Cited by 169Origins and Evolution of LifeATP Synthase and ATPases ResearchLipid Membrane Structure and Behavior

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Co-evolution of primordial membranes and membrane proteins

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Mulkidjanian, Armen Y., Galperin, Michael Y., Koonin, Eugene V.·2009·Trends in Biochemical Sciences

DOI 10.1016/j.tibs.2009.01.005PMC PMC2752816

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Abstract

Studies of the past several decades have provided major insights into the structural organization of biological membranes and mechanisms of many membrane molecular machines. However, the origin(s) of the membrane(s) and membrane proteins remains enigmatic. We discuss different concepts of the origin and early evolution of membranes with a focus on the evolution of the (im)permeability to charged molecules such as proteins, nucleic acids and small ions. Reconstruction of the evolution of F-type and A/V-type membrane ATPases (ATP synthases), which are either proton- or sodium-dependent, might help us to understand not only the origin of membrane bioenergetics but also of membranes themselves. We argue that evolution of biological membranes occurred as a process of co-evolution of lipid bilayers, membrane proteins and membrane bioenergetics.

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VMD: visual molecular dynamics
Humphrey, W., Dalke, A., & Schulten, K. (1996) · Journal of Molecular Graphics · doi:10.1016/0263-7855(96)00018-5 · Cited by 66,952
CHEMIOSMOTIC COUPLING IN OXIDATIVE AND PHOTOSYNTHETIC PHOSPHORYLATION
Mitchell, P. D. (1966) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/j.1469-185x.1966.tb01501.x · Cited by 3,674
THE ATP SYNTHASE—A SPLENDID MOLECULAR MACHINE
Boyer, P. D. (1997) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.66.1.717 · Cited by 2,014
Synthesizing life
Szostak, J. W., Bartel, D. P., & Luisi, P. L. (2001) · Nature · doi:10.1038/35053176 · Cited by 1,681
Vacuolar ATPases: rotary proton pumps in physiology and pathophysiology
Forgac, M. D. (2007) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2272 · Cited by 1,626
Intracellular protein topogenesis
Blobel, G. (1980) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.77.3.1496 · Cited by 1,393
The biological chemistry of the elements: the inorganic chemistry of life
(1992) · Choice Reviews Online · doi:10.5860/choice.30-0286 · Cited by 1,326
Biomembranes: molecular structure and function
(1989) · Choice Reviews Online · doi:10.5860/choice.27-0304 · Cited by 1,232
The universal ancestor
Woese, C. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.12.6854 · Cited by 1,053
Data growth and its impact on the SCOP database: new developments
Andreeva, A. E., Howorth, D., Chandonia, J., Brenner, S. E., Hubbard, T., Chothia, C., & Murzin, A. G. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm993 · Cited by 933
On the origins of cells: A hypothesis for the evolutionary transitions from abiotic geochemistry to chemoautotrophic prokaryotes, and from prokaryotes to nucleated cells
Martin, W., & Russell, M. J. (2003) · Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences · doi:10.1098/rstb.2002.1183 · Cited by 856
A Functional-Phylogenetic Classification System for Transmembrane Solute Transporters
Saier, M. H. (2000) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.64.2.354-411.2000 · Cited by 827
Comparative genomics, minimal gene-sets and the last universal common ancestor
Koonin, E. V. (2003) · Nature Reviews Microbiology · doi:10.1038/nrmicro751 · Cited by 661
Self-citation
The V-type H+ ATPase: molecular structure and function, physiological roles and regulation
Beyenbach, K., & Wieczorek, H. (2006) · Journal of Experimental Biology · doi:10.1242/jeb.02014 · Cited by 637
The Lipid World
Segré, D., Ben-Eli, D., Deamer, D. W., & Lancet, D. (2001) · Origins of life and evolution of the biosphere · doi:10.1023/a:1006746807104 · Cited by 620
Helical Membrane Protein Folding, Stability, and Evolution
Popot, J., & Engelman, D. M. (2000) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.69.1.881 · Cited by 591
Chemiosmotic coupling in oxidative and photosynthetic phosphorylation
Mitchell, P. (2011) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2011.09.018 · Cited by 588
Structure and Function of Hexameric Helicases
Patel, S. S., & Picha, K. M. (2000) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.69.1.651 · Cited by 563
Mechanically driven ATP synthesis by F1-ATPase
Itoh, H., Takahashi, A., Adachi, K., Noji, H., Yasuda, R., Yoshida, M., & Kinosita, K. (2004) · Nature · doi:10.1038/nature02212 · Cited by 545
Pore-forming protein toxins: from structure to function
Parker, M. W., & Feil, S. C. (2004) · Progress in Biophysics and Molecular Biology · doi:10.1016/j.pbiomolbio.2004.01.009 · Cited by 468
The structure of the central stalk in bovine F(1)-ATPase at 2.4 A resolution.
