Comparison of the thermodynamic landscapes of unfolding and formation of the energy dissipative state in the isolated light harvesting complex ii

S. Santabarbara, P. Horton, A.V. Ruban

Research output: Contribution to journalArticle

19 Citations (Scopus)

Abstract

In biochemistry and cell biology, understanding the molecular mechanisms by which physiological processes are regulated is regarded as an ultimate goal. In higher plants, one of the most widely investigated regulatory processes occurs in the light harvesting complexes (LHCII) of the chloroplast thylakoid membranes. Under limiting photon flux densities, LHCII harvests sunlight with high efficiency. When the intensity of incident radiation reaches levels close to the saturation of the photosynthesis, the efficiency of light harvesting is decreased by a process referred to as nonphotochemical quenching (NPQ), which enhances the singlet-excited state deactivation via nonradiative dissipative processes. Conformational rearrangements in LHCII are known to be crucial in promoting and controlling NPQ in vitro and in vivo. In this article, we address the thermodynamic nature of the conformational rearrangements promoting and controlling NPQ in isolated LHCII. A combined, linear reaction scheme in which the folded, quenched state represents a stable intermediate on the unfolding pathway was employed to describe the temperature dependence of the spectroscopic signatures associated with the chlorophyll fluorescence quenching and the loss of secondary structure motifs in LHCII. The thermodynamic model requires considering the temperature dependence of Gibbs free energy difference between the quenched and the unquenched states, as well as the unfolded and quenched states, of LHCII. Even though the same reaction scheme is adequate to describe the quenching and the unfolding processes in LHCII monomers and trimers, their thermodynamic characteristics were found to be markedly different. The results of the thermodynamic analysis shed light on the physiological importance of the trimeric state of LHCII in stabilizing the efficient light harvesting mode as well as preventing the quenched conformation of the protein from unfolding. Moreover, the transition to the quenched conformation in trimers reveals a larger degree of cooperativity than in monomers, explained by a small characteristic entropy (Delta H-q = 85 +/- 3 kJ mol(-1) compared to 125 +/- 5 kJ mol(-1) in monomers), which enables the fine-tuning of nonphotochemical quenching in vivo.
LanguageEnglish
Pages1188-1197
Number of pages9
JournalBiophysical Journal
Volume97
Issue number4
DOIs
Publication statusPublished - 19 Aug 2009

Fingerprint

Thermodynamics
Light
Physiological Phenomena
Protein Unfolding
Thylakoids
Temperature
Sunlight
Photosynthesis
Entropy
Chloroplasts
Chlorophyll
Photons
Biochemistry
Cell Biology
Fluorescence
Radiation

Keywords

  • time-resolved fluorescence
  • non-arrhenius kinetics
  • photsystem-ii
  • thylakoid membranes
  • globular-proteins
  • plant antenna
  • green plants
  • photoprotection
  • zeaxanthin

Cite this

@article{01d486600599473899b734b285ea4b3c,
title = "Comparison of the thermodynamic landscapes of unfolding and formation of the energy dissipative state in the isolated light harvesting complex ii",
abstract = "In biochemistry and cell biology, understanding the molecular mechanisms by which physiological processes are regulated is regarded as an ultimate goal. In higher plants, one of the most widely investigated regulatory processes occurs in the light harvesting complexes (LHCII) of the chloroplast thylakoid membranes. Under limiting photon flux densities, LHCII harvests sunlight with high efficiency. When the intensity of incident radiation reaches levels close to the saturation of the photosynthesis, the efficiency of light harvesting is decreased by a process referred to as nonphotochemical quenching (NPQ), which enhances the singlet-excited state deactivation via nonradiative dissipative processes. Conformational rearrangements in LHCII are known to be crucial in promoting and controlling NPQ in vitro and in vivo. In this article, we address the thermodynamic nature of the conformational rearrangements promoting and controlling NPQ in isolated LHCII. A combined, linear reaction scheme in which the folded, quenched state represents a stable intermediate on the unfolding pathway was employed to describe the temperature dependence of the spectroscopic signatures associated with the chlorophyll fluorescence quenching and the loss of secondary structure motifs in LHCII. The thermodynamic model requires considering the temperature dependence of Gibbs free energy difference between the quenched and the unquenched states, as well as the unfolded and quenched states, of LHCII. Even though the same reaction scheme is adequate to describe the quenching and the unfolding processes in LHCII monomers and trimers, their thermodynamic characteristics were found to be markedly different. The results of the thermodynamic analysis shed light on the physiological importance of the trimeric state of LHCII in stabilizing the efficient light harvesting mode as well as preventing the quenched conformation of the protein from unfolding. Moreover, the transition to the quenched conformation in trimers reveals a larger degree of cooperativity than in monomers, explained by a small characteristic entropy (Delta H-q = 85 +/- 3 kJ mol(-1) compared to 125 +/- 5 kJ mol(-1) in monomers), which enables the fine-tuning of nonphotochemical quenching in vivo.",
keywords = "time-resolved fluorescence, non-arrhenius kinetics, photsystem-ii, thylakoid membranes, globular-proteins, plant antenna, green plants, photoprotection, zeaxanthin",
author = "S. Santabarbara and P. Horton and A.V. Ruban",
year = "2009",
month = "8",
day = "19",
doi = "10.1016/j.bpj.2009.06.005",
language = "English",
volume = "97",
pages = "1188--1197",
journal = "Biophysical Journal",
issn = "0006-3495",
number = "4",

}

Comparison of the thermodynamic landscapes of unfolding and formation of the energy dissipative state in the isolated light harvesting complex ii. / Santabarbara, S.; Horton, P.; Ruban, A.V.

