Elucidating Low-energy Dark States in the Major Photosynthetic Light-Harvesting Antenna of Plants with 2D Electronic Spectroscopy

Charusheela Ramanana, Marco Ferrettia, Vladimir Novoderezhkinb, Rienk van Grondellea
aDepartment of Physics and Astronomy and Institute for Lasers, Life and Biophotonics, Faculty of Sciences, VU University Amsterdam, De Boelelaan 1081, 1081 HV, Amsterdam, The Netherlands; bA.N. Belozersky Institut of Physico-Chemical Biology, Moscow State University, Leninskie Gory 1, 119992, Moscow, Russia

Light-harvesting complex II (LHCII) is the most abundant photosynthetic antenna complex on earth, with the primary purpose to harvest solar light and transfer the excitation energy further into the photosynthetic assembly where it can be converted into chemical energy. LHCII further plays an essential role in protection from excess light energy, which can cause photodamage to the biological assembly. Earlier work proposes that low lying dark CT states play an essential role in this non-photochemical quenching (NPQ) process. Previously, this had been demonstrated only in in vitro model systems based on aggregation of LHCII. [1-4] However, recent results have shown that such a state may also be present in unaggregated LHCII trimers.[5]

Over the years, experimental studies have been combined with modeling to map the energy transfer processes within LHCII. In this work, we expand further on this model as well as on the understanding of possible NPQ states in this ubiquitous pigment-protein complex. We measured 2D electronic spectroscopy [6,7] of unaggregated LHCII trimers from spinach at both 77K and room temperature, with a particular emphasis on elucidating low-lying dark states. This highly sensitive technique returns spectra which correlate photoexcitation and emission frequencies, giving not only energy transfer dynamics, but also vibronic/excitonic coherences which appear as oscillatory features. We map the beating frequencies of these oscillations in LHCII and find evidence for a low-lying dark state which is coupled to a low-energy excitonic state. We use these results to further refine the model of energy transfer in LHCII.

References

[1] P. Horton, et al. FEBS Lett. 1991, 292,1.
[2] Y. Miloslavina, et al. FEBS Lett. 2008, 582, 3625−3631.
[3] A.V. Ruban, et al. Nature 2007, 450, 575−579.
[4] M. Wahadoszamen, et al. Phys. Chem. Chem. Phys. 2012, 14, 759.
[5] B. van Oort, et al. J. Phys. Chem. B 2015.
[6] G.S. Schlau-Cohen, et al. J. Phys. Chem. B 113, 15352–15363 2009.
[7] H.-G. Duan, et al. J. Phys. Chem. B 119, 12017–27 2015.