Lipid polymorphism in chloroplast thylakoid membranes - as revealed by P-NMR and time-resolved merocyanine fluorescence spectroscopy.

Győző Garab, Bettina Ughy, Pieter de Waard, Parveen Akhtar, Uroš Javornik, Christos Kotakis, Primož Šket, Václav Karlický, Zuzana Materová, Vladimír Špunda, Janez Plavec, Herbert van Amerongen, László Vígh, Henk Van As, Petar H Lambrev

Journal: Scientific reports 2019;7(1):13343

PMID: 29042649

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Abstract

Chloroplast thylakoid membranes contain virtually all components of the energy-converting photosynthetic machinery. Their energized state, driving ATP synthesis, is enabled by the bilayer organization of the membrane. However, their most abundant lipid species is a non-bilayer-forming lipid, monogalactosyl-diacylglycerol; the role of lipid polymorphism in these membranes is poorly understood. Earlier P-NMR experiments revealed the coexistence of a bilayer and a non-bilayer, isotropic lipid phase in spinach thylakoids. Packing of lipid molecules, tested by fluorescence spectroscopy of the lipophilic dye, merocyanine-540 (MC540), also displayed heterogeneity. Now, our P-NMR experiments on spinach thylakoids uncover the presence of a bilayer and three non-bilayer lipid phases; time-resolved fluorescence spectroscopy of MC540 also reveals the presence of multiple lipidic environments. It is also shown by P-NMR that: (i) some lipid phases are sensitive to the osmolarity and ionic strength of the medium, (ii) a lipid phase can be modulated by catalytic hydrogenation of fatty acids and (iii) a marked increase of one of the non-bilayer phases upon lowering the pH of the medium is observed. These data provide additional experimental evidence for the polymorphism of lipid phases in thylakoids and suggest that non-bilayer phases play an active role in the structural dynamics of thylakoid membranes.

Address: Institute of Plant Biology, Biological Research Centre, Hungarian Academy of Sciences, Temesvári körút 62, H-6726, Szeged, Hungary. [email protected].; Department of Physics, Faculty of Science, University of Ostrava, Chittussiho 10, CZ-710 00, Ostrava, Czech Republic. [email protected].; Institute of Plant Biology, Biological Research Centre, Hungarian Academy of Sciences, Temesvári körút 62, H-6726, Szeged, Hungary.; MAGNEFY, Magnetic Resonance Research Facility (Wageningen NMR Centre), Wageningen University & Research, Stippeneng 4, 6708 WE, Wageningen, The Netherlands.; Laboratory of BioNano Technology, Wageningen University & Research, Bornse Weilanden 9, 6708 WG, Wageningen, The Netherlands.; Slovenian NMR Center, National Institute of Chemistry, Hajdrihova 19, Ljubljana, Slovenia.; EN-FIST Center of Excellence, Trg OF 13, Ljubljana, Slovenia.; Department of Physics, Faculty of Science, University of Ostrava, Chittussiho 10, CZ-710 00, Ostrava, Czech Republic.; Faculty of Chemistry and Chemical Technology, Večna pot 113, Ljubljana, Slovenia.; Laboratory of Biophysics, Wageningen University & Research, Stippeneng 4, 6708 WE, Wageningen, The Netherlands.; MicroSpectroscopy Centre, Wageningen University & Research, Stippeneng 4, 6708 WE, Wageningen, The Netherlands.; Institute of Biochemistry, Biological Research Centre, Hungarian Academy of Sciences, Temesvári körút 62, H-6726, Szeged, Hungary.; MAGNEFY, Magnetic Resonance Research Facility (Wageningen NMR Centre), Wageningen University & Research, Stippeneng 4, 6708 WE, Wageningen, The Netherlands. [email protected].; Laboratory of Biophysics, Wageningen University & Research, Stippeneng 4, 6708 WE, Wageningen, The Netherlands. [email protected].; Institute of Plant Biology, Biological Research Centre, Hungarian Academy of Sciences, Temesvári körút 62, H-6726, Szeged, Hungary. [email protected].

DOI: 10.1038/s41598-017-13574-y

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MeSH Terms: Catalysis, Hydrogen-Ion Concentration, Lipids, Magnetic Resonance Spectroscopy, Phosphorus Isotopes, Spectrometry, Fluorescence, Thylakoids