Abstract
The concept of “electric cables” involved in bioenergetic processes in a living cell was proposed half a century ago [Skulachev, V. P. (1971) Curr. Top. Bioenerg., Elsevier, pp. 127-190]. Membrane structures of a cell were considered as probable pathways for transferring transmembrane electrochemical potential. Further studies have shown that coupling membranes (inner mitochondrial membrane or bacterial cell membrane), i.e., those involved in the generation of membrane potential, can also serve for its transfer. A wide range of organisms from almost all major taxa have been discovered to employ the energy-transmitting function of coupling membranes. Macroscopic (millimeter or even centimeter in length) cable-like structures have been found, the most striking examples of which are giant mitochondria of some unicellular organisms (algae, fungi, protozoa) and animal tissues, filamentous mitochondria, mitochondrial reticulum in animal muscle tissue, and trichomes of cyanobacteria. The importance of such “electric cables” in cells or multicellular structures is determined by their ability to provide rapid energy exchange between metabolic counterparts, energy producers and energy consumers, as the diffusive transport of soluble macroergic molecules (ATP, etc.) requires much longer time. However, in the last 10-15 years, a new type of bacterial “electric cables” of presumably proteinaceous nature has been discovered, which serve a quite different purpose in cell bioenergetics. The molecular structure and functions of these cables will be discussed in the second part of the review (“Electric cables of living cells. II. Bacterial electron conductors”).
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Abbreviations
- ΔµH+ :
-
transmembrane proton electrochemical potential
- ER:
-
endoplasmic reticulum
- GFP:
-
green fluorescent protein
REFERENCES
Galvani, L. (1792) De viribus electricitatis in motu musculari comentarius cum Joannis Aldini dissertatione et notis; accesserunt epistolae ad animalis electricitatis theoriam pertinentes, Apud Societatem Typographicam.
Hodgkin, A. L., and Huxley, A. F. (1952) A quantitative description of membrane current and its application to conduction and excitation in nerve, J. Physiol., 117, 500-544.
Mitchell, P. (1961) Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism, Nature, 191, 144-148.
Mitchell, P. (1966) Chemiosmotic coupling in oxidative and photosynthetic phosphorylation, Biol. Rev., 41, 445-501.
Liberman, E. A., Topaly, V. P., Tsofina, L. M., Jasaitis, A. A., and Skulachev, V. P. (1969) Mechanism of coupling of oxidative phosphorylation and the membrane potential of mitochondria, Nature, 222, 1076-1078.
Green, D. E. (1974) The electromechanical model for energy coupling in mitochondria, Biochim. Biophys. Acta, 346, 27-78.
Skulachev, V. P. (1971) Energy transformations in the respiratory chain, Curr. Top. Bioenerg., Elsevier, pp. 127-190.
Skulachev, V. P. (1980) Integrating functions of biomembranes. Problems of lateral transport of energy, metabolites and electrons, Biochim. Biophys. Acta, 604, 297-320.
Reguera, G., McCarthy, K. D., Mehta, T., Nicoll, J. S., Tuominen, M. T., and Lovley, D. R. (2005) Extracellular electron transfer via microbial nanowires, Nature, 435, 1098-1101.
Nielsen, L. P., Risgaard-Petersen, N., Fossing, H., Christensen, P. B., and Sayama, M. (2010) Electric currents couple spatially separated biogeochemical processes in marine sediment, Nature, 463, 1071-1074.
Filman, D. J., Marino, S. F., Ward, J. E., Yang, L., Mester, Z., Bullitt, E, Lovley, D. R., and Strauss, M. (2019) Cryo-EM reveals the structural basis of long-range electron transport in a cytochrome-based bacterial nanowire, Commun. Biol., 2, 1-6.
Wang, F., Gu, Y., O’Brien, J. P., Sophia, M. Y., Yalcin, S. E., Srikanth, V. Shen, C., Vu, D., Ing, N. L., Hochbaum, A. I., Egelman, E. H., and Malvankar, N. S. (2019) Structure of microbial nanowires reveals stacked hemes that transport electrons over micrometers, Cell, 177, 361-369.
Gilëv, V. P., and Mel’nikova, E. (1969) Mitochondria and the excitation-contraction process in a muscle fiber, Tsitologiia, 11, 117-120.
Margreth, A., Muscatello, U., and Andersson-Cedergren, E. (1963) A morphological and biochemical study on the regulation of carbohydrate metabolism in the muscle cell, Exp. Cell Res., 32, 484-509.
Walker, S. M., and Schrodt, G. R. (1966) Evidence for connections between mitochondria and the sarcoplasmic reticulum and evidence for glycogen granules within the sarcoplasmic reticulum, Am. J. Phys. Med., 45, 25-44.