(2000) · Nature Structural Biology · doi:10.1038/80981 · Cited by 448
On the origin of genomes and cells within inorganic compartments
Koonin, E. V., & Martin, W. (2005) · Trends in Genetics · doi:10.1016/j.tig.2005.09.006 · Cited by 406
Self-citation
Do sterols reduce proton and sodium leaks through lipid bilayers?
Haines, T. H. (2001) · Progress in Lipid Research · doi:10.1016/s0163-7827(01)00009-1 · Cited by 387
The biological chemistry of the elements: The inorganic chemistry of life
THOMSON, A. J. (1992) · Journal of Inorganic Biochemistry · doi:10.1016/0162-0134(92)84050-w · Cited by 387
Root of the universal tree of life based on ancient aminoacyl-tRNA synthetase gene duplications.
Brown, J. R., & Doolittle, W. F. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.7.2441 · Cited by 379
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
Biosynthesis of Ether-Type Polar Lipids in Archaea and Evolutionary Considerations
Koga, Y., & Morii, H. (2007) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00033-06 · Cited by 366
Structure 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
Did DNA replication evolve twice independently?
Leipe, D. D., Aravind, L., & Koonin, E. V. (1999) · Nucleic Acids Research · doi:10.1093/nar/27.17.3389 · Cited by 351
Self-citation
On the functional proton current pathway of electron transport phosphorylation
Kell, D. B. (1979) · Biochimica et Biophysica Acta (BBA) - Reviews on Bioenergetics · doi:10.1016/0304-4173(79)90018-1 · Cited by 339
Biomembranes: Molecular structure and function
Jain, M. K. (1989) · Cell · doi:10.1016/0092-8674(89)90932-x · Cited by 334
The first living systems: a bioenergetic perspective
Deamer, D. W. (1997) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.61.2.239-261.1997 · Cited by 305
Ancestral lipid biosynthesis and early membrane evolution.
Peretó, J., López-García, P., & Moreira, D. (2004) · TIBS -Trends in Biochemical Sciences. Regular ed · doi:10.1016/j.tibs.2004.07.002 · Cited by 297
The Last Universal Common Ancestor: emergence, constitution and genetic legacy of an elusive forerunner
Glansdorff, N., Xu, Y., & Labedan, B. (2008) · Biology Direct · doi:10.1186/1745-6150-3-29 · Cited by 264
ATP synthesis driven by proton transport in F1F0‐ATP synthase
Weber, J., & Senior, A. E. (2003) · FEBS Letters · doi:10.1016/s0014-5793(03)00394-6 · Cited by 259
Protein Physics: A Course of Lectures
Finkel‘štejn, A. V., & Pticyn, O. B. (2002) · Medical Entomology and Zoology · Cited by 247
Sodium Ion Cycle in Bacterial Pathogens: Evidence from Cross-Genome Comparisons
Häse, C. C., Fedorova, N. D., Galperin, M. Y., & Dibrov, P. A. (2001) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.65.3.353-370.2001 · Cited by 235
Self-citation
Primary sodium ion translocating enzymes
Dimroth, P. (1997) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/s0005-2728(96)00127-2 · Cited by 225
Rooting the tree of life by transition analyses.
Cavalier‐Smith, T. (2006) · Biology Direct · doi:10.1186/1745-6150-1-19 · Cited by 224
Bacteriorhodopsin is an inside-out protein.
