Carotenoids in Photosynthesis
Frank, H. A.; Brudvig, G. W. Biochemistry 2004, 43, 8607-8615.
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quenching triplet (B)Chl excited states
direct role in scavenging of singlet oxygen
deactivation of Chl excited states (NPQ)
redox activity in PSII reaction centers
antenna chromophores for the midvisible part of the solar spectrum
β-carotene
LHCII trimer (2BHW.pdb)
Standfuss et al. EMBO J. 2005, 24, 919.
Excitation Energy Transfer
from Carotenoids to Chlorophylls
Carotenoids
S2
11Bu+
S1
21Ag−
A
S0
(B)Chls
Qx
Qy
F T1
11Ag−
A
F
S0
Optical transitions between the carotenoid S₀ and S₁ states
are forbidden by symmetry (C2h point group).
Birge, R. R. Acc. Chem. Res. 1986, 19, 138-146.
T1
Peridinin–Chlorophyll a Protein (1PPR)
Peridinin
Hofmann et al. Science 1996, 272, 1788.
Intramolecular Charge Transfer in Peridinin
Hypothesis: The S₁ state of peridinin enhances energy transfer to the Qy state
of chlorophyll a by obtaining an intramolecular charge-transfer (ICT) character.
Ilagan et al. Biochemistry 2006, 45, 14052.
Third-Order Nonlinear Spectroscopy
Stimulated photon-echo and transient-grating spectroscopy
k
k
with optical heterodyne detection.
LO
k2
1
t
signal
ND
Sample
1 and 2
DO
WP (τ)
β-carotene
3 and LO
Miller and coworkers, Proc. Natl. Acad. Sci. U.S.A. 2001, 98, 6110.
Fleming and coworkers, J. Chem. Phys. 2004, 121, 4221.
Scherer and coworkers, J. Chem. Phys. 2006, 124, 194904.
k3
T
ks
t
Fourier Transform Spectral Interferometry
Isolation of the third-order nonlinear signal as the interference term at tLO
Complex
Signal (Real)
FT-1
Window at tLO
Complex
e
-iwt LO -f
Phasing
Real component = Absorption
Imaginary component = Dispersion
FT
β-carotene
Heterodyne transient-grating signal in benzonitrile
S2
16 fs
I
142 fs
9 ps / 12 ps
S1
S0
β-carotene
Heterodyne transient-grating signal in benzonitrile
S2
16 fs
I
142 fs
9 ps / 12 ps
S1
An intermediate state is formed from the initially formed S₂ state in 16 fs.
S0
β-carotene
Heterodyne transient-grating signal in benzonitrile
S2
16 fs
I
142 fs
9 ps / 12 ps
S1
An intermediate state is formed from the initially formed S₂ state in 16 fs.
The intermediate decays to the S₁ state in 142 fs, which is comparable to the
fluorescence lifetime detected in upconversion experiments.
S0
β-carotene
Heterodyne transient-grating signal in benzonitrile
S2
16 fs
I
142 fs
9 ps / 12 ps
S1
S0
The dispersion and absorption recovery time constants show that a "hot" or
conformationally displaced ground-state ensemble is produced by nonradiative
decay of the S₁ state.
Xu et al. J. Chem. Phys. 2002, 116, 9333.
Peridinin
Heterodyne transient-grating signal in methanol
S2
31 fs
I
615 fs
7 ps / 11 ps
S1
S0
Peridinin
Heterodyne transient-grating signal in methanol
S2
31 fs
I
615 fs
7 ps / 11 ps
S1
S0
The decay of the intermediate is
strongly dependent on the polar
solvation timescale.
Solvent
τpolar
S₂
I
S₁
ethyl acetate
2.5 ps
23 fs
160 fs
85 ps / 150 ps
methanol
6.2 ps
31 fs
615 fs
7 ps / 11 ps
2-propanol
220 ps
35 fs
1600 fs
29 ps / 49 ps
Peridinin
Heterodyne transient-grating signal in methanol
S2
31 fs
I
615 fs
7 ps / 11 ps
S1
S0
The decay of the intermediate is
strongly dependent on the polar
solvation timescale.
But the S₁ state lifetime is
dramatically lengthened as the
polarity of the solvent decreases.
Bautista et al.