Bubenzer, H. J. (1966) The thin and the thick muscular fibers of the rat diaphragm, Z. Zellforsch. Mikrosk. Anat., 69, 520.
Gauthier, G. F. (1969) On the relationship of ultrastructural and cytochemical features to color in mammalian skeletal muscle, Z. Zellforsch. Mikrosk. Anat., 95, 462-482.
Bakeeva, L. E., Chentsov, Y. S., and Skulachev, V. P. (1978) Mitochondrial framework (reticulum mitochondriale) in rat diaphragm muscle, Biochim. Biophys. Acta, 501, 349-369.
Bakeeva, L. E., Chentsov, Y. S., and Skulachev, V. P. (1981) Ontogenesis of mitochondrial reticulum in rat diaphragm muscle, Eur. J. Cell Biol., 25, 175-181.
Bakeeva, L. E., Chentsov, Y. S., and Skulachev, V. P. (1983) Intermitochondrial contacts in myocardiocytes, J. Mol. Cell. Cardiol., 15, 413-420.
Glancy, B., Hartnell, L. M., Malide, D., Yu, Z. X., Combs, C. A., Connelly, P. S., Subramaniam, S., and Balaban, R. S. (2015) Mitochondrial reticulum for cellular energy distribution in muscle, Nature, 523, 617-620.
Skulachev, V. P., Bogachev, A. V., and Kasparinsky, F. O. (2011) Membrannaya bioenergetica [Membrane bioenergetics], Izdatelstvo MGU, Moscow.
Amchenkova, A. A., Bakeeva, L. E., Chentsov, Y. S., Skulachev, V. P., and Zorov, D. B. (1988) Coupling membranes as energy-transmitting cables. I. Filamentous mitochondria in fibroblasts and mitochondrial clusters in cardiomyocytes, J. Cell Biol., 107, 481-495.
Drachev, V. A., and Zorov, D. B. (1986) Mitochondria as an electric cable. Experimental testing of a hypothesis, Doklady Akademii Nauk SSSR, 287, 1237-1238.
Osafune, T. (1973) Three-dimensional structures of giant mitochondria, dictyosomes and “concentric lamellar bodies” formed during the cell cycle of Euglena gracilis (Z) in synchronous culture, Microscopy, 22, 51-61.
Burton, M. D., and Moore, J. (1974) The mitochondrion of the flagellate, Polytomella agilis, J. Ultrastruct. Res., 48, 414-419.
Hoffmann, H.-P., and Avers, C. J. (1973) Mitochondrion of yeast: ultrastructural evidence for one giant, branched organelle per cell, Science, 181, 749-751.
Komárek, J., and Johansen, J. R. (2015) Filamentous cyanobacteria, Freshwater Algae of North America, Elsevier, pp. 135-235.
Schnepf, E. (1964) Zur Feinstruktur von Geosiphon Pyriforme, Arch. Mikrobiol., 49, 112-131, doi: https://doi.org/10.1007/BF00422136 .
Van De Meene, A. M. L., Hohmann-Marriott, M. F., Vermaas, W. F. J., and Roberson, R. W. (2006) The three-dimensional structure of the cyanobacterium Synechocystis sp. PCC 6803, Arch. Microbiol., 184, 259-270.
Schneider, D., Fuhrmann, E., Scholz, I., Hess, W. R., and Graumann, P. L. (2007) Fluorescence staining of live cyanobacterial cells suggest non-stringent chromosome segregation and absence of a connection between cytoplasmic and thylakoid membranes, BMC Cell Biol., 8, 1-10.
Nevo, R., Charuvi, D., Shimoni, E., Schwarz, R., Kaplan, A., Ohad, I., and Reich, Z. (2007) Thylakoid membrane perforations and connectivity enable intracellular traffic in cyanobacteria, EMBO J., 26, 1467-1473.
Flores, E., Nieves-Morión, M., and Mullineaux, C. W. (2019) Cyanobacterial septal junctions: properties and regulation, Life, 9, 1.
Chailakhyan, L. M., Glagolev, A. N., Glagoleva, T. N., Murvanidze, G. V., Potapova, T. V., and Skulachev, V. P. (1982) Intercellular power transmission along trichomes of cyanobacteria, Biochim. Biophys. Acta, 679, 60-67.
Potapova, T. V., and Koksharova, O. A. (2020) Filamentous cyanobacteria as a prototype of multicellular organisms, Russ. J. Plant Physiol., 67, 17-30.
Chapman, A. G., and Atkinson, D. E. (1977) Adenine nucleotide concentrations and turnover rates. Their correlation with biological activity in bacteria and yeast, Adv. Microb. Physiol., 15, 253-306.
Nasrulhaq-Boyce, A., and Duckett, J. G. (1991) Dimorphic epidermal cell chloroplasts in the mesophyll-less leaves of an extreme-shade tropical fern, Teratophyllum rotundifoliatum (R. Bonap.) Holtt.: a light and electron microscope study, New Phytol., 119, 433-444.