Engelman, D. M., & Zaccaı̈, G. (1980) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.77.10.5894 · Cited by 211
Inventing the dynamo machine: the evolution of the F-type and V-type ATPases
Mulkidjanian, A. Y., Makarova, K. S., Galperin, M. Y., & Koonin, E. V. (2007) · Nature Reviews Microbiology · doi:10.1038/nrmicro1767 · Cited by 210
Self-citation
Protons @ interfaces: Implications for biological energy conversion
Mulkidjanian, A. Y., Heberle, J., & Cherepanov, D. A. (2006) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2006.02.015 · Cited by 208
Self-citation
The multifarious couplings of energy transduction
Williams, R. J. P. (1978) · Biochimica et Biophysica Acta (BBA) - Reviews on Bioenergetics · doi:10.1016/0304-4173(78)90007-1 · Cited by 200
The Na+-translocating methyltransferase complex from methanogenic archaea
Gottschalk, G., & Thauer, R. K. (2001) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/s0005-2728(00)00274-7 · Cited by 193
Alkaliphiles:‘basic’molecular problems of pH tolerance and bioenergetics
KRULWICH, T. A. (1995) · Molecular Microbiology · doi:10.1111/j.1365-2958.1995.tb02253.x · Cited by 182
Unique Rotary ATP Synthase and Its Biological Diversity
von Ballmoos, C., Cook, G. M., & Dimroth, P. (2008) · Annual Review of Biophysics · doi:10.1146/annurev.biophys.37.032807.130018 · Cited by 178
ATP 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
Atomic Snapshots of an RNA Packaging Motor Reveal Conformational Changes Linking ATP Hydrolysis to RNA Translocation
Mancini, E. J., Kainov, D. E., Grimes, J. M., Tůma, R., Bamford, D. H., & Stuart, D. I. (2004) · Cell · doi:10.1016/j.cell.2004.09.007 · Cited by 164
Evolutionary primacy of sodium bioenergetics
Mulkidjanian, A. Y., Galperin, M. Y., Makarova, K. S., Wolf, Y. I., & Koonin, E. V. (2008) · Biology Direct · doi:10.1186/1745-6150-3-13 · Cited by 163
Self-citation
Obcells as Proto-Organisms: Membrane Heredity, Lithophosphorylation, and the Origins of the Genetic Code, the First Cells, and Photosynthesis
Cavalier‐Smith, T. (2001) · Journal of Molecular Evolution · doi:10.1007/s002390010245 · Cited by 157
The past and present of sodium energetics: May the sodium-motive force be with you
Mulkidjanian, A. Y., Dibrov, P. A., & Galperin, M. Y. (2008) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2008.04.028 · Cited by 157
Self-citation
Tracing pathways of transport protein evolution
Saier, M. H. (2003) · Molecular Microbiology · doi:10.1046/j.1365-2958.2003.03499.x · Cited by 154
The general protein secretory pathway: phylogenetic analyses leading to evolutionary conclusions
Cao, T. B., & Saier, M. H. (2002) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/s0005-2736(02)00662-4 · Cited by 148
Mechanics of coupling proton movements to c‐ring rotation in ATP synthase
Fillingame, R. H., Angevine, C. M., & Dmitriev, O. Y. (2003) · FEBS Letters · doi:10.1016/s0014-5793(03)01101-3 · Cited by 147
Disparate proteins use similar architectures to damage membranes
Anderluh, G., & Lakey, J. H. (2008) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2008.07.004 · Cited by 144
Transmembrane helices before, during, and after insertion
White, S. H., & von HEIJNE, G. (2005) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2005.07.004 · Cited by 140
Crystal structure of a central stalk subunit C and reversible association/dissociation of vacuole-type ATPase