J. Phys. Chem. B 1999, 103, 8751.
Solvent
Polarity S₂
I
S₁
ethyl acetate
0.626
23 fs
160 fs
85 ps / 150 ps
methanol
0.913
31 fs
615 fs
7 ps / 11 ps
2-propanol
0.852
35 fs
1600 fs
29 ps / 49 ps
Peridinin–Chlorophyll a Protein
Heterodyne transient-grating signal
31 fs
S2
500 fs
I
16 ps / 16 ps
S1
3 ps
200 fs
Qx
Qy
The intermediate state is the energy-transfer donor to the Qx state of Chl a.
S0
Peridinin–Chlorophyll a Protein
Heterodyne transient-grating signal
31 fs
S2
500 fs
I
16 ps / 16 ps
S1
S0
3 ps
200 fs
Qx
Qy
The intermediate state is the energy-transfer donor to the Qx state of Chl a.
The absorption and dispersion components for the decay of S₁ have the same
time constant, so conformational relaxation does not make a strong contribution
to the recovery to the photoselected ground state.
β-carotene
Time-resolved transient grating spectra in benzonitrile
-10 fs
0 fs
25 fs
Re [Es]
50 fs
75 fs
100 fs
200 fs
1 ps
500
510
520
530
Wavelength (nm)
540
550
S2
16 fs
I
142 fs
9 ps / 12 ps
S1
S0
The S₂ state decays as the stimulated
emission contribution to the signal
shifts irreversibly to the red.
β-carotene
Time-resolved transient grating spectra in benzonitrile
-10 fs
0 fs
25 fs
Re [Es]
50 fs
75 fs
100 fs
200 fs
1 ps
500
510
520
530
Wavelength (nm)
540
550
S2
16 fs
I
142 fs
9 ps / 12 ps
S1
S0
The S₂ state decays as the stimulated
emission contribution to the signal
shifts irreversibly to the red.
The ESA spectrum shifts to the red as
the intermediate forms, and then it
shifts back to the blue as the S₁ state
forms.
β-carotene
Time-resolved transient grating spectra in benzonitrile
-10 fs
0 fs
25 fs
Re [Es]
50 fs
75 fs
S2
16 fs
I
142 fs
9 ps / 12 ps
S1
S0
The S₂ state decays as the stimulated
emission contribution to the signal
shifts irreversibly to the red.
The ESA spectrum shifts to the red as
the intermediate forms, and then it
shifts back to the blue as the S₁ state
forms.
100 fs
200 fs
1 ps
500
510
520
530
Wavelength (nm)
540
550
Similar ESA dynamics (and the same
time constants) are observed in the
ESA in the red and near-IR part of the
spectrum.
Cerullo et al. Science 2002, 298, 2395.
Four-Mode Dynamics
Four coordinates control the
nonradiative decay of β-carotene and
peridinin in solution.
Sanchez-Galvez, A.; Hunt, P.; Robb, M. A.;
Olivucci, M.; Vreven, T.; Schlegel, H. B.
J. Am. Chem. Soc. 2000, 122, 2911-2924.
Four-Mode Dynamics
Four coordinates control the
nonradiative decay of β-carotene and
peridinin in solution.
1. Bond-alternation (C–C, C=C)
coordinates in the Franck–Condon
region
Sanchez-Galvez, A.; Hunt, P.; Robb, M. A.;
Olivucci, M.; Vreven, T.; Schlegel, H. B.
J. Am. Chem. Soc. 2000, 122, 2911-2924.
Four-Mode Dynamics
Four coordinates control the
nonradiative decay of β-carotene and
peridinin in solution.
1. Bond-alternation (C–C, C=C)
coordinates in the Franck–Condon
region
2. Torsional coordinates (φ) over the
S₂-state barrier and to a twisted
minimum
Sanchez-Galvez, A.; Hunt, P.; Robb, M. A.;
Olivucci, M.; Vreven, T.; Schlegel, H. B.
J. Am. Chem. Soc. 2000, 122, 2911-2924.
Four-Mode Dynamics
Four coordinates control the
nonradiative decay of β-carotene and
peridinin in solution.
1. Bond-alternation (C–C, C=C)
coordinates in the Franck–Condon
region
2. Torsional coordinates (φ) over the
S₂-state barrier and to a twisted
minimum
3. Out-of-plane motions (α) that
produce a pyramidal structure in the
S₁ state with enhanced ICT character.
Sanchez-Galvez, A.; Hunt, P.; Robb, M. A.;
Olivucci, M.; Vreven, T.; Schlegel, H. B.
J. Am. Chem. Soc. 2000, 122, 2911-2924.
Levine, B.; Martínez, T. J.
