and experimentally demonstrate that the rotary mechanism of its ATP synthase is coupled to the concurrent translocation of both H(+) and Na(+) across the membrane under physiological conditions. Using free-energy molecular simulations, we explain this unprecedented observation in terms of the ion selectivity of the binding sites in the membrane rotor, which appears to have been tuned via amino acid substitutions so that ATP synthesis in M. acetivorans can be driven by the H(+) and Na(+) gradients resulting from methanogenesis. We propose that this promiscuity is a molecular mechanism of adaptation to life at the thermodynamic limit.Keywords
This publication has 45 references indexed in Scilit:
- Biochemistry, evolution and physiological function of the Rnf complex, a novel ion-motive electron transport complex in prokaryotesCellular and Molecular Life Sciences, 2010
- Direct observation of stepped proteolipid ring rotation in E. coli FoF1-ATP synthaseThe EMBO Journal, 2010
- On the Question of Hydronium Binding to ATP-Synthase Membrane RotorsBiophysical Journal, 2010
- A New Type of Proton Coordination in an F1Fo-ATP Synthase Rotor RingPLoS Biology, 2010
- Aqueous Accessibility to the Transmembrane Regions of Subunit c of the Escherichia coli F1F0 ATP SynthasePublished by Elsevier BV ,2009
- Complete Ion-Coordination Structure in the Rotor Ring of Na+-Dependent F-ATP SynthasesJournal of Molecular Biology, 2009
- Mutations alter the sodium versus proton use of a Bacillus clausii flagellar motor and confer dual ion use on Bacillus subtilis motorsProceedings of the National Academy of Sciences of the United States of America, 2008
- Subunit a Facilitates Aqueous Access to a Membrane-embedded Region of Subunit c in Escherichia coli F1F0 ATP SynthasePublished by Elsevier BV ,2008
- Catalytic and mechanical cycles in F‐ATP synthasesEMBO Reports, 2006
- A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye bindingAnalytical Biochemistry, 1976