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Impact of salt adaptation on esterified fatty acids and cytochrome oxidase in plasma and thylakoid membranes from the cyanobacterium Anacystis nidulans

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Abstract

During adaptation of photoautotrophically growing fresh water cyanobacterium Anacystis nidulans to high salinity the cells showed a pronounced increase of proton-sodium antiporter activity, and of cytochrome c oxidase in isolated and purified plasma membrane. At the same time the concentrations of plasma membrane-bound EDTA-resistant copper and iron (determined by inductively coupled plasma atomic emission spectrometry) rose proportionately, accompanied by an increase in whole cell respiration. In plasma membranes from salt adapted cells lipid/protein ratios were markedly higher than in control cells, levels of esterified saturated and long-chain fatty acids being significantly higher than the respective levels of unsaturated and short-chain fatty acids which explains the higher lipid-phase transition temperatures derived from Arrhenius plots. Immunoblotting of the membrane proteins with antisera raised against the cytochrome c oxidases from Paracoccus denitrificans and A. nidulans gave two cross-reacting bands with apparent molecular weights around 50000 and 30000 (subunits I and II, respectively) which were more pronounced in plasma membranes from salt adapted cells when compared to control cells. The protein pattern of plasma membranes from salt adapted cells also showed the appearance of bands at apparent molecular weights of 44000–48000 and 54000–56000 which might stem from the proton/sodium-antiporter in this membrane.

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Abbreviations

CM:

cytoplasmic or plasma membrane

ICM:

intracytoplasmic or thylakoid membrane

cyt:

cytochrome

DCCD:

N,N′-dicyclohexylcarbodiimide

Hepes:

N-2-hydroxyethylpiperazine-N′-2-ethanesulfonate

ICP-AES:

inductively coupled plasma atomic emission spectrometry

SDS-PAGE:

sodium dodecylsulfate polyacrylamide gel electrophoresis

EPR:

electron paramagnetic resonance spectrometry

References

  • Azaria-Gabay R, Tel-Or E, Schonfeld M (1988) Mechanisms of salt tolerance in the marine cyanobacterium Spirulina subsalsa. In: Mur LR, Burger-Wiersma T (eds) Abstr. 6th International Symposium on Phototrophic Prokaryotes. Noordwijkerhout, The Netherlands, p 155

  • Bishop DG, Kenrick JR, Bayston JH, MacPherson AS, Johns SR (1980) Monolayer properties of chloroplast lipids. Biochim Biophys Acta 602:248–259

    Google Scholar 

  • Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917

    Google Scholar 

  • Blumwald E, Tel-Or E (1982a) Structural aspects of the Nostoc muscorum to salt. Arch Microbiol 132:163–167

    Google Scholar 

  • Blumwald E, Tel-Or E (1982b) Osmoregulation and cell composition in salt adaptation of Nostoc muscorum. Arch Microbiol 132: 168–172

    Google Scholar 

  • Blumwald E, Mehlhorn RJ, Packer L (1983a) Studies of osmoregulation in salt adaptation of cyanobacteria with ESR spin probe techniques. Proc Natl Acad Sci USA 80: 2599–2602

    Google Scholar 

  • Blumwald E, Mehlhorn RJ, Packer L (1983b) Ionic osmoregulation during salt adaptation of the cyanobacterium Synechococcus 6311. Plant Physiol 73:377–380

    Google Scholar 

  • Blumwald E, Wolosin JM, Packer L (1984) Na+/H+ exchange in the cyanobacterium Synechococcus 6311. Biochem Biophys Res Commun 122:452–459

    Google Scholar 

  • Boumans PWJM (1987) Inductively coupled plasma emission spectroscopy. John Wiley & Sons, New York

    Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Google Scholar 

  • Brock TD (1973) Evolutionary and ecological aspects of the cyanophytes. In: Carr NG, Whitton BA (eds) The biology of blue-green algae, 1st edn. Blackwell, Oxford, pp 487–500

    Google Scholar 

  • Broda E (1975) The evolution of the bioenergetic processes. Pergamon Press, Oxford

