Energy transfer processes and coherent phenomena in the fucoxanthin–chlorophyll protein complex, which is responsible for the light harvesting function in marine algae diatoms, were investigated at 77 K by using two-dimensional electronic spectroscopy. Experiments performed on femtosecond and picosecond timescales led to separation of spectral dynamics, witnessing evolutions of coherence and population states of the system in the spectral region of Qy transitions of chlorophylls a and c. Analysis of the coherence dynamics allowed us to identify chlorophyll (Chl) a and fucoxanthin intramolecular vibrations dominating over the first few picoseconds. Closer inspection of the spectral region of the Qy transition of Chl c revealed previously not identified, mutually non-interacting chlorophyll c states participating in femtosecond or picosecond energy transfer to the Chl a molecules. Consideration of separated coherent and incoherent dynamics allowed us to hypothesize the vibrations-assisted coherent energy transfer between Chl c and Chl a and the overall spatial arrangement of chlorophyll molecules.

1.
P. G.
Falkowski
,
R. T.
Barber
, and
V.
Smetacek
,
Science
281
,
200
(
1998
).
2.
C. B.
Field
,
M. J.
Behrenfeld
,
J. T.
Randerson
, and
P.
Falkowski
,
Science
281
,
237
(
1998
).
4.
M.
Eppard
and
E.
Rhiel
,
Mol. Gen. Genet.
260
,
335
(
1998
).
5.
E.
Papagiannakis
,
I. H. M.
van Stokkum
,
H.
Fey
,
C.
Büchel
, and
R.
van Grondelle
,
Photosynth. Res.
86
,
241
(
2005
).
6.
C.
Wilhelm
,
C.
Büchel
,
J.
Fisahn
,
R.
Goss
,
T.
Jakob
,
J.
LaRoche
,
J.
Lavaud
,
M.
Lohr
,
U.
Riebesell
,
K.
Stehfest
,
K.
Valentin
, and
P. G.
Kroth
,
Protist
157
,
91
(
2006
).
7.
L.
Premvardhan
,
B.
Robert
,
A.
Beer
, and
C.
Büchel
,
Biochim. Biophys. Acta, Bioenerg.
1797
,
1647
(
2010
).
8.
N.
Gildenhoff
,
J.
Herz
,
K.
Gundermann
,
C.
Büchel
, and
J.
Wachtveitl
,
Chem. Phys.
373
,
104
(
2010
).
9.
L.
Premvardhan
,
L.
Bordes
,
A.
Beer
,
C.
Büchel
, and
B.
Robert
,
J. Phys. Chem. B
113
,
12565
(
2009
).
10.
Z.
Liu
,
H.
Yan
,
K.
Wang
,
T.
Kuang
,
J.
Zhang
,
L.
Gui
,
X.
An
, and
W.
Chang
,
Nature
428
,
287
(
2004
).
11.
R.
Croce
and
H.
van Amerongen
,
Nat. Chem. Biol.
10
,
492
(
2014
).
12.
E.
Songaila
,
R.
Augulis
,
A.
Gelzinis
,
V.
Butkus
,
A.
Gall
,
C.
Büchel
,
B.
Robert
,
D.
Zigmantas
,
D.
Abramavicius
, and
L.
Valkunas
,
J. Phys. Chem. Lett.
4
,
3590
(
2013
).
13.
T.
Brixner
,
J.
Stenger
,
H. M.
Vaswani
,
M.
Cho
,
R. E.
Blankenship
, and
G. R.
Fleming
,
Nature
434
,
625
(
2005
).
14.
G. S.
Schlau-Cohen
,
T. R.
Calhoun
,
N. S.
Ginsberg
,
E. L.
Read
,
M.
Ballottari
,
R.
Bassi
,
R.
van Grondelle
, and
G. R.
Fleming
,
J. Phys. Chem. B
113
,
15352
(
2009
).
15.
A.
Gelzinis
,
L.
Valkunas
,
F. D.
Fuller
,
J. P.
Ogilvie
,
S.
Mukamel
, and
D.
Abramavicius
,
New J. Phys.
15
,
075013
(
2013
).
16.
F. D.
Fuller
,
J.
Pan
,
A.
Gelzinis
,
V.
Butkus
,
S. S.
Senlik
,
D. E.
Wilcox
,
C. F.
Yocum
,
L.
Valkunas
,
D.
Abramavicius
, and
J. P.
Ogilvie
,
Nat. Chem.
6
,
706
(
2014
).
