Vibronic structure of photosynthetic pigments probed by polarized two-dimensional electronic spectroscopy and ab initio calculations

Yin Song; Alexander Schubert; Elizabeth Maret; Ryan K Burdick; Barry D Dunietz; Eitan Geva; Jennifer P Ogilvie

doi:10.1039/c9sc02329a

Vibronic structure of photosynthetic pigments probed by polarized two-dimensional electronic spectroscopy and ab initio calculations

Chem Sci. 2019 Jul 3;10(35):8143-8153. doi: 10.1039/c9sc02329a. eCollection 2019 Sep 21.

Authors

Yin Song¹, Alexander Schubert^{2

3}, Elizabeth Maret⁴, Ryan K Burdick², Barry D Dunietz³, Eitan Geva², Jennifer P Ogilvie¹

Affiliations

¹ Department of Physics , University of Michigan , 450 Church St , Ann Arbor , MI 48109 , USA . Email: jogilvie@umich.edu.
² Department of Chemistry , University of Michigan , 930 N University Ave , Ann Arbor , MI 48109 , USA.
³ Department of Chemistry and Biochemistry , Kent State University , 1175 Risman Drive , Kent , OH 44242 , USA.
⁴ Applied Physics Program , University of Michigan , 450 Church St , Ann Arbor , MI 48109 , USA.

Abstract

Bacteriochlorophyll a (Bchl a) and chlorophyll a (Chl a) play important roles as light absorbers in photosynthetic antennae and participate in the initial charge-separation steps in photosynthetic reaction centers. Despite decades of study, questions remain about the interplay of electronic and vibrational states within the Q-band and its effect on the photoexcited dynamics. Here we report results of polarized two-dimensional electronic spectroscopic measurements, performed on penta-coordinated Bchl a and Chl a and their interpretation based on state-of-the-art time-dependent density functional theory calculations and vibrational mode analysis for spectral shapes. We find that the Q-band of Bchl a is comprised of two independent bands, that are assigned following the Gouterman model to Q _x and Q _y states with orthogonal transition dipole moments. However, we measure the angle to be ∼75°, a finding that is confirmed by ab initio calculations. The internal conversion rate constant from Q _x to Q _y is found to be 11 ps^-1. Unlike Bchl a, the Q-band of Chl a contains three distinct peaks with different polarizations. Ab initio calculations trace these features back to a spectral overlap between two electronic transitions and their vibrational replicas. The smaller energy gap and the mixing of vibronic states result in faster internal conversion rate constants of 38-50 ps^-1. We analyze the spectra of penta-coordinated Bchl a and Chl a to highlight the interplay between low-lying vibronic states and their relationship to photoinduced relaxation. Our findings shed new light on the photoexcited dynamics in photosynthetic systems where these chromophores are primary pigments.