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Unveiling large charge transfer character of PSII in an iron-deficient cyanobacterial membrane: A Stark fluorescence spectroscopy study

Authors:
Anjue Ara at Jagannath University
Anjue Ara
Sandrine Dhaene at Vrije Universiteit Amsterdam
Sandrine Dhaene
Rienk van Grondelle at Vrije Universiteit Amsterdam
Rienk van Grondelle
Md Wahadoszamen at University of Dhaka, Bangladesh
Md Wahadoszamen
  • University of Dhaka, Bangladesh
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Abstract and Figures

In this work, we applied Stark fluorescence spectroscopy to an iron-stressed cyanobacterial membrane to reveal key insights about the electronic structures and excited state dynamics of the two important pigment-protein complexes, IsiA and PSII, both of which prevail simultaneously within the membrane during iron deficiency and whose fluorescence spectra are highly overlapped and hence often hardly resolved by conventional fluorescence spectroscopy. Thanks to the ability of Stark fluorescence spectroscopy, the fluorescence signatures of the two complexes could be plausibly recognized and disentangled. The systematic analysis of the SF spectra, carried out by employing standard Liptay formalism with a realistic spectral deconvolution protocol, revealed that the IsiA in an intact membrane retains almost identical excited state electronic structures and dynamics as compared to the isolated IsiA we reported in our earlier study. Moreover, the analysis uncovered that the excited state of the PSII subunit of the intact membrane possesses a significantly large CT character. The observed notably large magnitude of the excited state CT character may signify the supplementary role of PSII in regulative energy dissipation during iron deficiency.
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RESEARCH
Photosynthesis Research (2024) 160:77–86
https://doi.org/10.1007/s11120-024-01099-1
complexes are very similar in most plants and algae, cya-
nobacteria are not equipped with light-harvesting pigment-
protein complexes (LHCs) for harvesting solar energy and
subsequently transferring it to the two photosystems. On the
contrary, to accomplish the same function, cyanobacteria
have evolved a special antenna system termed phycobili-
somes (PBS), which is a huge water-soluble pigment–pro-
tein complex interacting with the cytoplasmic surface of the
thylakoid membrane (Campbell et al. 1998).
By triggering several coordinated protection mecha-
nisms, cyanobacteria are able to fortify their photosynthetic
activity during some inevitable environmental stresses
(Grossman et al. 1994). Since iron is a necessary element
for producing important proteins in the photosynthetic appa-
ratus, the overall photosynthetic activity of cyanobacteria
is greatly impacted by iron deciency. Iron has a very low
biological availability for aquatic photoautotrophs like cya-
nobacteria due to its extremely poor solubility. As a result,
iron is frequently quite scarce for cyanobacteria. During
iron stress, cyanobacteria have evolved, as a survival strat-
egy, the expression of several stress-inducible genes. One
of them is IsiAB operon, which encodes for the synthe-
sis of two genes, IsiA and IsiB (Laudenbach and Straus
Introduction
Cyanobacteria is among the oldest life forms whose exis-
tence can be observed in almost every conceivable environ-
ment. Cyanobacteria dier from other bacteria in that they
possess chlorophyll a (Chla), while most bacteria do not.
Chla combined with phycobilin pigments gives them their
characteristic blue-green color and name as photosynthetic
bacteria. There are two types of photosystems in cyanobac-
teria, called photosystem 1 (PSI) and photosystem 2 (PSII)
both of which are multi-subunit pigment-protein complexes
(Albertsson 2001; Boekema et al. 1987). Although these
Md. Wahadoszamen
wahado.phy@du.ac.bd
1 Department of Physics, Jagannath University, Dhaka
1100, Bangladesh
2 Biophysics of Photosynthesis, Department of Physics and
Astronomy, Faculty of Sciences, VU University Amsterdam,
Amsterdam, The Netherlands
3 Department of Physics, University of Dhaka, Dhaka
1000, Bangladesh
Abstract
In this work, we applied Stark uorescence spectroscopy to an iron-stressed cyanobacterial membrane to reveal key
insights about the electronic structures and excited state dynamics of the two important pigment-protein complexes, IsiA
and PSII, both of which prevail simultaneously within the membrane during iron deciency and whose uorescence
spectra are highly overlapped and hence often hardly resolved by conventional uorescence spectroscopy. Thanks to the
ability of Stark uorescence spectroscopy, the uorescence signatures of the two complexes could be plausibly recognized
and disentangled. The systematic analysis of the SF spectra, carried out by employing standard Liptay formalism with
a realistic spectral deconvolution protocol, revealed that the IsiA in an intact membrane retains almost identical excited
state electronic structures and dynamics as compared to the isolated IsiA we reported in our earlier study. Moreover, the
analysis uncovered that the excited state of the PSII subunit of the intact membrane possesses a signicantly large CT
character. The observed notably large magnitude of the excited state CT character may signify the supplementary role of
PSII in regulative energy dissipation during iron deciency.
Keywords Cyanobacteria · IsiA · PSII · Light harvesting · Charge transfer states · Stark spectroscopy.
Received: 6 October 2023 / Accepted: 25 March 2024 / Published online: 15 April 2024
© The Author(s), under exclusive licence to Springer Nature B.V. 2024
Unveiling large charge transfer character of PSII in an iron-decient
cyanobacterial membrane: A Stark uorescence spectroscopy study
Anjue ManeAra1,2· SandrineD’Haene2· RienkvanGrondelle2· Md.Wahadoszamen2,3
1 3
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