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Energy metabolic regulation of oscillatory contraction activity in Physarum polycephalum

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Summary

The influence of inhibitors of respiration (KCN), glycolysis (2-deoxy-D-glucose alone or in combination with monoiodo-acetate) and anaerobic conditions (N2 or 95% N2 + 5% CO2), as well as the effect of application of appropriate substrates (D-glucose, sodium acetate, αketoglutarate and pyruvate) on contraction behavior (of plasmodia) of Physarum polycephalum was investigated under low intensity red-light illumination. Application of inhibitors of respiration or glycolysis leads to significantly different periods of the force oscillations (2.0±0.4 min and 4.1±0.5 min, in the presence of inhibitors of glycolysis and respiration, respectively). In both cases, the force amplitude of oscillations is diminished in comparison to undisturbed energy production. The persistence of oscillations in the presence of inhibitors of glycolysis seems to rule out an exclusively glycolytic origin of the force oscillations. A continuous production of ATP is necessary since a blockade of the energy production causes a cessation of the oscillations.

Application of substrates for respiration in the presence of inhibitors of glycolysis leads to an increase in the force amplitude and a slight prolongation of the oscillation period. In contrast, an application of glucose in the presence of a respiration inhibitor has no effect on the force amplitude and period.

It is suggested that the oscillator in Physarum represents a feedback system between (i) the contractile apparatus, (ii) the calcium regulatory system, and (iii) the energy metabolism.

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References

  • Atkinson DE (1965) Biological feedback at the molecular level. Science 150:851–857

    Google Scholar 

  • Baranowski Z, Wohlfarth-Bottermann KE (1982) Endoplasmic veins from plasmodia of Physarum polycephalum: A new strand model with defined age, structure, and behaviour. Eur J Cell Biol 27:1–9

    Google Scholar 

  • Batra S (1975) The role of mitochondria in the regulation of myoplasmic calcium concentration in smooth muscle. In: Carafoli E, Clementi F, Drabikowski W, Margreth A (eds) Calcium transport in contraction and secretion. North-Holland Publ Co, Amsterdam Oxford, pp 87–94

    Google Scholar 

  • Berridge MJ, Rapp PE (1979) A comparative survey of the function, mechanism and control of cellular oscillators. J Exp Biol 81:217–279

    Google Scholar 

  • Bershadsky AD, Gelfand VI, Svitkina TM, Tint IS (1980) Destruction of microfilament bundles in mouse embryo fibroblasts treated with inhibitors of energy metabolism. Exp Cell Res 127:421–429

    Google Scholar 

  • Block I, Wohlfarth-Bottermann KE (1981) Blue light as a medium to influence oscillatory contraction frequency in Physarum. Cell Biol Int Repts 5:73–81

    Google Scholar 

  • Borle AB (1975) Modulation of mitochondrial control of cytoplasmic calcium activity. In: Carafoli E, Clementi F, Drabikowski W, Margreth A (eds) Calcium transport in contraction and secretion. North-Holland Publ Co, Amsterdam Oxford, pp 77–86

    Google Scholar 

  • Braatz R (1975) Differential histochemical localization of calcium and its relation to shuttle streaming in Physarum. Cytobiologie 12:74–78

    Google Scholar 

  • Braatz R, Komnick H (1973) Vacuolar calcium segregation in relaxed myxomycete protoplasma as revealed by combined electrolyte histochemistry and energy dispersive analysis of X-rays. Cytobiologie 8:158–163

    Google Scholar 

  • Carafoli E, Malström K, Capano M, Sigel E, Crompton M (1975) Mitochondria and the regulation of cell calcium. In: Carafoli E, Clementi F, Drabikowski W, Margreth A (eds) Calcium transport in contraction and secretion. North-Holland Publ Co, Amsterdam Oxford, pp 53–64

    Google Scholar 

  • Chance B (1972) Transients in metabolism: An approach to the chemical mechanisms of metabolic control. In: Waterman TM, Morowitz HJ (eds) Theoretical and mathematical biology. Blaisdell Publ Co, New York, pp 334–343