In: Biophysical Journal, Vol. 97, No. 4, 19.08.2009, p. 1188-1197.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Comparison of the thermodynamic landscapes of unfolding and formation of the energy dissipative state in the isolated light harvesting complex ii

AU - Santabarbara, S.

AU - Horton, P.

AU - Ruban, A.V.

PY - 2009/8/19

Y1 - 2009/8/19

N2 - In biochemistry and cell biology, understanding the molecular mechanisms by which physiological processes are regulated is regarded as an ultimate goal. In higher plants, one of the most widely investigated regulatory processes occurs in the light harvesting complexes (LHCII) of the chloroplast thylakoid membranes. Under limiting photon flux densities, LHCII harvests sunlight with high efficiency. When the intensity of incident radiation reaches levels close to the saturation of the photosynthesis, the efficiency of light harvesting is decreased by a process referred to as nonphotochemical quenching (NPQ), which enhances the singlet-excited state deactivation via nonradiative dissipative processes. Conformational rearrangements in LHCII are known to be crucial in promoting and controlling NPQ in vitro and in vivo. In this article, we address the thermodynamic nature of the conformational rearrangements promoting and controlling NPQ in isolated LHCII. A combined, linear reaction scheme in which the folded, quenched state represents a stable intermediate on the unfolding pathway was employed to describe the temperature dependence of the spectroscopic signatures associated with the chlorophyll fluorescence quenching and the loss of secondary structure motifs in LHCII. The thermodynamic model requires considering the temperature dependence of Gibbs free energy difference between the quenched and the unquenched states, as well as the unfolded and quenched states, of LHCII. Even though the same reaction scheme is adequate to describe the quenching and the unfolding processes in LHCII monomers and trimers, their thermodynamic characteristics were found to be markedly different. The results of the thermodynamic analysis shed light on the physiological importance of the trimeric state of LHCII in stabilizing the efficient light harvesting mode as well as preventing the quenched conformation of the protein from unfolding. Moreover, the transition to the quenched conformation in trimers reveals a larger degree of cooperativity than in monomers, explained by a small characteristic entropy (Delta H-q = 85 +/- 3 kJ mol(-1) compared to 125 +/- 5 kJ mol(-1) in monomers), which enables the fine-tuning of nonphotochemical quenching in vivo.

AB - In biochemistry and cell biology, understanding the molecular mechanisms by which physiological processes are regulated is regarded as an ultimate goal. In higher plants, one of the most widely investigated regulatory processes occurs in the light harvesting complexes (LHCII) of the chloroplast thylakoid membranes. Under limiting photon flux densities, LHCII harvests sunlight with high efficiency. When the intensity of incident radiation reaches levels close to the saturation of the photosynthesis, the efficiency of light harvesting is decreased by a process referred to as nonphotochemical quenching (NPQ), which enhances the singlet-excited state deactivation via nonradiative dissipative processes. Conformational rearrangements in LHCII are known to be crucial in promoting and controlling NPQ in vitro and in vivo. In this article, we address the thermodynamic nature of the conformational rearrangements promoting and controlling NPQ in isolated LHCII. A combined, linear reaction scheme in which the folded, quenched state represents a stable intermediate on the unfolding pathway was employed to describe the temperature dependence of the spectroscopic signatures associated with the chlorophyll fluorescence quenching and the loss of secondary structure motifs in LHCII. The thermodynamic model requires considering the temperature dependence of Gibbs free energy difference between the quenched and the unquenched states, as well as the unfolded and quenched states, of LHCII. Even though the same reaction scheme is adequate to describe the quenching and the unfolding processes in LHCII monomers and trimers, their thermodynamic characteristics were found to be markedly different. The results of the thermodynamic analysis shed light on the physiological importance of the trimeric state of LHCII in stabilizing the efficient light harvesting mode as well as preventing the quenched conformation of the protein from unfolding. Moreover, the transition to the quenched conformation in trimers reveals a larger degree of cooperativity than in monomers, explained by a small characteristic entropy (Delta H-q = 85 +/- 3 kJ mol(-1) compared to 125 +/- 5 kJ mol(-1) in monomers), which enables the fine-tuning of nonphotochemical quenching in vivo.

KW - time-resolved fluorescence

KW - non-arrhenius kinetics

KW - photsystem-ii

KW - thylakoid membranes

KW - globular-proteins

KW - plant antenna

KW - green plants

KW - photoprotection

KW - zeaxanthin

UR - http://dx.doi.org/10.1016/j.bpj.2009.06.005

U2 - 10.1016/j.bpj.2009.06.005

DO - 10.1016/j.bpj.2009.06.005

M3 - Article

VL - 97

SP - 1188

EP - 1197

JO - Biophysical Journal

T2 - Biophysical Journal

JF - Biophysical Journal

SN - 0006-3495

IS - 4

ER -