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Cellular and Molecular Biology Letters

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Volume 20, Issue 5

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Non-cooperative immobilization of residual water bound in lyophilized photosynthetic lamellae

Hubert Harańczyk
  • Corresponding author
  • Institute of Physics, Jagiellonian University, ul. Prof. Stanisława Łojasiewicza 11, 30-348 Kraków, Poland
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/ Ewelina Baran
  • Institute of Physics, Jagiellonian University, ul. Prof. Stanisława Łojasiewicza 11, 30-348 Kraków, Poland
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/ Piotr Nowak
  • Institute of Physics, Jagiellonian University, ul. Prof. Stanisława Łojasiewicza 11, 30-348 Kraków, Poland
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/ Małgorzata Florek-Wojciechowska
  • Institute of Physics, Jagiellonian University, ul. Prof. Stanisława Łojasiewicza 11, 30-348 Kraków, Poland
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/ Anna Leja
  • Institute of Physics, Jagiellonian University, ul. Prof. Stanisława Łojasiewicza 11, 30-348 Kraków, Poland
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/ Dorota Zalitacz
  • Institute of Physics, Jagiellonian University, ul. Prof. Stanisława Łojasiewicza 11, 30-348 Kraków, Poland
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/ Kazimierz Strzałka
  • Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, ul. Gronostajowa 7, 30-387 Kraków, Poland
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Published Online: 2016-03-05 | DOI: https://doi.org/10.1515/cmble-2015-0040

Abstract

This study applied 1H-NMR in time and in frequency domain measurements to monitor the changes that occur in bound water dynamics at decreased temperature and with increased hydration level in lyophilizates of native wheat photosynthetic lamellae and in photosynthetic lamellae reconstituted from lyophilizate. Proton relaxometry (measured as free induction decay = FID) distinguishes a Gaussian component S within the NMR signal (o). This comes from protons of the solid matrix of the lamellae and consists of (i) an exponentially decaying contribution L1 from mobile membrane protons, presumably from lipids, and from water that is tightly bound to the membrane surface and thus restricted in mobility; and (ii) an exponentially decaying component L2 from more mobile, loosely bound water pool. Both proton relaxometry data and proton spectroscopy show that dry lyophilizate incubated in dry air, i.e., at a relative humidity (p/p0) of 0% reveals a relatively high hydration level. The observed liquid signal most likely originates from mobile membrane protons and a tightly bound water fraction that is sealed in pores of dry lyophilizate and thus restricted in mobility. The estimations suggest that the amount of sealed water does not exceed the value characteristic for the main hydration shell of a phospholipid. Proton spectra collected for dry lyophilizate of photosynthetic lamellae show a continuous decrease in the liquid signal component without a distinct freezing transition when it is cooled down to -60ºC, which is significantly lower than the homogeneous ice nucleation temperature [Bronshteyn, V.L. et al. Biophys. J. 65 (1993) 1853].

Keywords: Wheat photosynthetic lamellae; Membrane lyophilizate; Bound water fractions; Bound water freezing; Bound water overcooling; 1H-NMR relaxometry; 1H-NMR spectroscopy; FID moment expansion; Thylakoid lyophilizate molecular mobility; CPMG

References

  • 1. Singer, S.J. and Nicolson, G.L. The fluid mosaic model of the structure of cell membranes. Science 175 (1972) 720-731.Google Scholar

  • 2. Luzzati, V. and Tardieu, A. Lipid phases: structure and structural transitions. Annu. Rev. Phys. Chem. 25 (1974) 79-94.CrossrefGoogle Scholar

  • 3. Pralle, A., Keller, P., Florin, E.L., Simons, K. and Hörber, J.K.H. Sphingolipid-cholesterol rafts diffuse as small entities in the plasma membrane of mammalian cells. J. Cell Biol. 148 (2000) 997-1008.Google Scholar

  • 4. Simons, K. and Ikonen, E. Functional rafts in cell membranes. Nature 387 (1997) 569-572.Google Scholar

  • 5. Anderson, R.G. and Jacobson, K. A role for lipid shells in targeting proteins to caveolae, rafts, and other lipid domains. Science 296 (2003) 1821-1825.Google Scholar