    Google Scholar 

  • Erecinska M, Stubbs M, Miyata Y, Ditre CM, Wilson DF (1977) Regulation of cellular metabolism by intracellular phosphate. Biochim Biophys Acta 462:20–35

    Google Scholar 

  • Fleischer M, Wohlfarth-Bottermann KE (1975) Correlation between tension force generation, fibrillogenesis and ultrastructure of cytoplasmic actomyosin during isometric and isotonic contractions of protoplasmic strands. Cytobiologie 10:339–365

    Google Scholar 

  • Hasegawa T, Takahashi S, Hayashi H, Hatano S (1980) Fragmin: A calcium ion sensitive regulatory factor on the formation of actin filaments. Biochemistry 19:2677–2683

    Google Scholar 

  • Hess B (1979) The glycolytic oscillator. J Exp Biol 81:7–14

    Google Scholar 

  • Hinssen H (1981) An actin-modulating protein from Physarum polycephalum. II. Ca+ +-dependence and other properties. Eur J Cell Biol 23:234–240

    Google Scholar 

  • Holmes RP, Stewart PR (1979) The isolation of coupled mitochondria from Physarum polycephalum and their response to Ca2+. Biochim Biophys Acta 545:94–105

    Google Scholar 

  • Hüttermann A (1973) Biochemical events during spherule formation of Physarum polycephalum. Ber Deutsch Bot Ges 86:55–76

    Google Scholar 

  • Isenberg G, Wohlfarth-Bottermann KE (1976) Transformation of cytoplasmic actin. Importance for the organization of the contractile gel reticulum and the contraction-relaxation cycle of cytoplasmic actomyosin. Cell Tissue Res 173:495–528

    Google Scholar 

  • Kamiya N (1959) Protoplasmic streaming. Protoplasmatologia 8:1–199

    Google Scholar 

  • Kamiya N (1970) Contractile properties of the plasmodial strand. Proc Jpn Acad 46:1026–1031

    Google Scholar 

  • Kamiya N (1981) Physical and chemical basis of cytoplasmic streaming. Ann Rev Plant Physiol 32:205–236

    Google Scholar 

  • Kamiya N, Yoshimoto Y (1972) Dynamic characteristics of the cytoplasm — A study on the plasmodial strand of a myxomycete. In: Hamaguchi K (ed) Aspects of cellular and molecular physiology. Univ Tokyo Press, Tokyo, pp 167–189

    Google Scholar 

  • Kamiya N, Abe A, Nakajima H (1957) Simultaneous measurements of respiration and the motive force of protoplasmic streaming in myxomycete plasmodium II. The effect of cyanide. Proc Jpn Acad 33:407–419

    Google Scholar 

  • Kessler D (1982) Plasmodial structure and motility. In: Aldrich HC, Daniel JW (eds) Cell biology of Physarum and Didymium. Academic Press, New York London 1:145–207

    Google Scholar 

  • Korohoda W, Shraideh Z, Baranowski Z, Wohlfarth-Bottermann KE (1983) The blue light reaction of Physarum polycephalum plasmodia is coupled to respiration. Planta (in press)

  • Kuroda R, Kuroda H (1982) Relation of cytoplasmic calcium to contractility in Physarum polycephalum. J Cell Sci 53:37–48

    Google Scholar 

  • Kuźnicki J, Kuźnicki L, Drabikowski W (1978) Ca++-binding modulator protein in protozoa and myxomycete. Cell Biol Int Repts 3:17–23

    Google Scholar 

  • Lehninger AL (1975) Biochemistry (2nd ed) Worth Publishers, New York, Inc.

