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Title: Role of Protein-Water Interface in the Stacking Interactions of Granum Thylakoid Membranes—As Revealed by the Effects of Hofmeister Salts

Abstract

The thylakoid membranes of vascular plants are differentiated into stacked granum and unstacked stroma regions. The formation of grana is triggered by the macrodomain formation of photosystem II and light-harvesting complex II (PSII-LHCII) and thus their lateral segregation from the photosystem I—light-harvesting complex I (PSI-LHCI) super-complexes and the ATP-synthase; which is then stabilized by stacking interactions of the adjacent PSII-LHCII enriched regions of the thylakoid membranes. The self-assembly and dynamics of this highly organized membrane system and the nature of forces acting between the PSII-LHCII macrodomains are not well understood. By using circular dichroism (CD) spectroscopy, small-angle neutron scattering (SANS) and transmission electron microscopy (TEM), we investigated the effects of Hofmeister salts on the organization of pigment-protein complexes and on the ultrastructure of thylakoid membranes. We found that the kosmotropic agent (NH4)2SO4 and the Hofmeister-neutral NaCl, up to 2 M concentrations, hardly affected the macro-organization of the protein complexes and the membrane ultrastructure. In contrast, chaotropic salts, NaClO4, and NaSCN destroyed the mesoscopic structures, the multilamellar organization of the thylakoid membranes and the chiral macrodomains of the protein complexes but without noticeably affecting the short-range, pigment-pigment excitonic interactions. Comparison of the concentration- and time-dependences of SANS, TEM and CD parametersmore » revealed the main steps of the disassembly of grana in the presence of chaotropes. It begins with a rapid diminishment of the long-range periodic order of the grana membranes, apparently due to an increased stacking disorder of the thylakoid membranes, as reflected by SANS experiments. SANS measurements also allowed discrimination between the cationic and anionic effects—in stacking and disorder, respectively. This step is followed by a somewhat slower disorganization of the TEM ultrastructure, due to the gradual loss of stacked membrane pairs. Occurring last is the stepwise decrease and disappearance of the long-range chiral order of the protein complexes, the rate of which was faster in LHCII-deficient membranes. These data are interpreted in terms of a theory, from our laboratory, according to which Hofmeister salts primarily affect the hydrophylic-hydrophobic interactions of proteins, and the stroma-exposed regions of the intrinsic membrane proteins, in particular—pointing to the role of protein-water interface in the stacking interactions of granum thylakoid membranes.« less

Authors:
 [1];  [2]; ORCiD logo [3];  [2];  [1];  [4];  [5];  [6];  [1];  [1]
+ Show Author Affiliations
  1. Biological Research Centre, Szeged (Hungary)
  2. Centre for Energy Research, Budapest (Hungary)
  3. Paul Scherrer Inst. (PSI), Villigen (Switzerland); Wigner Research Centre for Physics, Budapest (Hungary); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  4. Forschungszentrum Juelich, Garching (Germany)
  5. Paul Scherrer Inst. (PSI), Villigen (Switzerland)
  6. Biological Research Centre, Szeged (Hungary); Univ. of Ostrava (Czechia)
Publication Date:
Research Org.:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE; National Research Development and Innovation Office of Hungary; Czech Science Foundation; Hungarian Academy of Sciences; Hungarian Ministry for Innovation and Technology; Ministry for National Economy of Hungary
OSTI Identifier:
1747014
Grant/Contract Number:  
AC05-00OR22725; KH-124985; K-128679; GACR-19-13637S; UNKP-19-4; GINOP-2.3.2-15-2016-00001
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Plant Science
Additional Journal Information:
Journal Volume: 11; Journal ID: ISSN 1664-462X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; circular dichroism; granum; Hofmeister effect; thylakoid membranes; protein-water interface; small-angle neutron scattering; ultrastructure