Sheue, C.-R., Sarafis, V., Kiew, R., Liu, H.-Y., Salino, A., Kuo-Huang, L.-L., Yang, Y.-P., Tsai, C.-C., Lin, C.-H., Yong, J. W. H., and Ku, M. S. B. (2007) Bizonoplast, a unique chloroplast in the epidermal cells of microphylls in the shade plant Selaginella erythropus (Selaginellaceae., Am. J. Botany, 94, 1922-1929.
Paolillo, D. J. (1970) The three-dimensional arrangement of intergranal lamellae in chloroplasts, J. Cell Sci., 6, 243-253.
Austin, J. R., and Staehelin, L. A. (2011) Three-dimensional architecture of grana and stroma thylakoids of higher plants as determined by electron tomography, Plant Physiol., 155, 1601-1611.
Anderson, J. M. (2012) Lateral heterogeneity of plant thylakoid protein complexes: early reminiscences, Philos. Trans. R. Soc. B Biol. Sci., 367, 3384-3388.
Rottenberg, H., and Grunwald, T. (1972) Determination of ΔpH in chloroplasts. 3. Ammonium uptake as a measure of ΔpH in chloroplasts and sub-chloroplast particles, Eur. J. Biochem., 25, 71-74.
Tikhonov, A. N., Agafonov, R. V, Grigor’ev, I. A., Kirilyuk, I. A., Ptushenko, V. V., and Trubitsin, B. V. (2008) Spin-probes designed for measuring the intrathylakoid pH in chloroplasts, Biochim. Biophys. Acta, 1777, 285-294.
De Kouchkovsky, Y., and Haraux, F. (1981) 2H2O effect on the electron and proton flow in isolated chloroplasts: an indication for lateral heterogeneity of membrane pH, Biochem. Biophys. Res. Commun., 99, 205-212.
De Kouchkovsky, Y., Haraux, F., and Sigalat, C. (1982) Effect of hydrogen-deuterium exchange on energy-coupled processes in thylakoids: a new illustration of the hypothesis of local proton gradients with the energy-transducing biomembranes, FEBS Lett., 139, 245-249.
Vershubskii, A. V., Trubitsin, B. V., Priklonskii, V. I., and Tikhonov, A. N. (2017) Lateral heterogeneity of the proton potential along the thylakoid membranes of chloroplasts, Biochim. Biophys. Acta, 1859, 388-401.
Rieger, B., Junge, W., and Busch, K. B. (2014) Lateral pH gradient between OXPHOS complex IV and F(0)F(1) ATP-synthase in folded mitochondrial membranes, Nat. Commun., 5, 1-7.
Kirchhoff, H., Hall, C., Wood, M., Herbstová, M., Tsabari, O., Nevo, R., Charuvi, D., Shimoni, E., and Reich, Z. (2011) Dynamic control of protein diffusion within the granal thylakoid lumen, Proc. Natl. Acad. Sci. USA, 108, 20248-20253.
Daum, B., Nicastro, D., Austin, J., McIntosh, J. R., and Kühlbrandt, W. (2010) Arrangement of photosystem II and ATP synthase in chloroplast membranes of spinach and pea, Plant Cell, 22, 1299-1312.
Takizawa, K., Cruz, J. A., Kanazawa, A., and Kramer, D. M. (2007) The thylakoid proton motive force in vivo. Quantitative, non-invasive probes, energetics, and regulatory consequences of light-induced PMF, Biochim. Biophys. Acta, 1767, 1233-1244.
Jahns, P., Latowski, D., and Strzalka, K. (2009) Mechanism and regulation of the violaxanthin cycle: the role of antenna proteins and membrane lipids, Biochim. Biophys. Acta, 1787, 3-14.
Ptushenko, V. V, Ptushenko, E. A., Samoilova, O. P., and Tikhonov, A. N. (2013) Chlorophyll fluorescence in the leaves of Tradescantia species of different ecological groups: induction events at different intensities of actinic light, Biosystems, 114, 85-97.
Bulychev, A. A., and Komarova, A. V. (2014) Long-distance signal transmission and regulation of photosynthesis in characean cells, Biochemistry (Moscow), 79, 273-281.
Krupenina, N. A., and Bulychev, A. A. (2007) Action potential in a plant cell lowers the light requirement for non-photochemical energy-dependent quenching of chlorophyll fluorescence, Biochim. Biophys. Acta, 1767, 781-788.
Szechynska-Hebda, M., Kruk, J., Górecka, M., Karpińska, B., and Karpiński, S. (2010) Evidence for light wavelength-specific photoelectrophysiological signaling and memory of excess light episodes in Arabidopsis, Plant Cell, 22, 2201-2218.