    Google Scholar 

  • De Boor C (1978) A practical guide to splines. Applied mathematical sciences, vol 27. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Erber WWA (1988) Charakterisierung und Identifizierung des Na+/H+-Antiports bei Cyanobakterien. Doctoral Thesis, University of Vienna, Austria

  • Erber WWA, Nitschmann WH, Muchl R, Peschek GA (1986) Endogenous energy supply to the plasma membrane of dark aerobic cyanobacterium Anacystis nidulans: ATPase-independent efflux of H+ and Na+ from respiring cells. Arch Biochem Biophys 247:28–39

    Google Scholar 

  • Erber WWA, Obinger C, Peschek GA (1988) Amiloride-sensitive sodium-proton antiport in cyanobacteria: Interplay with respiration and role for salt adaptation. In Mur LR, Burger-Wiersma T (eds) Abstr. 6th International Symposium on Phototrophic Prokaryotes. Noordwijkerhout, The Netherlands, p 152

  • Fry IV, Peschek GA, Huflejt M, Packer L (1985) EPR signals of redox-active copper in EDTA washed membranes from the cyanobacterium Synechococcus 6311. Biochem Biophys Res Commun 129:109–116

    Google Scholar 

  • Fry IV, Huflejt M, Erber WWA, Peschek GA, Packer L (1986) The role of respiration during adaptation of the freshwater cyanobacterium Synechococcus 6311 to salinity. Arch Biochem Biophys 244:686–691

    Google Scholar 

  • Ho KK, Krogmann DW (1982) Photosynthesis. In Carr NG, Whitton BA (eds) The biology of cyanobacteria, 2nd edn. Blackwell, Oxford, pp 191–214

    Google Scholar 

  • Hunter DR, Capaldi RA (1974) Respiratory control in cytochrome oxidase. Biochem Biophys Res Commun 56:623–630

    Google Scholar 

  • Kratz WA, Myers J (1955) Nutrition and growth of several blue-green algae. Am J Bot 42:282–287

    Google Scholar 

  • Ludwig B, Schatz G (1980) A two-subunit cytochrome c oxidase from Paracoccus denitrificans. Proc Natl Acad Sci USA 77:196–200

    Google Scholar 

  • Mackinney G (1941) Absorption of light by chlorophyll solutions. J Biol Chem 140:315–322

    Google Scholar 

  • Molitor V, Erber WWA, Peschek GA (1986a) Increased levels of cytochrome oxidase and sodium-proton antiporter in the plasma membrane of Anacystis nidulans after growth in sodium-enriched media. FEBS Lett 204:251–256

    Google Scholar 

  • Molitor V, Kuntner O, Peschek GA (1986b) Different levels of cytochrome c oxidase in plasma and thylakoid membranes of Anacystis nidulans as related to growth phase and medium salinity. In: EBEC Reports, vol 4. Prague, Czechoslovakia, p 187

  • Molitor V, Trnka M, Peschek GA (1987) Isolated and purified plasma and thylakoid membranes of the cyanobacterium Anacystis nidulans contain immunologically cross-reactive aa3-type cytochrome oxidase. Curr Microbiol 14:263–268

    Google Scholar 

  • Murata N, Nishida I (1987) Lipids of blue-green algae (cyanobacteria). In Stumpf PK (ed) The biochemistry of plants. Academic Press, New York, pp 315–347

    Google Scholar 

  • Nitschmann WH, Peschek GA (1985) Modes of proton translocation across the cell membrane of respiring cyanobacteria. Arch Microbiol 141:330–336

    Google Scholar 

  • Nitschmann WH, Peschek GA (1986) Oxidative phosphorylation and energy buffering in cyanobacteria. J Bacteriol 168:1205–1211

    Google Scholar 

  • Ono T, Murata N (1979) Temperature dependence of the photosynthetic activities in the thylakoid membranes from the blue-green algae Anacystis nidulans. Biochim Biophys Acta 545:69–76

    Google Scholar 

  • Peschek GA, Schmetterer G (1981) Effects of lipids on the membrane-bound cytochrome oxidase of cyanobacteria. Naturwissenschaften 68:575

