Cited by 131ATP Synthase and ATPases ResearchIon Transport and Channel RegulationPhotosynthetic Processes and Mechanisms

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Promiscuous archaeal ATP synthase concurrently coupled to Na + and H + translocation

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Schlegel, Katharina, Leone, Vanessa, Faraldo-Gómez, José D., Müller, Volker·2012·Proceedings of the National Academy of Sciences

DOI 10.1073/pnas.1115796109PMC PMC3271924

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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.

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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
ORCID: Schlegel, Katharina
Leone, Vanessa
Müller, Volker
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
DOI: 10.1073/pnas.1115796109
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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Promiscuous archaeal ATP synthase concurrently coupled to Na + and H + translocation

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