Home Non-cooperative immobilization of residual water bound in lyophilized photosynthetic lamellae
Article
Licensed
Unlicensed Requires Authentication

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

  • Hubert Harańczyk EMAIL logo , Ewelina Baran , Piotr Nowak , Małgorzata Florek-Wojciechowska , Anna Leja , Dorota Zalitacz and Kazimierz Strzałka
Published/Copyright: March 5, 2016
Become an author with De Gruyter Brill

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].

References

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

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

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

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

7. Maxfield, F.R. Plasma membrane microdomains. Curr. Opin. Cell Biol. 14 (2002) 483-487.10.1016/S0955-0674(02)00351-4Search in Google 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.Search in 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.Search in 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.Search in 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.Search in Google 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.Search in Google Scholar

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

19. Gaff, D.F. Desiccation tolerant vascular plants of Southern Africa. Oecologia (Berl.) 31 (1977) 95-109.Search in Google 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) 1909-1920.10.1088/0022-3727/33/15/322Search in Google Scholar

21. Abragam, A. The principles of nuclear magnetism. Oxford University Press, London (1961).10.1063/1.3057238Search in 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.Search in 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.Search in 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.Search in 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.Search in Google 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.Search in 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.Search in Google Scholar

28. Harańczyk, H. On water in extremely dry biological systems. Jagielonian University Press, Kraków, 2003.Search in 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. 10.12693/APhysPolA.121.491Search in 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.Search in 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.Search in Google Scholar

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

36. Meiboom, S. and Gill, D. Modified spinecho method for measuring nuclear relaxation times. Rev. Sci. Instrum. 29 (1958) 688-691.Search in Google 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.Search in Google 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.Search in Google 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.Search in Google 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) 185-195.10.1016/0005-2728(80)90124-3Search in 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.Search in Google 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.Search in Google Scholar

43. Cheniae, G.M. Photosystem II and O2 Evolution. Annu. Rev. Plant Physiol. 21 (1970) 467-498.10.1146/annurev.pp.21.060170.002343Search in Google 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. Search in Google 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.Search in 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.Search in Google Scholar

47. Bronshteyn, V.L. and Steponkus, P.L. Calorimetric studies of freeze-induced dehydration of phospholipids. Biophys. J. 65 (1993) 1853-1865.Search in Google 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.Search in 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) 2310-2318.10.1016/j.bbamem.2007.06.001Search in Google Scholar PubMed

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

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

Received: 2015-3-19
Accepted: 2015-9-16
Published Online: 2016-3-5
Published in Print: 2015-12-1

© University of Wroclaw, Poland

Articles in the same Issue

  1. How taste works: cells, receptors and gustatory perception
  2. Non-cooperative immobilization of residual water bound in lyophilized photosynthetic lamellae
  3. Coexistence of rare variant HbD Punjab [α2β2121(Glu→Gln)] and alpha 3.7 kb deletion in a young boy of Hindu family in West Bengal, India
  4. Somatic stem cell aging and malignant transformation – impact on therapeutic application
  5. 1H NMR-based metabolic profiling for evaluating poppy seed rancidity and brewing
  6. Homology arms of targeting vectors for gene insertions and CRISPR/Cas9 technology: size does not matter; quality control of targeted clones does
  7. Death domain associated protein (Daxx), a multi-functional protein
  8. In silico screening of alleged miRNAs associated with cell competition: an emerging cellular event in cancer
  9. MGL induces nuclear translocation of EndoG and AIF in caspase-independent T cell death
  10. Cerivastatin represses atherogenic gene expression through the induction of KLF2 via isoprenoid metabolic pathways
  11. Proteasomes raise the microtubule dynamics in influenza A (H1N1) virus-infected LLC-MK2 cells
  12. Purinergic signaling and the functioning of the nervous system cells
  13. The effect of cultureware surfaces on functional and structural components of differentiated 3T3-L1 preadipocytes
  14. Ramipril inhibits high glucose-stimulated up-regulation of adhesion molecules via the ERK1/2 MAPK signaling pathway in human umbilical vein endothelial cells
  15. The effect of nicotine on the expressions of the α7 nicotinic receptor gene and Bax and Bcl-2 proteins in the mammary gland epithelial-7 breast cancer cell line and its relationship to drug resistance
  16. The cloning, expression and purification of recombinant human neuritin from Escherichia coli and the partial analysis of its neurobiological activity
Downloaded on 5.11.2025 from https://www.degruyterbrill.com/document/doi/10.1515/cmble-2015-0040/html
Scroll to top button