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Promiscuous archaeal ATP synthase concurrently coupled to Na + and H + translocation
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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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Cites
Bradford, M. M. (1976) · Analytical Biochemistry · doi:10.1016/0003-2697(76)90527-3 · Cited by 255,302
Structure at 2.8 Â resolution of F1-ATPase from bovine heart mitochondria
Abrahams, J., Leslie, A. G., Lutter, R., & Walker, J. (1994) · Nature · doi:10.1038/370621a0 · Cited by 2,961
Methanogenic archaea: ecologically relevant differences in energy conservation
Thauer, R. K., Kaster, A.-K., Seedorf, H., Buckel, W., & Hedderich, R. (2008) · Nature Reviews Microbiology · doi:10.1038/nrmicro1931 · Cited by 2,184
ATP synthase — a marvellous rotary engine of the cell
Yoshida, M., Muneyuki, E., & Hisabori, T. (2001) · Nature Reviews Molecular Cell Biology · doi:10.1038/35089509 · Cited by 964
Mechanical Rotation of the c Subunit Oligomer in ATP Synthase (F 0 F 1 ): Direct Observation
Sambongi, Y., Iko, Y., Tanabe, M., Omote, H., Iwamoto-Kihara, A., Ueda, I., Yanagida, T., Wada, Y., & Futai, M. (1999) · Science · doi:10.1126/science.286.5445.1722 · Cited by 445
Structure of the Rotor Ring of F-Type Na + -ATPase from Ilyobacter tartaricus
Meier, T. W., Polzer, P., Diederichs, K., Welte, W., & Dimroth, P. (2005) · Science · doi:10.1126/science.1111199 · Cited by 370
Torque generation and elastic power transmission in the rotary FOF1-ATPase
Junge, W., Sielaff, H., & Engelbrecht, S. (2009) · Nature · doi:10.1038/nature08145 · Cited by 358
Biegel, E., Schmidt, S., Gónzalez, J. M., & Müller, V. (2011) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-010-0555-8 · Cited by 354
Self-citationStructure of the Rotor of the V-Type Na + -ATPase from Enterococcus hirae
Murata, T., Yamato, I., Kakinuma, Y., Leslie, A. G. W., & Walker, J. E. (2005) · Science · doi:10.1126/science.1110064 · Cited by 354
Vik, S. B., & Antonio, B. J. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)43822-7 · Cited by 339
Essentials for ATP Synthesis by F1F0 ATP Synthases
von Ballmoos, C., Wiedenmann, A., & Dimroth, P. (2009) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.78.081307.104803 · Cited by 332
The rotary mechanism of ATP synthase
Stock, D., Gibbons, C., Aréchaga, I., Leslie, A. G. W., & Walker, J. E. (2000) · Current Opinion in Structural Biology · doi:10.1016/s0959-440x(00)00147-0 · Cited by 325
F‐ATPase: specific observation of the rotating c subunit oligomer of EFoEF1
Pänke, O., Gumbiowski, K., Junge, W., & Engelbrecht, S. (2000) · FEBS Letters · doi:10.1016/s0014-5793(00)01436-8 · Cited by 189
High-resolution structure of the rotor ring of a proton-dependent ATP synthase
Pogoryelov, D., Yıldız, Ö., Faraldo‐Gómez, J. D., & Meier, T. W. (2009) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.1678 · Cited by 186
Self-citationATP synthases: structure, function and evolution of unique energy converters
M�ller, V., & Gr�ber, G. (2003) · Cellular and Molecular Life Sciences (CMLS) · doi:10.1007/s000180300040 · Cited by 174
Self-citationMicroscopic rotary mechanism of ion translocation in the Fo complex of ATP synthases
Pogoryelov, D., Krah, A., Langer, J. D., Yıldız, Ö., Faraldo‐Gómez, J. D., & Meier, T. W. (2010) · Nature Chemical Biology · doi:10.1038/nchembio.457 · Cited by 145
Self-citationLife Close to the Thermodynamic Limit: How Methanogenic Archaea Conserve Energy
Deppenmeier, U., & Müller, V. (2007) · Results and Problems in Cell Differentiation · doi:10.1007/400_2006_026 · Cited by 132
Self-citationCatalytic and mechanical cycles in F‐ATP synthases
Dimroth, P., von Ballmoos, C., & Meier, T. W. (2006) · EMBO Reports · doi:10.1038/sj.embor.7400646 · Cited by 128
Laubinger, W., & Dimroth, P. (1989) · Biochemistry · doi:10.1021/bi00444a010 · Cited by 122
Structure–function relationships of A-, F- and V-ATPases
Grüber, G., Wieczorek, H., Harvey, W. R., & Müller, V. (2001) · Journal of Experimental Biology · doi:10.1242/jeb.204.15.2597 · Cited by 122
Self-citationThe Proton-Driven Rotor of ATP Synthase: Ohmic Conductance (10 fS), and Absence of Voltage Gating