  • 6. Mayor, S. and Rao, M. Rafts: scale-dependent, active lipid organization at the cell surface. Traffic 5 (2004) 231-240.CrossrefGoogle Scholar

  • 7. Maxfield, F.R. Plasma membrane microdomains. Curr. Opin. Cell Biol. 14 (2002) 483-487.CrossrefGoogle Scholar

  • 8. Subczynski, W.K. and Kusumi, A. Dynamics of raft molecules in the cell and artificial membranes: approaches by pulse EPR spin labelling and single molecule optical microscopy. Biochim. Biophys. Acta 1610 (2003) 231-243.Google Scholar

  • 9. Harańczyk, H., Bacior, M., Jamróz, J., Jemioła-Rzemińska, M., and Strzałka, K. Rehydration of DGDG (digalactosyl diacylglicerol) model membrane lyophilizates observed by NMR and sorption isotherm. Acta Phys. Polon. A 115 (2009) 521-525.Google Scholar

  • 10. Latowski, D., Kruk, J., Burda, K., Skrzynecka-Jaskier, M., Kostecka- Gugała, A. and Strzałka, K. Kinetics of violaxanthin de-epoxidation by violaxanthin de-epoxidase, a xanthophyll cycle enzyme, is regulated by membrane fluidity in model lipid bilayers. Eur. J. Biochem. 269 (2002) 4656-4665.Google Scholar

  • 11. Latowski, D., H.-E. Akerlund, H.-E. and Strzalka, K. Violaxanthin deepoxidase, the xanthophyll cycle enzyme, requires lipid inverted hexagonal structures for its activity. Biochemistry 43 (2004) 4417-4420.CrossrefGoogle Scholar

  • 12. Krumova, S.B., Dijkema, C., de Waard, P., Van As, H., Garab, G. and van Amerongen, H. Phase behavior of phosphatidylglycerol in spinach thylakoid membranes as revealed by 31 P-NMR. Biochim. Biophys. Acta 1778 (2008) 997-1003.Google Scholar

  • 13. Liljenberg, C.S. The effects of water deficit stress on plant membrane lipids. Prog. Lipid Res. 31 (1992) 335-343.CrossrefGoogle Scholar

  • 14. Harańczyk, H., Strzałka, K., Bayerl, T., Klose, G. and Blicharski, J.S. 31P-NMR measurements in photosynthetic membranes of wheat. Photosynthetica 19 (1985) 414-416.Google Scholar

  • 15. Harańczyk, H., Strzałka, K., Dietrich, W. and Blicharski, J.S. 31P-NMR observation of the temperature and glycerol induced non-lamellar phase formation in wheat thylakoid membranes. J. Biol. Phys. 21 (1995) 125-139.CrossrefGoogle Scholar

  • 16. Harańczyk, H., Leja, A., Jemioła-Rzemińska, M. and Strzałka, K. Maturation processes of photosynthetic membranes observed by proton magnetic relaxation and sorption isotherm. Acta Phys. Polon. A 115 (2009) 526-532.Google Scholar

  • 17. Harańczyk, H., Leja, A. and Strzałka, K. The effect of water accessible paramagnetic ions on subcellular structures formed in developing wheat photosynthetic membranes as observed by NMR and by sorption isotherm. Acta Phys. Polon. A 109 (2006) 389-398.Google Scholar

  • 18. Strzałka, K., Majewska, G. and Mędrela, E. Effects of chloramphenicol and cyclohemixide on the relative content of chlorophyll and protein in various subchloroplast fractions. Acta Physiol. Plant. 11 (1980) 49-59.Google Scholar

  • 19. Gaff, D.F. Desiccation tolerant vascular plants of Southern Africa. Oecologia (Berl.) 31 (1977) 95-109.CrossrefGoogle Scholar

  • 20. Węglarz, W. and Harańczyk, H. Two-dimensional analysis of the nuclear relaxation function in the time domain: the program CracSpin. J. Phys. D: Appl. Phys. 33 (2000) 1909-1920.CrossrefGoogle Scholar