Citation Formats

Zsiros, Ottó, Ünnep, Renáta, Nagy, Gergely, Almásy, László, Patai, Roland, Székely, Noémi K., Kohlbrecher, Joachim, Garab, Győző, Dér, András, and Kovács, László. Role of Protein-Water Interface in the Stacking Interactions of Granum Thylakoid Membranes—As Revealed by the Effects of Hofmeister Salts. United States: N. p., 2020. Web. doi:10.3389/fpls.2020.01257.
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Zsiros, Ottó, Ünnep, Renáta, Nagy, Gergely, Almásy, László, Patai, Roland, Székely, Noémi K., Kohlbrecher, Joachim, Garab, Győző, Dér, András, & Kovács, László. Role of Protein-Water Interface in the Stacking Interactions of Granum Thylakoid Membranes—As Revealed by the Effects of Hofmeister Salts. United States. https://doi.org/10.3389/fpls.2020.01257
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Zsiros, Ottó, Ünnep, Renáta, Nagy, Gergely, Almásy, László, Patai, Roland, Székely, Noémi K., Kohlbrecher, Joachim, Garab, Győző, Dér, András, and Kovács, László. Fri . "Role of Protein-Water Interface in the Stacking Interactions of Granum Thylakoid Membranes—As Revealed by the Effects of Hofmeister Salts". United States. https://doi.org/10.3389/fpls.2020.01257. https://www.osti.gov/servlets/purl/1747014.
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@article{osti_1747014,
title = {Role of Protein-Water Interface in the Stacking Interactions of Granum Thylakoid Membranes—As Revealed by the Effects of Hofmeister Salts},
author = {Zsiros, Ottó and Ünnep, Renáta and Nagy, Gergely and Almásy, László and Patai, Roland and Székely, Noémi K. and Kohlbrecher, Joachim and Garab, Győző and Dér, András and Kovács, László},
abstractNote = {The thylakoid membranes of vascular plants are differentiated into stacked granum and unstacked stroma regions. The formation of grana is triggered by the macrodomain formation of photosystem II and light-harvesting complex II (PSII-LHCII) and thus their lateral segregation from the photosystem I—light-harvesting complex I (PSI-LHCI) super-complexes and the ATP-synthase; which is then stabilized by stacking interactions of the adjacent PSII-LHCII enriched regions of the thylakoid membranes. The self-assembly and dynamics of this highly organized membrane system and the nature of forces acting between the PSII-LHCII macrodomains are not well understood. By using circular dichroism (CD) spectroscopy, small-angle neutron scattering (SANS) and transmission electron microscopy (TEM), we investigated the effects of Hofmeister salts on the organization of pigment-protein complexes and on the ultrastructure of thylakoid membranes. We found that the kosmotropic agent (NH4)2SO4 and the Hofmeister-neutral NaCl, up to 2 M concentrations, hardly affected the macro-organization of the protein complexes and the membrane ultrastructure. In contrast, chaotropic salts, NaClO4, and NaSCN destroyed the mesoscopic structures, the multilamellar organization of the thylakoid membranes and the chiral macrodomains of the protein complexes but without noticeably affecting the short-range, pigment-pigment excitonic interactions. Comparison of the concentration- and time-dependences of SANS, TEM and CD parameters revealed the main steps of the disassembly of grana in the presence of chaotropes. It begins with a rapid diminishment of the long-range periodic order of the grana membranes, apparently due to an increased stacking disorder of the thylakoid membranes, as reflected by SANS experiments. SANS measurements also allowed discrimination between the cationic and anionic effects—in stacking and disorder, respectively. This step is followed by a somewhat slower disorganization of the TEM ultrastructure, due to the gradual loss of stacked membrane pairs. Occurring last is the stepwise decrease and disappearance of the long-range chiral order of the protein complexes, the rate of which was faster in LHCII-deficient membranes. These data are interpreted in terms of a theory, from our laboratory, according to which Hofmeister salts primarily affect the hydrophylic-hydrophobic interactions of proteins, and the stroma-exposed regions of the intrinsic membrane proteins, in particular—pointing to the role of protein-water interface in the stacking interactions of granum thylakoid membranes.},
doi = {10.3389/fpls.2020.01257},
journal = {Frontiers in Plant Science},
number = ,
volume = 11,
place = {United States},
year = {Fri Aug 14 00:00:00 EDT 2020},
month = {Fri Aug 14 00:00:00 EDT 2020}
}
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