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Promiscuous archaeal ATP synthase concurrently coupled to Na + and H + translocation
Open accessAbstract
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.
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“Any improvement in coupling, of course, requires that the ancient ATPase could use Na+ ions, similar to how the modern one can [204,205], perhaps because hydronium ions (H3O+) have an identical charge and similar ionic radius to Na+ (ionic radii for unhydrated H3O+ = 115 pm, and for Na+ = 117 pm).”
From Early bioenergetic evolution (2013) · cites this paper as [204]
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Metadata
- Authors
- Schlegel, K., Leone, V., Faraldo-Gómez, J. D., & Müller, V.
- Affiliations
- Goethe University Frankfurt (DE)
- Max Planck Institute of Biophysics (DE)
- Theoretical Molecular Biophysics Group, Max Planck Institute of Biophysics, 60438 Frankfurt am Main, Germany, and
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2012-01-04
- Volume
- 109
- Issue
- 3
- Pages
- 947-952
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3271924
- OpenAlex
- W2148772877
- Cited by
- 131
- References
- 43
- Citations by year
- 2026: 12 · 2025: 7 · 2024: 7 · 2023: 8 · 2022: 5 · 2021: 6 · 2020: 7 · 2019: 12 · 2018: 12 · 2017: 6 · 2016: 7 · 2015: 10 · 2014: 6 · 2013: 14 · 2012: 12
- FWCI
- 5.40
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Max Planck Institute for Plasma Physics (submittedVersion)
- Max Planck Digital Library (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- Funders
- Deutsche Forschungsgemeinschaft (SFB 807)
- Senckenberg Biodiversität und Klima Forschungszentrum
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › ATP Synthase and ATPases Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion Transport and Channel Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Photosynthetic Processes and Mechanisms
- Keywords
- ATP synthase, Methanosarcina acetivorans, archaea, proton translocation, sodium translocation, ion selectivity, rotary mechanism, methanogenesis, inverted membrane vesicles, ATP hydrolysis
- MeSH terms
- Adenosine Triphosphatases, Adenosine Triphosphate, Biological Transport, Energy Metabolism, Hydrogen-Ion Concentration, Hydrolysis, Models, Biological, Protein Binding, Protons, Sodium, Methanosarcina, Protein Subunits, Unilamellar Liposomes
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