The ground state and excited state electronic properties of chlorophyll (Chl) a and Chl b in diethyl ether, acetone, and ethanol solutions are investigated using quantum mechanical and molecular mechanical calculations with density functional theory (DFT) and time-dependent DFT (TDDFT). Although the DFT/TDDFT methods are widely used, the electronic structures of molecules, especially large molecules, calculated with these methods are known to be strongly dependent on the functionals and the parameters used in the functionals. Here, we optimize the range-separated parameter, μ, of the CAM-B3LYP functional of Chl a and Chl b to reproduce the experimental excitation energy differences of these Chl molecules in solution. The optimal values of μ for Chl a and Chl b are smaller than the default value of μ and that for bacteriochlorophyll a, indicating the change in the electronic distribution, i.e., an increase in electron delocalization, within the molecule. We find that the electronic distribution of Chl b with an extra formyl group is different from that of Chl a. We also find that the polarity of the solution and hydrogen bond cause the decrease in the excitation energies and the increase in the widths of excitation energy distributions of Chl a and Chl b. The present results are expected to be useful for understanding the electronic properties of each pigment molecule in a local heterogeneous environment, which will play an important role in the excitation energy transfer in light-harvesting complex II.

1.
R. E.
Blankenship
,
Molecular Mechanisms of Photosynthesis
(
John Wiley & Sons
,
2021
).
2.
I.
Bos
,
K. M.
Bland
,
L.
Tian
,
R.
Croce
,
L. K.
Frankel
,
H.
van Amerongen
,
T. M.
Bricker
, and
E.
Wientjes
,
Biochim. Biophys. Acta, Bioenerg.
1858
,
371
(
2017
).
3.
C.
Olbrich
,
J.
Strümpfer
,
K.
Schulten
, and
U.
Kleinekathöfer
,
J. Phys. Chem. Lett.
2
,
1771
(
2011
).
4.
T.
Renger
,
A.
Klinger
,
F.
Steinecker
,
M.
Schmidt am Busch
,
J.
Numata
, and
F.
Müh
,
J. Phys. Chem. B
116
,
14565
(
2012
).
5.
S.
Shim
,
P.
Rebentrost
,
S.
Valleau
, and
A.
Aspuru-Guzik
,
Biophys. J.
102
,
649
(
2012
).
6.
C.
Kӧnig
and
J.
Neugebauer
,
J. Chem. Theory Comput.
9
,
1808
(
2013
).
7.
E.
Rivera
,
D.
Montemayor
,
M.
Masia
, and
D. F.
Coker
,
J. Phys. Chem. B
117
,
5510
(
2013
).
8.
M.
Higashi
,
T.
Kosugi
,
S.
Hayashi
, and
S.
Saito
,
J. Phys. Chem. B
118
,
10906
(
2014
).
9.
M.
Higashi
and
S.
Saito
,
J. Chem. Theory Comput.
12
,
4128
(
2016
).
10.
X.
Jia
,
Y.
Mei
,
J. Z. H.
Zhang
, and
Y.
Mo
,
Sci. Rep.
5
,
17096
(
2015
).
11.
C. W.
Kim
and
Y. M.
Rhee
,
J. Chem. Theory Comput.
12
,
5235
(
2016
).
12.
C. W.
Kim
,
B.
Choi
, and
Y. M.
Rhee
,
Phys. Chem. Chem. Phys.
20
,
3310
(
2018
).
13.
E. I.
Iseri
and
D.
Gülen
,
Eur. Biophys. J.
28
,
243
(
1999
).
14.
S. I. E.
Vulto
,
M. A.
de Baat
,
S.
Neerken
,
F. R.
Nowak
,
H.
van Amerongen
,
J.
Amesz
, and
T. J.
Aartsma
,
J. Phys. Chem. B
103
,
8153
(
1999
).
15.
M.
Wendling
,
M. A.
Przyjalgowski
,
D.
Gülen
,
S. I. E.
Vulto
,
T. J.
Aartsma
,
R. v.
Grondelle
, and
H.
Van Amerongen
,
Photosynth. Res.
71
,
99
(
2002
).
16.
J.
Adolphs
and
T.
Renger
,
Biophys. J.
91
,
2778
(
2006
).
17.
E. L.
Read
,
G. S.
Schlau-Cohen
,
G. S.
Engel
,
J.