17.
E.
Romero
,
R.
Augulis
,
V. I.
Novoderezhkin
,
M.
Ferretti
,
J.
Thieme
,
D.
Zigmantas
, and
R.
van Grondelle
,
Nat. Phys.
10
,
676
(
2014
).
18.
H.
Lee
,
Y.-C.
Cheng
, and
G.
Fleming
,
Science
316
,
1462
(
2007
).
19.
D.
Zigmantas
,
E. L.
Read
,
T.
Mančal
,
T.
Brixner
,
A. T.
Gardiner
,
R. J.
Cogdell
, and
G. R.
Fleming
,
Proc. Natl. Acad. Sci. U. S. A.
103
,
12672
(
2006
).
20.
J.
Dostál
,
T.
Mančal
,
R.
Augulis
,
F.
Vácha
,
J.
Pšenčik
, and
D.
Zigmantas
,
J. Am. Chem. Soc.
134
,
11611
(
2012
).
21.
J. M.
Anna
,
E. E.
Ostroumov
,
K.
Maghlaoui
,
J.
Barber
, and
G. D.
Scholes
,
J. Phys. Chem. Lett.
3
,
3677
(
2012
).
22.
E.
Collini
and
G. D.
Scholes
,
Science
323
,
369
(
2009
).
23.
F.
Milota
,
J.
Sperling
,
A.
Nemeth
, and
H. F.
Kauffmann
,
Chem. Phys.
357
,
45
(
2009
).
24.
D. B.
Turner
,
Y.
Hassan
, and
G. D.
Scholes
,
Nano Lett.
12
,
880
(
2012
).
25.
A.
Gelzinis
,
V.
Butkus
,
E.
Songaila
,
R.
Augulis
,
A.
Gall
,
C.
Büchel
,
B.
Robert
,
D.
Abramavicius
,
D.
Zigmantas
, and
L.
Valkunas
,
Biochim. Biophys. Acta, Bioenerg.
1847
,
241
(
2015
).
26.
C.
Büchel
,
Biochemistry
42
,
13027
(
2003
).
27.
T.
Brixner
,
I. V.
Stiopkin
, and
G. R.
Fleming
,
Opt. Lett.
29
,
884
(
2004
).
28.
R.
Augulis
and
D.
Zigmantas
,
Opt. Express
19
,
13126
(
2011
).
29.
J. D.
Hybl
,
A. W.
Albrecht
,
S. M. G.
Faeder
, and
D. M.
Jonas
,
Chem. Phys. Lett.
297
,
307
(
1998
).
31.
J. K.
Gillie
and
G. J.
Small
,
J. Phys. Chem.
93
,
1620
(
1989
).
32.
V.
Butkus
,
A.
Gelzinis
, and
L.
Valkunas
,
J. Phys. Chem. A
115
,
3876
(
2011
).
33.
D.
Abramavicius
,
Europhys. Lett.
101
,
57007
(
2013
).
34.
J.
Han
,
H.
Zhang
, and
D.
Abramavicius
,
J. Chem. Phys.
139
,
034313
(
2013
).
35.
J.
Du
,
T.
Teramoto
,
K.
Nakata
,
E.
Tokunaga
, and
T.
Kobayashi
,
Biophys. J.
101
,
995
(
2011
).
36.
G.
Panitchayangkoon
,
D.
Voronine
,
D.
Abramavicius
,
J.
Caram
,
N.
Lewis
,
S.
Mukamel
, and
G.
Engel
,
Proc. Natl. Acad. Sci. U. S. A.
108
,
20908
(
2011
).
37.
H.
Li
,
A. D.
Bristow
,
M. E.
Siemens
,
G.
Moody
, and
S. T.
Cundiff
,
Nat. Commun.
4
,
1390
(
2013
).
38.
V.
Butkus
,
D.
Zigmantas
,
L.
Valkunas
, and
D.
Abramavicius
,
Chem. Phys. Lett.
545
,
40
(
2012
).
39.
J.
Seibt
and
T.
Pullerits
,
J. Phys. Chem. C
117
,
18728
(
2013
).
40.
M.
Ferretti
,
V. I.
Novoderezhkin
,
E.
Romero
,
R.
Augulis
,
A.
Pandit
,
D.
Zigmantas
, and
R.
Grondelle
,
Phys. Chem. Chem. Phys.
16
,
9930
(
2014
).
41.