  • 21. Abragam, A. The principles of nuclear magnetism. Oxford University Press, London (1961).Google Scholar

  • 22. Strzalka, K. and Subczynski, W.K. Formation of the thylakoid membranes in greening leaves and their modification by protein synthesis inhibitors. II. A spin label study of membrane lipid mobility. Photobiochemistry and Photobiophysics 2 (1981) 227-232.Google Scholar

  • 23. Strzalka, K. and Machowicz, E. Effect of chloramphenicol and cycloheximide on the fatty acid composition in various thylakoid lipid fractions in greening wheat seedlings. Acta Physiol. Plant. 6 (1984) 41-49.Google Scholar

  • 24. Harańczyk, H., Węglarz, W.P. and Sojka, S. The investigation of hydration processes in horse chestnut (Aesculus hippocastanum, L.) and pine (Pinus silvestris, L.) bark and bast using proton magnetic relaxation. Holzforschung 53 (1999) 299-310.Google Scholar

  • 25. Harańczyk, H., Nowak, P., Bacior, M., Lisowska, M., Marzec, M., Florek M. and Olech, M.A. Bound water freezing in Umbilicaria aprina from continental Antarctica. Antarctic Sci. 24 (2012) 342-352.CrossrefGoogle Scholar

  • 26. Harańczyk, H., Pater, Ł., Nowak, P., Bacior, M. and Olech, M.A. Initial phases of Antarctic Ramalina terebrata Hook f. & Taylor thalli rehydration observed by proton relaxometry. Acta Phys. Polon. A 121 (2012) 480-484.Google Scholar

  • 27. Harańczyk, H., Bacior, M. and Olech M.A. Deep dehydration of Umbilicaria aprina thalli observed by proton NMR and sorption isotherm. Antarctic Sci. 20 (2008) 527-535.CrossrefGoogle Scholar

  • 28. Harańczyk, H. On water in extremely dry biological systems. Jagielonian University Press, Kraków, 2003.Google Scholar

  • 29. Harańczyk, H., Florek, M., Nowak, P. and Knutelski, S. Water bound in elytra of the weevil Liparus glabrirostris (Küster, 1849) by NMR and sorption isotherm (Coleoptera: Curculionidae). Acta Phys. Polon. A 121 (2012) 491-496. Google Scholar

  • 30. Zalitacz, D., Harańczyk, H., Nowak, P. and Delong, P. Mild hydration effect on bound-water dynamics in human hair monitored by H-1-NMR. J. Invest. Dermatol. 133 (2013) 1424.Google Scholar

  • 31. Funduk, N., Lahajnar, G., Miljković, L., Skočajić, S., Kydon, D.W., Schreiner, L.J. and Pintar, M.M. A com parative NMR study of proton groups in dentin of 20 and 50 years old donors. Zobozdrav. Vestn. 41 (Suppl.1) (1986) 139-160.Google Scholar

  • 32. Pintar, M.M. Some considerations of the round table subject. Magn. Reson. Imaging 9 (1991) 753-754.CrossrefGoogle Scholar

  • 33. Harańczyk, H., Soga, K.G., Rumm, R.J. and Pintar, M.M. Can we see, by proton spin relaxation, a percolation transition upon drying controlled pore size glass?. Magn. Reson. Imaging 9 (1991) 723-726.CrossrefGoogle Scholar

  • 34. Schreiner, L.J., Cameron, I.G., Funduk N., Miljković, L., Pintar, M.M. and Kydon, D.N. Proton NMR spin grouping and exchange in dentin. Biophys. J. 59 (1991) 629-639.CrossrefGoogle Scholar

  • 35. Carr, H.Y. and Purcell, E.M. Effects of diffusion on free precession in nuclear magnetic resonance experiments. Phys. Rev. 94 (1954) 630-638.CrossrefGoogle Scholar

  • 36. Meiboom, S. and Gill, D. Modified spinecho method for measuring nuclear relaxation times. Rev. Sci. Instrum. 29 (1958) 688-691.CrossrefGoogle Scholar

  • 37. MacKay, A.L. A Proton NMR moment study of the gel and liquid-crystalline phases of dipalmitoyl phosphatidylcholine. Biophys. J. 35 (1981) 301-313.CrossrefGoogle Scholar