Iwata, M., Imamura, H., Stambouli, E., Ikeda, C., Tamakoshi, M., Nagata, K., Makyio, H., Hankamer, B. D., Barber, J., Yoshida, M., et al. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0305165101 · Cited by 139
Membrane bioenergetics
Nicholls, D. G. (1989) · FEBS Letters · doi:10.1016/0014-5793(89)80591-5 · Cited by 130
Does Arginine Remain Protonated in the Lipid Membrane? Insights from Microscopic pKa Calculations
Yoo, J., & Cui, Q. (2008) · Biophysical Journal · doi:10.1529/biophysj.107.122945 · Cited by 110
The 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
Self-citation
Sodium Ion Pumps and Hydrogen Production in Glutamate Fermenting Anaerobic Bacteria
Boiangiu, C. D., Jayamani, E., Brügel, D., Herrmann, G., Kim, J., Forzi, L., Hedderich, R., Vgenopoulou, I., Pierik, A. J., Steuber, J., et al. (2005) · Microbial Physiology · doi:10.1159/000091558 · Cited by 107
Stoichiometry of the Peripheral Stalk Subunits E and G of Yeast V1-ATPase Determined by Mass Spectrometry
Kitagawa, N., Mazon, H., Heck, A. J. R., & Wilkens, S. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m707924200 · Cited by 105
Principles of membrane protein assembly and structure
von HEIJNE, G. (1996) · Progress in Biophysics and Molecular Biology · doi:10.1016/s0079-6107(97)85627-1 · Cited by 103
Energy transduction in biological membranes; A textbook of bioenergetics
(1990) · International Journal of Biochemistry · doi:10.1016/0020-711x(90)90215-o · Cited by 103
Stability of model membranes in extreme environments
Namani, T., & Deamer, D. W. (2008) · Origins of Life and Evolution of Biospheres · doi:10.1007/s11084-008-9131-8 · Cited by 97
Microbial transport: Adaptations to natural environments
Konings, W. N. (2006) · Antonie van Leeuwenhoek · doi:10.1007/s10482-006-9089-3 · Cited by 97
Chemistry and Physics of Primitive Membranes
Deamer, D. W., & Dworkin, J. P. (2005) · Springer eBooks · doi:10.1007/b136806 · Cited by 97
The Origin and Evolution of the Oceans
Pinti, D. L. (2005) · Advances in astrobiology and biogeophysics · doi:10.1007/10913406_4 · Cited by 94
Evolutionary links between FliH/YscL‐like proteins from bacterial type III secretion systems and second‐stalk components of the FoF1 and vacuolar ATPases
Pallen, M. J., Bailey, C. M., & Beatson, S. A. (2006) · Protein Science · doi:10.1110/ps.051958806 · Cited by 88
Mechanisms of Passive Ion Permeation through Lipid Bilayers: Insights from Simulations
Tepper, H. L., & Voth, G. A. (2006) · The Journal of Physical Chemistry B · doi:10.1021/jp064192h · Cited by 85
The Prokaryote-to-Eukaryote Transition Reflected in the Evolution of the V/F/A-ATPase Catalytic and Proteolipid Subunits
Hilario, E., & Gogarten, J. P. (1998) · Journal of Molecular Evolution · doi:10.1007/pl00006351 · Cited by 84
Structural and Dynamic Characterization of a Vinculin Binding Site in the Talin Rod,
Gingras, A. R., Vogel, K.-P., Steinhoff, H., Ziegler, W. H., PATEL, B., Emsley, J., Critchley, D. R., Roberts, G. C. K., & Barsukov, I. (2006) · Biochemistry · doi:10.1021/bi052136l · Cited by 80
Chromosomal elements conferring epigenetic inheritance
Lyko, F., & Paro, R. (1999) · BioEssays · doi:10.1002/(sici)1521-1878(199910)21:10 · Cited by 79
Changing the Ion Binding Specificity of the Escherichia coli H+-transporting ATP Synthase by Directed Mutagenesis of Subunit c
Zhang, Y. E., & Fillingame, R. H. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.1.87 · Cited by 74
How leaky were primitive cells?