    Google Scholar 

  • Peschek GA, Muchl R, Schmetterer G (1981) Temperature dependence of horse heart cytochrome c oxidase by membrane preparations of Anacystis nidulans: Characterization of two distinct Arrhenius discontinuities. Curr Microbiol 6:233–237

    Google Scholar 

  • Peschek GA, Muchl R, Kienzl PF, Schmetterer G (1982) Characteristic temperature dependence of respiratory and photosynthetic electron transport activities in membrane preparations from Anacystis nidulans grown at different temperatures. Biochim Biophys Acta 679:35–43

    Google Scholar 

  • Peschek GA, Nitschmann WH, Czerny T (1988a) Respiratory proton extrusion and plasma membrane energization. Methods Enzymol 167:361–379

    Google Scholar 

  • Peschek GA, Molitor V, Trnka M, Wastyn M, Erber WWA (1988b) Characterization of cytochrome c oxidase in isolated and purified plasma and thylakoid membranes from cyanobacteria. Methods Enzymol 167:437–449

    Google Scholar 

  • Peschek GA, Wastyn M, Trnka M, Molitor V, Fry IV, Packer L (1989a) Characterization of the cytochrome c oxidase in isolated and purified plasma membranes from the cyanobacterium Anacystis nidulans. Biochemistry 28:3057–3063

    Google Scholar 

  • Peschek GA, Wastyn M, Molitor V, Trnka M, Kraushaar H, Obinger C, Matthijs HCP (1989b) Self-contained or accessory respiration in the phototrophic cyanobacteria (blue-green algae)? In: Kotyk A, Skoda J, Paces V, Kosta V (eds). Highlights of modern biochemistry. VSP International Science Publishers, Zeist, The Netherlands, pp 893–902

    Google Scholar 

  • Peschek GA, Hinterstoisser B, Wastyn M, Kuntner O, Pineau B, Missbichler A, Lang J (1989c) Chlorophyll precursors in the plasma membrane of a cyanobacterium, Anacystis nidulans. J Biol Chem 264:11827–11832

    Google Scholar 

  • Reed RH, Richardson DL, Stewart WDP (1985) Na+ uptake and extrusion in the cyanobacterium Synechocystis PCC 6714 in response to hypersaline treatment. Evidence for transient changes in plasmalemma Na+ permeability. Biochim Biophys Acta 814:347–355

    Google Scholar 

  • Scherer S, Stürzl E, Böger P (1984) Oxygen-dependent proton efflux in cyanobacteriua (blue-green algae). J Bacteriol 158:609–614

    Google Scholar 

  • Stanier RY, Cohen-Bazire G (1977) Phototrophic prokaryotes: The cyanobacteria. Ann Res Microbiol 31:225–274

    Google Scholar 

  • Trnka M, Peschek GA (1986) Immunological identification of aa3-type cytochrome oxidase in membrane preparations of the cyanobacterium Anacystis nidulans. Biochem Biophys Res Commun 136:235–241

    Google Scholar 

  • Villereal ML (1986) Na+−H+ and Na+−Ca2+ exchange in activated cells. Curr Top Membranes and Transport 27:55–88

    Google Scholar 

  • Wada H, Hirasawa R, Omata T, Murata N (1984) The liquid phase of thylakoid and cytoplasmic membranes from the blue-green algae (cyanobacteria) Anacystic nidulans and Anabaena variabilis. Plant Cell Physiol 25:907–911

    Google Scholar 

  • Wastyn M, Achatz A, Trnka M, Peschek GA (1987) Immunological and spectral characterization of partly purified cytochrome oxidase from the cyanobacterium Synechocystis 6714. Biochem Biophys Res Commun 149:102–111

    Google Scholar 

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Molitor, V., Trnka, M., Erber, W. et al. Impact of salt adaptation on esterified fatty acids and cytochrome oxidase in plasma and thylakoid membranes from the cyanobacterium Anacystis nidulans . Arch. Microbiol. 154, 112–119 (1990). https://doi.org/10.1007/BF00423319

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  • DOI: https://doi.org/10.1007/BF00423319

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