Photoprotection through ultrafast charge recombination in photochemical reaction centres under oxidizing conditions

Fei Ma, David J. K. Swainsbury, Michael R. Jones, Rienk van Grondelle

Research output: Contribution to JournalArticleAcademicpeer-review

Abstract

Engineering natural photosynthesis to address predicted shortfalls in food and energy supply requires a detailed understanding of its molecular basis and the intrinsic photoprotective mechanisms that operate under fluctuating environmental conditions. Long-lived triplet or singlet excited electronic states have the potential to cause photodamage, particularly in the presence of oxygen, and so a variety of mechanisms exist to prevent formation of such states or safely dissipate their energy. Here, we report a dramatic difference in spectral evolution in fully reduced and partially oxidized Rhodobacter sphaeroides reaction centres (RCs) following excitation of the monomeric bacteriochlorophyll (BChl) cofactors at 805 nm. Three types of preparation were studied, including RCs purified as protein/lipid nanodiscs using the copolymer styrene maleic acid. In fully reduced RCs such excitation produces membrane-spanning charge separation. In preparations of partially oxidized RCs the spectroscopic signature of this charge separation is replaced by that of an energy dissipation process, including in the majority sub-population of reduced RCs. This process, which appears to take place on both cofactor branches, involves formation of a BChl(+)/bacteriopheophytin(-) radical pair that dissipates energy via recombination to a vibrationally hot ground state. The possible physiological role of this dissipative process under mildly oxidizing conditions is considered.
Original languageEnglish
Article number20160378
JournalPhilosophical Transactions of the Royal Society B. Biological Sciences
Volume372
Issue number1730
DOIs
Publication statusPublished - 26 Sep 2017

Keywords

  • reaction centre
  • photoprotection
  • charge recombination
  • ultrafast spectroscopy
  • styrene maleic acid

Cite this

@article{e755dad3003e472cbf239184284a038c,
title = "Photoprotection through ultrafast charge recombination in photochemical reaction centres under oxidizing conditions",
abstract = "Engineering natural photosynthesis to address predicted shortfalls in food and energy supply requires a detailed understanding of its molecular basis and the intrinsic photoprotective mechanisms that operate under fluctuating environmental conditions. Long-lived triplet or singlet excited electronic states have the potential to cause photodamage, particularly in the presence of oxygen, and so a variety of mechanisms exist to prevent formation of such states or safely dissipate their energy. Here, we report a dramatic difference in spectral evolution in fully reduced and partially oxidized Rhodobacter sphaeroides reaction centres (RCs) following excitation of the monomeric bacteriochlorophyll (BChl) cofactors at 805 nm. Three types of preparation were studied, including RCs purified as protein/lipid nanodiscs using the copolymer styrene maleic acid. In fully reduced RCs such excitation produces membrane-spanning charge separation. In preparations of partially oxidized RCs the spectroscopic signature of this charge separation is replaced by that of an energy dissipation process, including in the majority sub-population of reduced RCs. This process, which appears to take place on both cofactor branches, involves formation of a BChl(+)/bacteriopheophytin(-) radical pair that dissipates energy via recombination to a vibrationally hot ground state. The possible physiological role of this dissipative process under mildly oxidizing conditions is considered.",
keywords = "reaction centre, photoprotection, charge recombination, ultrafast spectroscopy, styrene maleic acid",
author = "Fei Ma and Swainsbury, {David J. K.} and Jones, {Michael R.} and {van Grondelle}, Rienk",
year = "2017",
month = "9",
day = "26",
doi = "10.1098/rstb.2016.0378",
language = "English",
volume = "372",
journal = "Philosophical Transactions of the Royal Society B. Biological Sciences",
issn = "0962-8436",
publisher = "Royal Society of London",
number = "1730",

}

Photoprotection through ultrafast charge recombination in photochemical reaction centres under oxidizing conditions. / Ma, Fei; Swainsbury, David J. K.; Jones, Michael R.; van Grondelle, Rienk.

In: Philosophical Transactions of the Royal Society B. Biological Sciences, Vol. 372, No. 1730, 20160378, 26.09.2017.

Research output: Contribution to JournalArticleAcademicpeer-review

TY - JOUR

T1 - Photoprotection through ultrafast charge recombination in photochemical reaction centres under oxidizing conditions

AU - Ma, Fei

AU - Swainsbury, David J. K.

AU - Jones, Michael R.

AU - van Grondelle, Rienk

PY - 2017/9/26

Y1 - 2017/9/26

N2 - Engineering natural photosynthesis to address predicted shortfalls in food and energy supply requires a detailed understanding of its molecular basis and the intrinsic photoprotective mechanisms that operate under fluctuating environmental conditions. Long-lived triplet or singlet excited electronic states have the potential to cause photodamage, particularly in the presence of oxygen, and so a variety of mechanisms exist to prevent formation of such states or safely dissipate their energy. Here, we report a dramatic difference in spectral evolution in fully reduced and partially oxidized Rhodobacter sphaeroides reaction centres (RCs) following excitation of the monomeric bacteriochlorophyll (BChl) cofactors at 805 nm. Three types of preparation were studied, including RCs purified as protein/lipid nanodiscs using the copolymer styrene maleic acid. In fully reduced RCs such excitation produces membrane-spanning charge separation. In preparations of partially oxidized RCs the spectroscopic signature of this charge separation is replaced by that of an energy dissipation process, including in the majority sub-population of reduced RCs. This process, which appears to take place on both cofactor branches, involves formation of a BChl(+)/bacteriopheophytin(-) radical pair that dissipates energy via recombination to a vibrationally hot ground state. The possible physiological role of this dissipative process under mildly oxidizing conditions is considered.

AB - Engineering natural photosynthesis to address predicted shortfalls in food and energy supply requires a detailed understanding of its molecular basis and the intrinsic photoprotective mechanisms that operate under fluctuating environmental conditions. Long-lived triplet or singlet excited electronic states have the potential to cause photodamage, particularly in the presence of oxygen, and so a variety of mechanisms exist to prevent formation of such states or safely dissipate their energy. Here, we report a dramatic difference in spectral evolution in fully reduced and partially oxidized Rhodobacter sphaeroides reaction centres (RCs) following excitation of the monomeric bacteriochlorophyll (BChl) cofactors at 805 nm. Three types of preparation were studied, including RCs purified as protein/lipid nanodiscs using the copolymer styrene maleic acid. In fully reduced RCs such excitation produces membrane-spanning charge separation. In preparations of partially oxidized RCs the spectroscopic signature of this charge separation is replaced by that of an energy dissipation process, including in the majority sub-population of reduced RCs. This process, which appears to take place on both cofactor branches, involves formation of a BChl(+)/bacteriopheophytin(-) radical pair that dissipates energy via recombination to a vibrationally hot ground state. The possible physiological role of this dissipative process under mildly oxidizing conditions is considered.

KW - reaction centre

KW - photoprotection

KW - charge recombination

KW - ultrafast spectroscopy

KW - styrene maleic acid

U2 - 10.1098/rstb.2016.0378

DO - 10.1098/rstb.2016.0378

M3 - Article

VL - 372

JO - Philosophical Transactions of the Royal Society B. Biological Sciences

JF - Philosophical Transactions of the Royal Society B. Biological Sciences

SN - 0962-8436

IS - 1730

M1 - 20160378

ER -