Wen
,
R. E.
Blankenship
, and
G. R.
Fleming
,
Biophys. J.
95
,
847
(
2008
).
18.
M.
Schmidt am Busch
,
F.
Müh
,
M.
El-Amine Madjet
, and
T.
Renger
,
J. Phys. Chem. Lett.
2
,
93
(
2011
).
19.
Y.
Song
,
A.
Schubert
,
E.
Maret
,
R. K.
Burdick
,
B. D.
Dunietz
,
E.
Geva
, and
J. P.
Ogilvie
,
Chem. Sci.
10
,
8143
(
2019
).
20.
H.
Aksu
,
A.
Schubert
,
E.
Geva
, and
B. D.
Dunietz
,
J. Phys. Chem. B
123
,
8970
(
2019
).
21.
S.
Saito
,
M.
Higashi
, and
G. R.
Fleming
,
J. Phys. Chem. B
123
,
9762
(
2019
).
22.
M. K.
Lee
and
D. F.
Coker
,
J. Phys. Chem. Lett.
7
,
3171
(
2016
).
23.
T. R.
Calhoun
,
N. S.
Ginsberg
,
G. S.
Schlau-Cohen
,
Y.-C.
Cheng
,
M.
Ballottari
,
R.
Bassi
, and
G. R.
Fleming
,
J. Phys. Chem. B
113
,
16291
(
2009
).
24.
V. I.
Novoderezhkin
,
M. A.
Palacios
,
H.
van Amerongen
, and
R.
van Grondelle
,
J. Phys. Chem. B
109
,
10493
(
2005
).
25.
F.
Müh
,
M. E.-A.
Madjet
, and
T.
Renger
,
J. Phys. Chem. B
114
,
13517
(
2010
).
26.
F.
Müh
and
T.
Renger
,
Biochim. Biophys. Acta, Bioenerg.
1817
,
1446
(
2012
).
27.
V.
Novoderezhkin
,
A.
Marin
, and
R.
van Grondelle
,
Phys. Chem. Chem. Phys.
13
,
17093
(
2011
).
28.
V. I.
Novoderezhkin
and
R.
Van Grondelle
,
J. Phys. B: At., Mol. Opt. Phys.
50
,
124003
(
2017
).
29.
T.
Renger
and
F.
Müh
,
Phys. Chem. Chem. Phys.
15
,
3348
(
2013
).
30.
D.
Sundholm
,
Chem. Phys. Lett.
302
,
480
(
1999
).
31.
A. B. J.
Parusel
and
S.
Grimme
,
J. Phys. Chem. B
104
,
5395
(
2000
).
32.
Z.-L.
Cai
,
M. J.
Crossley
,
J. R.
Reimers
,
R.
Kobayashi
, and
R. D.
Amos
,
J. Phys. Chem. B
110
,
15624
(
2006
).
33.
M.
Etinski
,
M.
Petkovic
, and
M.
Ristic
,
J. Serb. Chem. Soc.
78
,
1775
(
2013
).
34.
A.
Sirohiwal
,
R.
Berraud-Pache
,
F.
Neese
,
R.
Izsák
, and
D.
Pantazis
,
J. Phys. Chem. B
124
(
2020
).
35.
J.
Hasegawa
,
Y.
Ozeki
,
K.
Ohkawa
,
M.
Hada
, and
H.
Nakatsuji
,
J. Phys. Chem. B
102
,
1320
(
1998
).
36.
J.
Hasegawa
and
H.
Nakatsuji
,
J. Phys. Chem. B
102
,
10420
(
1998
).
37.
Y.
Kitagawa
,
K.
Matsuda
, and
J.-y.
Hasegawa
,
Biophys. Chem.
159
,
227
(
2011
).
38.
A. E.
Masunov
,
Int. J. Quantum Chem.
110
,
3095
(
2010
).
39.
N.
Mardirossian
and
M.
Head-Gordon
,
Mol. Phys.
115
,
2315
(
2017
).
40.
D.
Jacquemin
,
A.
Planchat
,
C.
Adamo
, and
B.
Mennucci
,
J. Chem. Theory Comput.
8
,
2359
(
2012
).
41.
D.
Grabarek
and
T.
Andruniów
,
J. Chem. Theory Comput.
15
,
490
(
2019
).
42.
Y.
Shao
,
Y.
Mei
,
D.