Haberlandt, G. (1888) Die Chlorophyllkörper der Selaginellen, Neubauer.
Velikanov, G. A. (2009) Stromules: their nature, structure and functions in a plant cell, Biol. Membr., 26, 468-478.
Senn, G. (1908) Die Gestalts- und Lageveränderung der Pflanzen-Chromatophoren: Mit einer Beilage: Die Lichtbrechung der Lebenden Pflanzenzelle, Engelmann, W., p. 397.
Schattat, M. H., Barton, K. A., and Mathur, J. (2015) The myth of interconnected plastids and related phenomena, Protoplasma, 252, 359-371.
Wildman, S. G., Hongladarom, T., and Honda, S. I. (1962) Chloroplasts and mitochondria in living plant cells: cinephotomicrographic studies, Science, 138, 434-436.
Menzel, D. (1994) An interconnected plastidom in Acetabularia: implications for the mechanism of chloroplast motility, Protoplasma, 179, 166-171.
Köhler, R. H., Cao, J., Zipfel, W. R., Webb, W. W., and Hanson, M. R. (1997) Exchange of protein molecules through connections between higher plant plastids, Science, 276, 2039-2042.
Kwok, E. Y., and Hanson, M. R. (2004) GFP-labelled Rubisco and aspartate aminotransferase are present in plastid stromules and traffic between plastids, J. Exp. Bot., 55, 595-604.
Kohler, R. H., and Hanson, M. R. (2000) Plastid tubules of higher plants are tissue-specific and developmentally regulated, J. Cell Sci., 113, 81-89.
Velikanov, G. A., Levanov, V. Y., Belova, L. P., Ponomareva, A. A., and Il’ina, T. M. (2012) Adjustable channel for diffusion between vacuoles of next cells: vacuolar symplast, Biol. Bull. Rev., 2, 306-317.
Robards, A. W. (1976) Plasmodesmata in higher plants, in Intercellular Communication in Plants: Studies on Plasmodesmata (Gunning, B. E. S., and Robards, A. W., eds.) Springer, pp. 15-57.
Carmody, M., and Pogson, B. (2013) Systemic photooxidative stress signalling, in Long-Distance Systemic Signaling and Communication in Plants (Baluska, F., ed.) Springer, pp. 251-274.
Hedrich, R., Salvador-Recatalà, V., and Dreyer, I. (2016) Electrical wiring and long-distance plant communication, Trends Plant Sci., 21, 376-387.
Borucki, W., Bederska, M., and Sujkowska-Rybkowska, M. (2015) Visualisation of plastid outgrowths in potato (Solanum tuberosum L.) tubers by carboxyfluorescein diacetate staining, Plant Cell Rep., 34, 853-860.
Roh, M. H., Shingles, R., Cleveland, M. J., and McCarty, R. E. (1998) Direct measurement of calcium transport across chloroplast inner-envelope vesicles, Plant Physiol., 118, 1447-1454.
Shingles, R., North, M., and McCarty, R. E. (2002) Ferrous ion transport across chloroplast inner envelope membranes, Plant Physiol., 128, 1022-1030.
Heber, U., and Heldt, H. W. (1981) The chloroplast envelope: structure, function, and role in leaf metabolism, Annu. Rev. Plant Physiol., 32, 139-168.
Carde, J. P., Joyard, J., and Douce, R. (1982) Electron microscopic studies of envelope membranes from spinach plastids, Biol. Cell, 44, 315-324.
Douce, R., and Joyard, J. (1990) Biochemistry and function of the plastid envelope, Annu. Rev. Cell Biol., 6, 173-216.
Vothknecht, U. C., and Westhoff, P. (2001) Biogenesis and origin of thylakoid membranes, Biochim. Biophys. Acta, 1541, 91-101.
Shimoni, E., Rav-Hon, O., Ohad, I., Brumfeld, V., and Reich, Z. (2005) Three-dimensional organization of higher-plant chloroplast thylakoid membranes revealed by electron tomography, Plant Cell, 17, 2580-2586.
Heldt, H. W., Werdan, K., Milovancev, M., and Geller, G. (1973) Alkalization of the chloroplast stroma caused by light-dependent proton flux into the thylakoid space, Biochim. Biophys. Acta, 314, 224-241.
Berkowitz, G. A., and Peters, J. S. (1993) Chloroplast inner-envelope ATPase acts as a primary H+ pump, Plant Physiol., 102, 261-267.
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The reported study was funded by the Russian Foundation for Basic Research (project No. 19-14-50558).
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Ptushenko, V. Electric Cables of Living Cells. I. Energy Transfer along Coupling Membranes. Biochemistry Moscow 85, 820–832 (2020). https://doi.org/10.1134/S000629792007010X
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DOI: https://doi.org/10.1134/S000629792007010X