  • Matveeva NB, Beylina SI, Teplov VA, Layrand DB (1978) Chemotactic and proton responses of the slime mold Physarum polycephalum to non-metabolizable glucose analogues. Acta Protozool 18:173–176

    Google Scholar 

  • Michejda J, Domka-Popek A, Hryniewiecka L (1982) Energetic competence of the alternative respiratory pathway in Amoeba, Acanthamoeba castellanii. Biol of the Cell 45 (522):223

    Google Scholar 

  • Mito Y, Kurihara K, Kobatake Y (1980) Selective suppression of positive chemotaxis in Physarum polycephalum by treatment with rotenone or under anaerobic condition. Eur J Cell Biol 21:43–47

    Google Scholar 

  • Nagai R, Yoshimoto Y, Kamiya N (1978) Cyclic production of tension force in the plasmodial strand of Physarum polycephalum and its relation to microfilament morphology. J Cell Sci 33:205–225

    Google Scholar 

  • Ogihara S (1982) Calcium and ATP regulation of the oscillatory torsional movement in a triton model of Physarum plasmodial strands. Exp Cell Res 138:377–384

    Google Scholar 

  • Ohta J (1952) Experimental studies on the protoplasmic streaming in the myxomycete plasmodium. II. The effects of some respiratory poisons and reduced oxygen tension on the motive force of protoplasmic streaming. Cytologia 17:300–310

    Google Scholar 

  • Racker E (1976) Why do tumour cells have a high aerobic glycolysis? J Cell Physiol 89:697–700

    Google Scholar 

  • Rasmussen H, Bikle DD (1975) Calcium and non-vesicular secretion in the kidney: calcium and mitochondrial function. In: Carafoli E, Clementi F, Drabikowski W, Margreth A (eds) Calcium transport in contraction and secretion. North-Holland Publ Co, Amsterdam Oxford, pp 111–121

    Google Scholar 

  • Ridgway EB, Durham ACH (1976) Oscillations of calcium ion concentrations in Physarum polycephalum. J Cell Biol 69:223–226

    Google Scholar 

  • Sachsenmaier W, Hansen K (1973) Long and short period oscillations in a myxomycete with synchronous nuclear divisions. In: Chance B, Pye EK, Ghosh AK, Hess B (eds) Biological and biochemical oscillators. Academic Press, New York London, pp 429–447

    Google Scholar 

  • Samans KE, Götz von Olenhusen K, Wohlfarth-Bottermann KE (1978) Oscillating contractions in protoplasmic strands of Physarum. Infrared reflexion as a non-invasive registration technique. Cell Biol Int Repts 2:271–277

    Google Scholar 

  • Satoh H, Ueda T, Kobatake Y (1982) Primary oscillator of contractional rhythm in the plasmodium of Physarum polycephalum: Role of mitochondria. Cell Structure and Function 7:275–283

    Google Scholar 

  • Seppälä AJ, Wikström MKF, Saris NEL (1973) Damping of mitochondrial volume oscillations by propranolol and related compounds. In: Chance B, Pye EK, Ghosh AK, Hess B (eds) Biological and biochemical oscillator. Academic Press, New York London, pp 115–124

    Google Scholar 

  • Solomos T (1977) Cyanide-resistant respiration in higher plants. Ann Rev Plant Physiol 28:279–297

    Google Scholar 

  • Teplov VA, Beylina SI, Layrand DB, Matveeva NB (1978) Contractile properties of plasmodium strand models. Acta Protozool 18:209–211

    Google Scholar 

  • Teplov VA, Matveeva NB, Zinchenko VP (1973) Free calcium level oscillation in myxomycete plasmodium during protoplasmic shuttle streaming (in Russian) In Frank GM, Karnaukhov NV (eds) Biophysics of living cell. Pushchino, 4:110–115

  • Termonia Y, Ross J (1981) Oscillations and control features in glycolysis: Numerical analysis of a comprehensive model. Proc Natl Acad Sci, USA 78:2952–2956

    Google Scholar 

  • Tyson JJ (1982) Periodic phenomena in Physarum. In: Aldrich HC, Daniel JW (eds) Cell biology of Physarum and Didymium. Academic Press, New York London, 1:61–110

    Google Scholar 

  • Ueda T, Kobatake Y (1982) Chemotaxis in plasmodia of Physarum polycephalum. In: Aldrich HC, Daniel JW (eds) Cell biology of Physarum and Didymium. Academic Press, New York London, 1:111–143