Deamer, D. W. (2008) · Nature · doi:10.1038/454037a · Cited by 68
Rotation, Structure, and Classification of Prokaryotic V-ATPase
Yokoyama, K., & Imamura, H. (2005) · Journal of Bioenergetics and Biomembranes · doi:10.1007/s10863-005-9480-1 · Cited by 68
Lectures in Astrobiology
Barbier, B., Reisse, J., Martin, H., & Gargaud, M. (2005) · Advances in astrobiology and biogeophysics · doi:10.1007/b10889 · Cited by 62
Lectures in Astrobiology
Gargaud, M., Martin, H., & Claeys, P. (2007) · Springer eBooks · doi:10.1007/978-3-540-33693-8 · Cited by 62
Two Distinct Proton Binding Sites in the ATP Synthase Family
von Ballmoos, C., & Dimroth, P. (2007) · Biochemistry · doi:10.1021/bi701083v · Cited by 61
The Emerging Structure of Vacuolar ATPases
Drory, O., & Nelson, N. (2006) · Physiology · doi:10.1152/physiol.00017.2006 · Cited by 59
Prebiotic replicase evolution in a surface-bound metabolic system: parasites as a source of adaptive evolution
Könnyű, B., Czárán, T., & Szathmáry, E. (2008) · BMC Evolutionary Biology · doi:10.1186/1471-2148-8-267 · Cited by 59
Cell evolution and the problem of membrane topology
Griffiths, G. W. (2007) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2287 · Cited by 55
Proton in the well and through the desolvation barrier
Mulkidjanian, A. Y. (2006) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2006.04.023 · Cited by 53
Self-citation
Na+-translocating NADH: Quinone oxidoreductase: Progress achieved and prospects of investigations
Bogachev, A. V., & Verkhovsky, M. I. (2005) · Biochemistry (Moscow) · doi:10.1007/s10541-005-0093-4 · Cited by 52
Stoichiometry and Localization of the Stator Subunits E and Gin Thermus thermophilus H+-ATPase/Synthase
Esteban, O., Bernal, R. A., Donohoe, M., Videler, H., Sharon, M., Robinson, C. V., & Stock, D. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m704941200 · Cited by 51
Coevolution of metabolic networks and membranes: the scenario of progressive sequestration
Szathmáry, E. (2007) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2007.2070 · Cited by 51
The role of sodium ion transport in Escherichia coli energetics
Dibrov, P. A. (1991) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/s0005-2728(05)80052-0 · Cited by 43
Did the last common ancestor have a biological membrane?
Jékely, G. (2006) · Biology Direct · doi:10.1186/1745-6150-1-35 · Cited by 42
The Influence of Environmental Conditions, Lipid Composition, and Phase Behavior on the Origin of Cell Membranes
Thomas, J. A., & Rana, F. R. (2007) · Origins of Life and Evolution of Biospheres · doi:10.1007/s11084-007-9065-6 · Cited by 39
Features of V‐ATPases that distinguish them from F‐ATPases
Perzov, N., Padler‐Karavani, V., Nelson, H. R., & Nelson, N. (2001) · FEBS Letters · doi:10.1016/s0014-5793(01)02709-0 · Cited by 39
The ATP synthase of Escherichia coli: structure and function of F0 subunits
Deckers‐Hebestreit, G., Greie, J., Stalz, W., & Altendorf, K. (2000) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/s0005-2728(00)00087-6 · Cited by 39
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Self-citation
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Harris, D. (1991) · Biochemical Education · doi:10.1016/0307-4412(91)90035-7 · Cited by 34
Intersubunit bridging by Na+ ions as a rationale for the unusual stability of the c‐rings of Na+‐translocating F1F0 ATP synthases
Meier, T. W., & Dimroth, P. (2002) · EMBO Reports · doi:10.1093/embo-reports/kvf216 · Cited by 34
ChemInform Abstract: ATP Synthesis by Rotary Catalysis
Walker, J. E. (1998) · ChemInform · doi:10.1002/chin.199852366 · Cited by 33