Sundholm
, and
V. R. I.
Kaila
,
J. Chem. Theory Comput.
16
,
587
(
2020
).
43.
D.
Jacquemin
,
E. A.
Perpète
,
G. E.
Scuseria
,
I.
Ciofini
, and
C.
Adamo
,
J. Chem. Theory Comput.
4
,
123
(
2008
).
44.
Y.
Li
,
Z.-L.
Cai
, and
M.
Chen
,
J. Phys. Chem. B
117
,
11309
(
2013
).
45.
N.
Zamzam
and
J. J.
van Thor
,
Molecules
24
,
1326
(
2019
).
46.
K.
Okuno
,
Y.
Shigeta
,
R.
Kishi
,
H.
Miyasaka
, and
M.
Nakano
,
J. Photochem. Photobiol., A
235
,
29
(
2012
).
47.
K.
Kornobis
,
N.
Kumar
,
P.
Lodowski
,
M.
Jaworska
,
P.
Piecuch
,
J. J.
Lutz
,
B. M.
Wong
, and
P. M.
Kozlowski
,
J. Comput. Chem.
34
,
987
(
2013
).
48.
M.
Uudsemaa
,
A.
Trummal
,
S.
de Reguardati
,
P. R.
Callis
, and
A.
Rebane
,
Phys. Chem. Chem. Phys.
19
,
28824
(
2017
).
49.
K.
Saito
,
T.
Suzuki
, and
H.
Ishikita
,
J. Photochem. Photobiol., A
358
,
422
(
2018
).
50.
S.
Mukamel
,
Principles of Nonlinear Optical Spectroscopy
(
Oxford University Press
,
1995
).
51.
L.
Fiedor
,
A.
Kania
,
B.
Myśliwa-Kurdziel
,
Ł.
Orzeł
, and
G.
Stochel
,
Biochim. Biophys. Acta, Bioenerg.
1777
,
1491
(
2008
).
52.
B. M.
Wong
and
T. H.
Hsieh
,
J. Chem. Theory Comput.
6
,
3704
(
2010
).
53.
J.
Song
,
F.
Gao
, and
W.
Liang
,
Comput. Theor. Chem.
965
,
53
(
2011
).
54.
M. P.
Balanay
and
D. H.
Kim
,
J. Phys. Chem. C
115
,
19424
(
2011
).
55.
A.
V Kityk
,
Spectrochim. Acta, Part A
128
,
370
(
2014
).
56.
O. S.
Bokareva
,
G.
Grell
,
S. I.
Bokarev
, and
O.
Kühn
,
J. Chem. Theory Comput.
11
,
1700
(
2015
).
57.
M. B.
Oviedo
,
N. V.
Ilawe
, and
B. M.
Wong
,
J. Chem. Theory Comput.
12
,
3593
(
2016
).
58.
Z.
Hu
,
B.
Zhou
,
Z.
Sun
, and
H.
Sun
,
J. Comput. Chem.
38
,
569
(
2017
).
59.
C.
Wang
and
Q.
Zhang
,
J. Phys. Chem. C
123
,
4407
(
2018
).
60.
S.
Bhandari
and
B. D.
Dunietz
,
J. Chem. Theory Comput.
15
,
4305
(
2019
).
61.
T.
Kosugi
and
S.
Hayashi
,
J. Chem. Theory Comput.
8
,
322
(
2012
).
62.
T.
Kosugi
and
S.
Hayashi
,
J. Am. Chem. Soc.
134
,
7045
(
2012
).
63.
C. I.
Bayly
,
P.
Cieplak
,
W.
Cornell
, and
P. A.
Kollman
,
J. Phys. Chem.
97
,
10269
(
1993
).
64.
T.
Yanai
,
D. P.
Tew
, and
N. C.
Handy
,
Chem. Phys. Lett.
393
,
51
(
2004
).
65.
M. J. G.
Peach
,
T.
Helgaker
,
P.
Sałek
,
T. W.
Keal
,
O. B.
Lutnæs
,
D. J.
Tozer
, and
N. C.
Handy
,
Phys. Chem. Chem. Phys.
8
,
558
(
2006
).
66.
L. A.
Curtiss
,
K.
Raghavachari
,
G. W.
Trucks
, and
J. A.
Pople
,
J. Chem. Phys.
94
,
7221
(
1991
).
67.
L. A.
Curtiss
,
K.