    Google Scholar 

  • Ueda T, Götz von Olenhusen K, Wohlfarth-Bottermann KE (1978) Reactions of the contractile apparatus in Physarum to injected Ca++, ATP, ADP and 5′-AMP. Cytobiologie 18:76–94

    Google Scholar 

  • Wohlfarth-Bottermann KE (1962) Weitreichende, fibrilläre Protoplasmadifferenzierungen und ihre Bedeutung für die Protoplasmaströmung. I. Elektronenmikroskopischer Nachweis und Feinstruktur. Protoplasma 54:514–539

    Google Scholar 

  • Wohlfarth-Bottermann KE (1963) Weitreichende, fibrilläre Protoplasmadifferenzierungen und ihre Bedeutung für die Protoplasmaströmung. II. Lichtmikroskopische Darstellung. Protoplasma 57:747–761

    Google Scholar 

  • Wohlfarth-Bottermann KE (1975a) Tensiometric demonstration of endogenous oscillating contractions in plasmodia of Physarum polycephalum. Z Pflanzenphysiol 76:14–27

    Google Scholar 

  • Wohlfarth-Bottermann KE (1975b) Weitreichende fibrilläre Protoplasmadifferenzierungen und ihre Bedeutung für die Protoplasmaströmung. X. Die Anordnung der Actomyosinfibrillen in experimentell unbeeinflußten Protoplasmaadern von Physarum in situ. Protistologica XI:19–30

    Google Scholar 

  • Wohlfarth-Bottermann KE (1979a) Contraction phenomena in Physarum: New results. Acta Protozool 18:59–73

    Google Scholar 

  • Wohlfarth-Bottermann KE (1979b) Oscillatory contraction activity in Physarum. J Exp Biol 81:15–32

    Google Scholar 

  • Wohlfarth-Bottermann KE, Achenbach F (1982) Lateral apertures as passage-ways between ectoplasm and endoplasm in plasmodial strands of Physarum. Cell Biol Int Repts 6:57–61

    Google Scholar 

  • Yamazaki I, Yokota K (1973) A siphon model for oscillatory reactions in the reduced pyridine nucleotide, O2 and peroxidase system. In: Chance B, Pye EK, Ghosh AK, Hess B (eds) Biological and biochemical oscillators. Academic Press, New York London, pp 109–114

    Google Scholar 

  • Yoshimoto Y, Kamiya N (1982) Ca2+ oscillation in the homogenate of Physarum plasmodium. Protoplasma 110:63–65

    Google Scholar 

  • Yoshimoto Y, Sakai T, Kamiya N (1981) ATP oscillation in Physarum plasmodium. Protoplasma 109:159–168

    Google Scholar 

  • Yoshimoto Y, Matsumura F, Kamiya N (1982) Simultaneous oscillations of Ca2+ efflux and tension generation in the permealized plasmodial strand of Physarum. Cell Motility 1:433–443

    Google Scholar 

  • Zubrzycka-Gaarn E, Korczak B, Osinska HE (1979) Identification of sarcoplasmic reticulumlike system in Physarum polycephalum. FEBS Letters 107 (2):335–339

    Google Scholar 

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Send offprint requests to: Institute of Cytology, University of Bonn, Ulrich-Haberland-Straße 61a, D-5300 Bonn 1, Federal Republic of Germany

Supported by the Deutsche Forschungsgemeinschaft as a Guest Professor at the University of Bonn

Supported by a fellowship from the Deutscher Akademischer Austauschdienst

Supported by a fellowship from the Alexander von Humboldt Stiftung

The authors wish to thank Dr. R.L. Snipes (Giessen) for reading the manuscript and Mrs. B. Koeppen for technical assistance

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Korohoda, W., Shraideh, Z., Baranowski, Z. et al. Energy metabolic regulation of oscillatory contraction activity in Physarum polycephalum . Cell Tissue Res. 231, 675–691 (1983). https://doi.org/10.1007/BF00218125

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