Interaction between Cytochrome caa3 and F1F0-ATP Synthase of Alkaliphilic Bacillus pseudofirmus OF4 Is Demonstrated by Saturation Transfer Electron Paramagnetic Resonance and Differential Scanning Calorimetry Assays
Liu, X., Gong, X., Hicks, D. B., KRULWICH, T. A., Yu, L. P. C., & Yu, C. (2007) · Biochemistry · doi:10.1021/bi0619167 · Cited by 31
Probing the rotor subunit interface of the ATP synthase from Ilyobacter tartaricus
Pogoryelov, D., Nikolaev, Y., Schlattner, U., Pervushin, K. V., Dimroth, P., & Meier, T. W. (2008) · FEBS Journal · doi:10.1111/j.1742-4658.2008.06623.x · Cited by 30
ATP Synthesis by Decarboxylation Phosphorylation
Dimroth, P., & von Ballmoos, C. (2007) · Results and problems in cell differentiation · doi:10.1007/400_2007_045 · Cited by 29
Experimental Verification of a Sequence-Based Prediction: F 1 F 0 -Type ATPase of Vibrio cholerae Transports Protons, Not Na + Ions
Dzioba, J., Häse, C. C., Gosink, K. K., Galperin, M. Y., & Dibrov, P. A. (2003) · Journal of Bacteriology · doi:10.1128/jb.185.2.674-678.2003 · Cited by 27
Self-citation
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Vlassov, A. V. (2005) · Origins of Life and Evolution of Biospheres · doi:10.1007/s11084-005-8901-9 · Cited by 25
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Pohorille, A., Wilson, M. A., & Chipot, C. J. (2003) · Origins of Life and Evolution of Biospheres · doi:10.1023/a:1024627726231 · Cited by 24
Distribution of F- and A/V-type ATPases in Thermus scotoductus and other closely related species
Lapierre, P., Shial, R., & Gogarten, J. P. (2005) · Systematic and Applied Microbiology · doi:10.1016/j.syapm.2005.06.004 · Cited by 21
Membrane Properties of Branched Polyprenyl Phosphates, Postulated as Primitive Membrane Constituents
Gotoh, M., Miki, A., Nagano, H., Ribeiro, N., Elhabiri, M., Gumienna‐Kontecka, E., Albrecht‐Gary, A., Schmutz, M., Ourisson, G., & Nakatani, Y. (2006) · Chemistry & Biodiversity · doi:10.1002/cbdv.200690047 · Cited by 17
ATP Synthesis by Rotary Catalysis (Nobel lecture)
Walker, J. E. (1998) · Angewandte Chemie International Edition · doi:10.1002/(sici)1521-3773(19980918)37:17

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Authors: Mulkidjanian, A. Y., Galperin, M. Y., & Koonin, E. V.
Affiliations: Osnabrück University (DE)
National Institutes of Health (US)
Corresponding author: Mulkidjanian, Armen Y.
Koonin, Eugene V.
ORCID: Mulkidjanian, Armen Y.
Galperin, Michael Y.
Koonin, Eugene V.
Venue: Trends in Biochemical Sciences
Publisher: Elsevier BV
Published: 2009-04
Volume: 34
Issue: 4
Pages: 206-215
ISSN: 0968-0004 (ISSN-L)
DOI: 10.1016/j.tibs.2009.01.005
PMC: PMC2752816
OpenAlex: W2153085358
Cited by: 169
References: 105
Citations by year: 2026: 6 · 2025: 7 · 2024: 14 · 2023: 7 · 2022: 9 · 2021: 12 · 2020: 8 · 2019: 9 · 2018: 4 · 2017: 5 · 2016: 9 · 2015: 13 · 2014: 11 · 2013: 14 · 2012: 12
FWCI: 0.96
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Trends in Biochemical Sciences (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health
U.S. National Library of Medicine (Z01LM000073)
Topics: Physical Sciences › Physics and Astronomy › Astronomy and Astrophysics › Origins and Evolution of Life
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › ATP Synthase and ATPases Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Lipid Membrane Structure and Behavior
Keywords: membrane protein evolution, lipid bilayers, membrane permeability, membrane ATPase, F-type ATP synthase, membrane bioenergetics, coevolution
MeSH terms: Adenosine Triphosphatases, Cell Membrane, Biological Evolution, Membrane Proteins, Evolution, Molecular

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Co-evolution of primordial membranes and membrane proteins

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