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Photoprotection Mechanism of Light-harvesting Antenna Complex from Purple Bacteria Daisuke Kosumi, Tomoko Horibe, Mitsuru Sugisaki, Richard J. Cogdell, and Hideki Hashimoto J. Phys. Chem. B, Just Accepted Manuscript • DOI: 10.1021/acs.jpcb.6b00121 • Publication Date (Web): 22 Jan 2016 Downloaded from http://pubs.acs.org on January 31, 2016
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The Journal of Physical Chemistry
Photoprotection Mechanism of Light-harvesting Antenna Complex from Purple Bacteria Daisuke Kosumi1,2*, Tomoko Horibe3, Mitsuru Sugisaki4, Richard J. Cogdell5, and Hideki Hashimoto3,* 1
Institute of Pulsed Power Science, Kumamoto University, 2-39-1 Kurokami, Chuo-ku, Kumamoto,
860-8555 Japan 2
Department of Physics, Graduate School of Science and Technology, Kumamoto University
3
Department of Applied Chemistry for Environment, Faculty of Science and Technology, Kwansei
Gakuin University, 2-1, Gakuen, Sanda, Hyogo, 669-1337 Japan 4
Department of Physics, Graduate School of Science, Osaka City University, 3-3-138 Sugimoto,
Sumiyoshi-ku, Osaka 558-8585, Japan 5
Glasgow Biomedical Research Centre, University of Glasgow, 126 University Place, Glasgow, G12
8QQ, Scotland, United Kingdom *
Corresponding authors: Email:
[email protected] (D. Kosumi),
[email protected] Email:
(H. Hashimoto)
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Abstract Photosynthetic light-harvesting apparatus efficiently capture sunlight and transfer the energy to reaction centers, while they safely dissipate excess energy to surrounding environments for a protection of their organisms.
In this study, we performed pump-probe spectroscopic measurements
with a temporal window ranging from femtosecond to sub-millisecond on the purple bacterial antenna complex LH2 from Rhodobacter sphaeroides 2.4.1 to clarify its photoprotection functions. The observed excited state dynamics in the time range from sub-nanosecond to microsecond exhibits that the triplet-triplet excitation energy transfer from bacteriochlorophyll a to carotenoid takes place with a time constant of 16.7 ns.
Furthermore, ultrafast spectroscopic data suggests that a molecular
assembly of bacteriochlorophyll a in LH2 efficiently suppresses a generation of triple bacteriochlorophyll a.
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The Journal of Physical Chemistry
1. Introduction Photosynthetic apparatus capture sun-light and subsequently convert energy to electro-chemical potential.
Light-harvesting (LH) antenna complexes from purple bacteria, termed LH1 and LH2,
consist of photosynthetic pigments, carotenoid (Car) and bacteriochlorophyll (Bchl) a, which are embedded in surrounding proteins.
The three-dimensional structures of light-harvesting complexes
from purple bacteria have been determined by X-ray crystallography with an atomic resolution.1-3 Car and Bchl a molecules are closely packed by surrounding proteins nearly in a van der Waals contact and formed ring-like molecular assemblies as shown in Figs. 1(A) and (B).
In a primary
photosynthetic process of purple bacteria, Car absorbs light in the blue-green region of the spectrum and efficiently transfer the energy to nearby Bchl a.4-5
This process is termed as singlet-singlet
excitation energy transfer (EET) from Car to Bchl a.
On the other hand, excess light energy
promotes to generate triplet Bchl a, which yields harmful singlet-oxygen for photosynthetic organisms.
Thus, Cars safely quench triplet Bchl a to inhibit yields of singlet oxygen as a
photoprotection function (Fig. 1(C)).6
Photoprotection in photosynthetic systems has been
traditionally described as a triplet-triplet EET from (B)Chls to Cars.6
This reaction has been
postulated to occur in a time-scale of nanosecond, whereas its process has not been clarified yet in detail because of a limited temporal resolution.
In addition, recent ultrafast spectroscopic
investigations have suggested other photoprotective mechanisms such as ultrafast triplet generation of Cars7-10 and singlet (B)Chl quenching by Cars11-16 in photosynthetic pigment-protein complexes. Femtosecond pump-probe measurements were widely performed on photosynthetic systems to observe energy transfer dynamics taking place up to several nanoseconds with a femtosecond temporal resolution.
A flash photolysis method has been widely utilized to observe chemical
reactions in organic materials, while this procedure was usually limited in a temporal resolution of several ten nanoseconds.17-18
A time-resolved fluorescence measurement using a streak camera or a
time-correlated single-photon counting system is also a powerful tool with a higher temporal 3
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resolution (µs).19-21 is suitable only to detect optically allowed states.
However, fluorescence spectroscopy
These situations have made difficult to clarify
triplet-triplet energy transfer dynamics between carotenoids and (B)Chls in photosynthetic systems. On the other hand, several groups have recently developed pump-probe spectroscopic systems to overcome such situations.22-24
Here we introduce a novel method which covers a wide temporal
range from picosecond to sub-millisecond with a sub-ns temporal resolution and achieves a very high signal-to-noise ratio.
Combining this spectroscopic method and a femtosecond pump-probe
measurement enables us to probe excited state dynamics of materials with a wide temporal range (sub-ms) and a high time resolution (