F. V. A.
Camargo
,
H. L.
Anderson
,
S. R.
Meech
, and
I. A.
Heisler
,
J. Phys. Chem. A
119
,
95
(
2014
).
42.
D.
Abramavicius
,
V.
Butkus
,
J.
Bujokas
, and
L.
Valkunas
,
Chem. Phys.
372
,
22
(
2010
).
43.
D.
Abramavicius
,
L.
Valkunas
, and
S.
Mukamel
,
Europhys. Lett.
80
,
17005
(
2007
).
44.
P.
Hamm
and
M.
Zanni
,
Concepts and Methods of 2D Infrared Spectroscopy
(
Cambridge University Press
,
2011
).
45.
V.
Butkus
,
J.
Alster
,
E.
Bašinskaitė
,
R.
Augulis
,
P.
Neuhaus
,
L.
Valkunas
,
H. L.
Anderson
,
D.
Abramavicius
, and
D.
Zigmantas
Diversity of coherences and origin of electronic transitions of supermolecular nanoring
,” preprint arXiv:1503.00870 (2015).
46.
V. I.
Novoderezhkin
,
E. G.
Andrizhiyevskaya
,
J. P.
Dekker
, and
R.
van Grondelle
,
Biophys. J.
89
,
1464
(
2005
).
47.
V.
Butkus
,
D.
Zigmantas
,
D.
Abramavicius
, and
L.
Valkunas
, “
Role of coherent vibrations in energy transfer and conversion in photosynthetic pigment-protein complexes
,”
Photosynth. Res.
587
,
93
(published online) (
2013
).
48.
V.
Butkus
,
L.
Valkunas
, and
D.
Abramavicius
,
J. Chem. Phys.
140
,
034306
(
2014
).
49.
A.
Telfer
,
A. A.
Pascal
,
L.
Bordes
,
J.
Barber
, and
B.
Robert
,
J. Phys. Chem. B
114
,
2255
(
2010
).
50.
A.
Chenu
,
N.
Christensson
,
H. F.
Kauffmann
, and
T.
Mančal
,
Sci. Rep.
3
,
2029
(
2013
).
51.
O.
Rancova
and
D.
Abramavicius
,
J. Phys. Chem. B
118
,
7533
(
2014
).
52.
H.
Dong
and
G. R.
Fleming
,
J. Phys. Chem. B
118
,
8956
(
2014
).
53.
D.
Kosumi
,
M.
Kita
,
R.
Fujii
,
M.
Sugisaki
,
N.
Oka
,
Y.
Takaesu
,
T.
Taira
,
M.
Iha
, and
H.
Hashimoto
,
J. Phys. Chem. Lett.
3
,
2659
(
2012
).
54.
C. D. P.
Duffy
,
J.
Chmeliov
,
M.
Macernis
,
J.
Sulskus
,
L.
Valkunas
, and
A. V.
Ruban
,
J. Phys. Chem. B
117
,
10974
(
2013
).
55.
D.
Abramavicius
and
L.
Valkunas
, “
Role of coherent vibrations in energy transfer and conversion in photosynthetic pigment-protein complexes
,”
Photosynth. Res.
(published online).
56.
F.
Caruso
,
A. W.
Chin
,
A.
Datta
,
S. F.
Huelga
, and
M. B.
Plenio
,
J. Chem. Phys.
131
,
105106
(
2009
).
57.
J.
Womick
and
A.
Moran
,
J. Phys. Chem. B
115
,
1347
(
2011
).
58.
A.
Kolli
,
E.
O’Reilly
,
G.
Scholes
, and
A.
Olaya-Castro
,
J. Chem. Phys.
137
,
174109
(
2012
).
59.
C. C.
Gradinaru
,
A. A.
Pascal
,
F.
van Mourik
,
B.
Robert
,
P.
Horton
,
R.
van Grondelle
, and
H.
van Amerongen
,
Biochemistry
37
,
1143
(
1998
).
60.
X.
Pan
,
M.
Li
,
T.
Wan
,
L.
Wang
,
C.
Jia
,
Z.
Hou
,
X.
Zhao
,
J.
Zhang
, and
W.
Chang
,
Nat. Struct. Mol. Biol.
18
,
309
(
2011
).
61.
S.
Akimoto
,
A.
Teshigahara
,
M.
Yokono
,
M.
Mimuro
,
R.
Nagao
, and
T.
Tomo
,
Biochim. Biophys. Acta, Bioenerg.
1837
,
1514
(
2014
).
You do not currently have access to this content.