Annu. Rev. Phys. Chem. 2007, 58, 613.
Four-Mode Dynamics
Four coordinates control the
nonradiative decay of β-carotene and
peridinin in solution.
1. Bond-alternation (C–C, C=C)
coordinates in the Franck–Condon
region
2. Torsional coordinates (φ) over the
S₂-state barrier and to a twisted
minimum
3. Out-of-plane motions (α) that
produce a pyramidal structure in the
S₁ state with enhanced ICT character.
4. Solvent motions that are coupled to
formation of intramolecular chargetransfer character near the the
twisted minimum.
Sanchez-Galvez, A.; Hunt, P.; Robb, M. A.;
Olivucci, M.; Vreven, T.; Schlegel, H. B.
J. Am. Chem. Soc. 2000, 122, 2911-2924.
Levine, B.; Martínez, T. J.
Annu. Rev. Phys. Chem. 2007, 58, 613.
Malhado, J. P.; Spezia, R.; Hynes, J. T.
J. Phys. Chem. A 2011, 115, 3720-3735.
-10 fs
Peridinin–Chlorophyll a Protein
0 fs
Time-resolved transient grating spectra
S2
31 fs
I
500 fs
16 ps / 16 ps50 fs
S1
S0 PB
-10
75 fs
0 fs
The earliest PCP spectra are
comparable in shape to the 50 fs1000 fs
peridinin/methanol spectrum.
25 fs
25 fs
200
50 fs
75 fs
Re [Es]
Re [Es]
-10 fs
Re [Es]
PB
25 fs
500
50
fs
1 ps
510
520
530
540
75 fs550
Wavelength (nm)
100 fs
100 fs
200 fs
1 ps
500
510
520
530
Wavelength (nm)
540
550
The structure of peridinin in PCP is like
200 fs
that for the twisted S₂ state in
solution.
1 ps
500
510
520
530
Wavelength (nm)
540
550
Binding-Site Control of Dynamics in PCP
Photochemical Properties of Peridinin
M
bo
str
co
af
ex
ad
sta
co
po
of
ve
un
bo
the
the
ch
the
ca
de
em
ex
S1
po
rec
ca
sta
an
an
in
sh
wh
ch
The X-ray crystal structure suggests that
a twisted and kinked structure is favored
by the peridinin binding site in PCP.
Figure 1. Structure of the pigments associated with one-third of the
trimeric minimal unit comprising the PCP complex is shown in A based
on PDB entry 1PPR (Hofmann, E.; Wrench, P. M.; Sharples, F. P.;
Hiller, R. G.; Welte, W.; Diederichs, K. Science 1996, 272, 1788). The
peridinin molecules are colored to reflect the pseudo 2-fold axis that
runs vertically through the center of the protein. The peridinin molecules
Hofmann et al. Science 1996, 272, 1788.
Shima et al., J. Phys. Chem. A 107, 8052 (2003).
Conclusions and Next Steps
Conclusions and Next Steps
1. In PCP, the twisted S₂ state intermediate serves as the
energy-transfer donor to the Chl a Qx state.
Conclusions and Next Steps
1. In PCP, the twisted S₂ state intermediate serves as the
energy-transfer donor to the Chl a Qx state.
2. The S₁ state of peridinin may obtain an enhanced ICT
character by forming a kinked (pyramidal) conformation.
Conclusions and Next Steps
1. In PCP, the twisted S₂ state intermediate serves as the
energy-transfer donor to the Chl a Qx state.
2. The S₁ state of peridinin may obtain an enhanced ICT
character by forming a kinked (pyramidal) conformation.
3. The structure of the peridinin-binding pocket favors a
twisted and kinked ground-state conformer.
Conclusions and Next Steps
1. In PCP, the twisted S₂ state intermediate serves as the
energy-transfer donor to the Chl a Qx state.
2. The S₁ state of peridinin may obtain an enhanced ICT
character by forming a kinked (pyramidal) conformation.
3. The structure of the peridinin-binding pocket favors a
twisted and kinked ground-state conformer.
Broadband 2D spectra to characterize the energy correlation of
the twisted/pyramidal intermediates with the S₂ state and with
the Chl a acceptors in PCP.
Acknowledgment
Amy LaFountain (Uconn)
Professor Andrew Moran (UNC Chapel Hill)
Professor Ben Levine (MSU)
NSF MCB-0920101
DOE BES DE-SC0010847