Feniouk, B. A., Kozlova, M. A., Кнорре, Д. А., Cherepanov, D. A., Mulkidjanian, A. Y., & Junge, W. (2004) · Biophysical Journal · doi:10.1529/biophysj.103.036962 · Cited by 108
Pourcher, T., Leclercq, S., Brandolin, G., & Leblanc, G. (1995) · Biochemistry · doi:10.1021/bi00013a033 · Cited by 99
Complete Ion-Coordination Structure in the Rotor Ring of Na+-Dependent F-ATP Synthases
Meier, T. W., Krah, A., Bond, P. J., Pogoryelov, D., Diederichs, K., & Faraldo‐Gómez, J. D. (2009) · Journal of Molecular Biology · doi:10.1016/j.jmb.2009.05.082 · Cited by 96
Self-citationHeise, R., Müller, V., & Gottschalk, G. (1992) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1992.tb16959.x · Cited by 93
Self-citationTolner, B., Ubbink-Kok, T., Poolmann, B., & Konings, W. N. (1995) · Molecular Microbiology · doi:10.1111/j.1365-2958.1995.mmi_18010123.x · Cited by 91
A New Type of Proton Coordination in an F1Fo-ATP Synthase Rotor Ring
Preiß, L., Yıldız, Ö., Hicks, D. B., KRULWICH, T. A., & Meier, T. W. (2010) · PLoS Biology · doi:10.1371/journal.pbio.1000443 · Cited by 90
Rotation of the Proteolipid Ring in the V-ATPase
Yokoyama, K., Nakano, M., Imamura, H., Yoshida, M., & Tamakoshi, M. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m303104200 · Cited by 90
Direct observation of stepped proteolipid ring rotation in E. coli FoF1‐ATP synthase
Ishmukhametov, R. R., Hornung, T., Spetzler, D. B., & Frasch, W. D. (2010) · The EMBO Journal · doi:10.1038/emboj.2010.259 · Cited by 88
Reidlinger, J., & Müller, V. (1994) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1994.tb18992.x · Cited by 87
Self-citationKluge, C., & Dimroth, P. (1993) · Biochemistry · doi:10.1021/bi00090a013 · Cited by 79
Aqueous access pathways in subunit a of rotary ATP synthase extend to both sides of the membrane
Angevine, C. M., Herold, K. A. G., & Fillingame, R. H. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2234364100 · Cited by 74
The ins and outs of Na+ bioenergetics in Acetobacterium woodii
Schmidt, S., Biegel, E., & Müller, V. (2009) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2008.12.015 · Cited by 64
Self-citationStructural and energetic basis for H+ versus Na+ binding selectivity in ATP synthase Fo rotors
Krah, A., Pogoryelov, D., Langer, J. D., Bond, P. J., Meier, T. W., & Faraldo‐Gómez, J. D. (2010) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2010.04.014 · Cited by 62
Self-citationTerahara, N., KRULWICH, T. A., & Ito, M. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0802106105 · Cited by 55
On the Structure of the Proton-Binding Site in the Fo Rotor of Chloroplast ATP Synthases
Krah, A., Pogoryelov, D., Meier, T. W., & Faraldo‐Gómez, J. D. (2009) · Journal of Molecular Biology · doi:10.1016/j.jmb.2009.10.059 · Cited by 44
Self-citationCatalytic properties of Na+-translocating V-ATPase in Enterococcus hirae
Murata, T., Kawano‐Kawada, M., Igarashi, K., Yamato, I., & Kakinuma, Y. (2001) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/s0005-2728(00)00278-4 · Cited by 43
Steed, R., & Fillingame, R. H. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m800901200 · Cited by 40
Bacterial sodium ion-coupled energetics
Dimroth, P. (1994) · Antonie van Leeuwenhoek · doi:10.1007/bf00872221 · Cited by 38
Steed, R., & Fillingame, R. H. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.002501 · Cited by 37
Correction: A New Type of Proton Coordination in an F1Fo-ATP Synthase Rotor Ring
Preiß, L., Yıldız, Ö., Hicks, D. B., KRULWICH, T. A., & Meier, T. W. (2010) · PLoS Biology · doi:10.1371/annotation/4b30bafe-631f-48dd-a5c2-4e727a5853d1 · Cited by 28
Duncan, T. M., Zhou, Y., Bulygin, V. V., Hutcheon, M. L., & Cross, R. L. (1995) · Biochemical Society Transactions · doi:10.1042/bst0230736 · Cited by 25
On the Question of Hydronium Binding to ATP-Synthase Membrane Rotors
Leone, V., Krah, A., & Faraldo‐Gómez, J. D. (2010) · Biophysical Journal · doi:10.1016/j.bpj.2010.07.046 · Cited by 22
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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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