  • 38. Zimmerman, J.R. and Brittin, W.E. Nuclear magnetic resonance studies in multiple phase systems: lifetime of a water molecule in an adsorbing phase on silica gel. J. Phys. Chem. 61 (1957) 1328-1333.CrossrefGoogle Scholar

  • 39. Robinson, H.H., Sharp, R.R. and Yocum, C.F. Effect of manganese on the nuclear magnetic relaxivity of water protons in chloroplast suspensions. Biochem. Biophys. Res. Commun. 93 (1980) 755-761.CrossrefGoogle Scholar

  • 40. Sharp, R.R. and Yocum, C.F. Field-dispersion profiles of the proton spinlattice relaxation rate in chloroplast suspensions. Effect of manganese extraction by EDTA, Tris and hydroxylamine. Biochim. Biophys. Acta 592 (1980) 185-195.Google Scholar

  • 41. Wydrzynski, T.J., Marks, S.B., Schmidt, P.G., Govindjee, and Gutowsky, H.S. Nuclear magnetic relaxation by the manganese in aqueous suspensions of chloroplasts. Biochemistry 17 (1978) 2155-2162.CrossrefGoogle Scholar

  • 42. Wydrzynski, T.J., Zumbulyadis, N., Schmidt, P.G. and Govindjee, Water proton relaxation as a monitor of membrane- bound manganese in spinach chloroplasts. Biochim. Biophys. Acta 408 (1975) 349-354.Google Scholar

  • 43. Cheniae, G.M. Photosystem II and O2 Evolution. Annu. Rev. Plant Physiol. 21 (1970) 467-498.CrossrefGoogle Scholar

  • 44. Cheniae, G.M. and Martin, I.F. Effects of hydroxylamine on photosystem II: I. Factors affecting the decay of O2 evolution. Annu. Rev. Plant Physiol. 47 (1971) 568-575. CrossrefGoogle Scholar

  • 45. Murthy, N.S. and Worthington, C.R. X-ray diffraction evidence for the presence of discrete water layers on the surface of membranes. Biochim. Biophys. Acta 1062 (1991) 172-176.Google Scholar

  • 46. Wolfe, J., Bryant, G., Koster, K.L. What is “unfreezable water”, how unfreezable is it and how much is there? Cryo Letters 23 (2002) 157-166.Google Scholar

  • 47. Bronshteyn, V.L. and Steponkus, P.L. Calorimetric studies of freeze-induced dehydration of phospholipids. Biophys. J. 65 (1993) 1853-1865.CrossrefGoogle Scholar

  • 48. Vladkova, R., Koynova, R., Teuchner, K. and Tenchov, B. Bilayer structural destabilization by low amounts of chlorophyll a. Biochim. Biophys. Acta 1798 (2010) 1586-1592.Google Scholar

  • 49. Szilagyi, A., Sommarin, M. and Akerlund, H.E. Membrane curvature stress controls the maximal conversion of violaxanthin to zeaxanthin in the violaxanthin cycle - influence of α-tocopherol, cetylethers, linolenic acid, and temperature. Biochim. Biophys. Acta 1768 (2007) 2310-2318.Google Scholar

  • 50. Garab, G. Hierarchical organization and structural flexibility of thylakoid membrane. Biochim. Biophys. Acta 1837 (2014) 481-494.Google Scholar

  • 51. Klose, G. and Gawrisch, K. Lipid water interaction in model membranes. Stud. Biophys. 84 (1981) 21-22.Google Scholar

  • 52. Bahl, J., Franckie, B. and Moneger, R. Lipid composition of envelopes, prolamellar bodies and other plastid membranes in etiolated, green and greening wheat leaves. Planta 129 (1976) 193-201. Google Scholar

About the article

Received: 2015-03-19

Accepted: 2015-09-16

Published Online: 2016-03-05

Published in Print: 2015-12-01


Citation Information: Cellular and Molecular Biology Letters, Volume 20, Issue 5, Pages 717–735, ISSN (Online) 1689-1392, DOI: https://doi.org/10.1515/cmble-2015-0040.

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