Raghavachari
,
P. C.
Redfern
, and
J. A.
Pople
,
J. Chem. Phys.
106
,
1063
(
1997
).
68.
Y.
Tawada
,
T.
Tsuneda
,
S.
Yanagisawa
,
T.
Yanai
, and
K.
Hirao
,
J. Chem. Phys.
120
,
8425
(
2004
).
69.
A. J.
Cohen
,
P.
Mori-Sánchez
, and
W.
Yang
,
Science
321
,
792
(
2008
).
70.
M.
Fujiwara
and
M.
Tasumi
,
J. Phys. Chem.
90
,
250
(
1986
).
71.
Z.
Liu
,
H.
Yan
,
K.
Wang
,
T.
Kuang
,
J.
Zhang
,
L.
Gui
,
X.
An
, and
W.
Chang
,
Nature
428
,
287
(
2004
).
72.
J.
Standfuss
,
A. C.
Terwisscha van Scheltinga
,
M.
Lamborghini
, and
W.
Kühlbrandt
,
EMBO J.
24
,
919
(
2005
).
73.
K.
Kahn
and
T. C.
Bruice
,
J. Comput. Chem.
23
,
977
(
2002
).
74.
J.
Wang
,
R. M.
Wolf
,
J. W.
Caldwell
,
P. A.
Kollman
, and
D. A.
Case
,
J. Comput. Chem.
25
,
1157
(
2004
).
75.
J.-P.
Ryckaert
,
G.
Ciccotti
, and
H. J. C.
Berendsen
,
J. Comput. Phys.
23
,
327
(
1977
).
76.
R. E.
Duke
,
H.
Gohlke
,
A. W.
Goetz
,
S.
Gusarov
,
N.
Homeyer
,
P.
Janowski
,
J.
Kaus
,
I.
Kolossváry
,
A.
Kovalenko
,
T. S.
Lee
 et al.,
Amber 14
(
University of California
,
San Francisco, CA
,
2014
).
77.
J. W.
Ponder
 et al.,
TINKER: Software Tools for Molecular Design
(
Washington University School of Medicine
,
St. Louis, MO
,
2004
), Vol. 3.
78.
M. W.
Schmidt
,
K. K.
Baldridge
,
J. A.
Boatz
,
S. T.
Elbert
,
M. S.
Gordon
,
J. H.
Jensen
,
S.
Koseki
,
N.
Matsunaga
,
K. A.
Nguyen
,
S.
Su
 et al.,
J. Comput. Chem.
14
,
1347
(
1993
).
79.
M.
Ferrario
,
M.
Haughney
,
I. R.
McDonald
, and
M. L.
Klein
,
J. Chem. Phys.
93
,
5156
(
1990
).
80.
W. L.
Jorgensen
,
D. S.
Maxwell
, and
J.
Tirado-Rives
,
J. Am. Chem. Soc.
118
,
11225
(
1996
).
81.
J. R.
Reimers
,
Z.-L.
Cai
,
R.
Kobayashi
,
M.
Rätsep
,
A.
Freiberg
, and
E.
Krausz
,
Sci. Rep.
3
,
2761
(
2013
).
82.
H. K.
Lichtenthaler
and
C.
Buschmann
,
Curr. Protoc. Food Anal. Chem.
1
,
F4.3.1
(
2001
).
83.
K.
Saito
,
K.
Mitsuhashi
, and
H.
Ishikita
,
J. Photochem. Photobiol., A
402
,
112799
(
2020
).
84.
A. R.
Wellburn
,
J. Plant Physiol.
144
,
307
(
1994
).
85.
M. A.
Rohrdanz
and
J. M.
Herbert
,
J. Chem. Phys.
129
,
034107
(
2008
).
86.
K.
Sauer
,
J. R. L.
Smith
, and
A. J.
Schultz
,
J. Am. Chem. Soc.
88
,
2681
(
1966
).
87.
S.
Mukamel
,
Principles of Nonlinear Optical Spectroscopy
(
Oxford University Press on Demand
,
1999
).
88.
K.
Saito
,
K.
Mukai
, and
H.
Sumi
,
Chem. Phys. Lett.
401
,
122
(
2005
).
89.
X.
Wei
,
X.
Su
,
P.
Cao
,
X.
Liu
,
W.
Chang
,
M.
Li
,
X.
Zhang
, and
Z.
Liu
,
Nature
534
,
69
(
2016
).

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