Molecular Mechanisms of Proton-coupled Electron Transfer and Water Oxidation in Photosystem

136 Pages·2020·4.788 MB·English

by  Shin Nakamura

Springer Theses
Recognizing Outstanding Ph.D. Research
Shin Nakamura
Molecular
Mechanisms of
Proton-coupled
Electron Transfer
and Water Oxidation
in Photosystem II
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Shin Nakamura
Molecular Mechanisms
of Proton-coupled Electron
Transfer and Water Oxidation
in Photosystem II
Doctoral Thesis accepted by
Nagoya University, Nagoya, Japan
123
Author Supervisor
Dr. ShinNakamura Prof. TakumiNoguchi
Department ofBiochemical Sciences Division of Material Science(Physics)
“A.Rossi Fanelli” Graduate Schoolof Science
University of Rome“Sapienza” Nagoya University
Rome, Italy Nagoya,Japan
ISSN 2190-5053 ISSN 2190-5061 (electronic)
SpringerTheses
ISBN978-981-15-1583-5 ISBN978-981-15-1584-2 (eBook)
https://doi.org/10.1007/978-981-15-1584-2
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’
Supervisor s Foreword
Photosynthetic water oxidation, which is performed in photosystem II (PSII) in
plants and cyanobacteria, is one of the most essential enzymatic reactions in bio-
logicalsystems.Utilizinglightenergy,wateroxidationprovideselectronsnecessary
for reduction in CO to synthesize sugars and produces molecular oxygen to form
2
the oxygenic atmosphere, and thus, it supports the sustenance of the environment
and life on the Earth. We now know the basic structure of the catalytic center of
wateroxidation,theso-calledMncluster,thankstotherecenthigh-resolutionX-ray
crystallographic studies of PSII. However, the molecular mechanism of water
oxidation, in which protons play the main role, is still the greatest mystery in
photosynthesis research. The key to answer the question is to understand how
protonsarecoupledwithelectrontransfer,whichcontrolsthewholemechanismof
water oxidation.
Inthisthesis,ShinNakamuratackledtheelusiveproblemofthewateroxidation
mechanism using both experimental and theoretical approaches such as Fourier
transform infrared measurements and quantum mechanics/molecular mechanics
simulations. Using these methodologies, he first addressed the mechanism of
asymmetricelectrontransferontheelectron-donorsideofPSII,whichisrelevantto
the high quantum yield of water oxidation. He also analyzed the structures and
vibrationsofwaternetworksneartheMnclusterandproposedanewmechanismof
protontransferduringwateroxidation.Furthermore,heclarifiedtherolesofamino
acidresiduesinteractingwiththeMnclusterwithrespecttothecontroloftheredox
potential and the activation of water molecules. I believe that his work not only
providesasignificantcontributiontoresearchofthewateroxidationmechanismbut
alsooffersanessentialbasisforthedevelopmentofefficientphotocatalystsofwater
oxidation, which is the bottleneck in artificial photosynthesis.
Nagoya, Japan Prof. Takumi Noguchi
December 2019
v
Parts of this thesis have been published in the following journal articles:
(1) S. Nakamura, R. Nagao, R. Takahashi, and T. Noguchi (2014) Fourier trans-
form infrared detection of a polarizable proton trapped between photooxidized
tyrosine Y and a coupled histidine in photosystem II: relevance to the proton
Z
transfer mechanism of water oxidation. Biochemistry 53, 3131–3144.
(2) S. Nakamura and T. Noguchi (2015) Infrared detection of a proton released
from tyrosine Y to the bulk upon its photo-oxidation in photosystem II,
D
Biochemistry 54, 5045–5053
(3) S. Nakamura, K. Ota, Y. Shibuya, and T. Noguchi (2016) Role of a water
network around the Mn4CaO5 cluster in photosynthetic water oxidation:
A Fourier transform infrared spectroscopy and quantum mechanics/molecular
mechanics calculation study, Biochemistry 55, 597–607
(4) S.Nakamura,andT.Noguchi(2016)Quantummechanics/molecularmechanics
simulation of the ligand vibrations of the water-oxidizing Mn CaO cluster in
4 5
photosystem II, Proc.Natl. Acad. Sci. U.S.A. 113, 12727–12732
(5) S.Nakamura,andT.Noguchi(2017)Infrareddeterminationoftheprotonation
state of a key histidine residue in the photosynthetic water oxidizing center,
J. Am. Chem. Soc. 139, 9364–9375.
vii
Acknowledgements
Iwouldliketoexpressmygratitudetoallofthosewhogavemetheopportunityto
complete this thesis. I am especially indebted to my supervisor, Prof. Takumi
Noguchi, for providing me his knowledge, guidance, and technical supports.
I learned the importance of objectivity and perseverance in science through the
research activities with him.
IdeeplyappreciateDr.RyoNagaoforsignificanttechnicaladvicesandsupports
for sample preparations. I learned most of the biochemical techniques used in the
presentworkfromhim.IalsoappreciateDr.RyoutaTakahashiandMr.KaiOtafor
their technical supports in FTIR measurements and Mr. Ryota Ashizawa for his
advice on computational techniques. Finally, I greatly thank Prof. Hiroyuki Mino,
Prof.YukiKato,andallmembersinthelaboratoryforhelpfuldiscussionandkind
supports.
This research was supported by Japan Society for the Promotion of Science
(JSPS) Fellows Grant-in-Aid 15J10320. QM/MM calculations were performed at
the Research Center for Computational Science, Okazaki, Japan, and Information
Technology Center, Nagoya University.
ix
Contents
1 General Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1
1.1 Photosystem II . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1
1.2 Fourier Transform Infrared Spectroscopy (FTIR) . . . . . . . . . . . . . 4
1.3 Quantum Chemical Calculation . . . . . . . . . . . . . . . . . . . . . . . . . . 6
1.4 Purpose of This Study. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
2 Hydrogen Bond Structure of Redox Active Tyrosines
in Photosystem II . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11
2.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11
2.2 Materials and Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13
2.3 Results. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16
2.4 Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 27
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 32
3 Proton Release Reaction of Tyrosine D in Photosystem II . . . . . . . . 37
3.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 37
3.2 Materials and Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 38
3.3 Results. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 40
3.4 Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 45
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 48
4 Vibrational Analysis of Water Network Around
the Mn Cluster . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 53
4.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 53
4.2 Materials and Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 54
4.3 Results. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 55
4.4 Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 60
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63
xi
xii Contents
5 Vibrational Analysis of Carboxylate Ligands
in the Water Oxidizing Center . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 67
5.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 67
5.2 Materials and Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 69
5.3 Results. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 70
5.4 Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 86
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 91
6 Protonation Structure of a Key Histidine
in the Water Oxidizing Center . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 95
6.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 95
6.2 Materials and Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 97
6.3 Results. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 100
6.4 Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 111
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 118
7 General Conclusion. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 123
Curriculum Vitae .. .... .... ..... .... .... .... .... .... ..... .... 125