Intramolecular charge-transfer enhances energy transfer efficiency in a carotenoid-reconstituted light-harvesting 1 complex of purple photosynthetic bacteria

In bacterial photosynthesis, the excitation energy transfer from carotenoids to bacteriochlorophyll a has a significant impact on the overall efficiency of the primary photosynthetic process. This efficiency can be enhanced when the involved carotenoid has intramolecular charge-transfer character.
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     Photosynthesis is the only major biochemical process on Earth that can use solar energy to power the conversion of atmospheric carbon dioxide into carbohydrates. This process begins by the absorption of that solar energy by the light harvesting complexes. There is a lot to learnt from how Nature has evolved these light harvesting systems, if we want to produce robust artificial light harvesters as part of systems designed to produce clean energy. In this study we used one of the photosynthetic bacteria, Rhodospirillum (Rsp.) rubrum strain G9+. This bacterium is the mutant of the wild-type strain of Rsp. rubrum strain S1, and it does not produce the photosynthetic pigment called carotenoid. Rsp. rubrum strain S1 biosynthesizes the carotenoid called spirilloxanthin, but the efficiency of EET from spirilloxanthin to bacteriochlorophyll (Bchl) a in its LH1 light-harvesting pigment-protein complex is only 28 %.1 On the other hand, some of the marine algae is known to have much higher EET efficiency (up to 90 %)2 from carotenoid to chlorophyll a because they transfer the energy through the intramolecular charge transfer (ICT) excited state of carotenoid. The original question of this work was “Could we improve the EET efficiency in the bacterial LH1 complex of the Rsp. rubrum by reconstituting the carotenoid which generates the ICT excited sate?”. To answer this question, we first tried to create the novel photosynthetic antenna by incorporating the carotenoid, β-apo-8'-carotenal to the LH1 core antenna pigment-protein complex of Rsp. rubrum strain G9+, a carotenoidless mutant. β-apo-8'-carotenal is the higher plant carotenoid and is known to generate the ICT excited state. This involved a careful repetitive effort to learn how to achieve this reconstitution. Fortunately, once we could successfully reconstitute this carotenoid into LH1, we measured the steady-state absorption, fluorescence, and fluorescence excitation spectra to test whether β-apo-8'-carotenal truly has the light-harvesting function in the reconstituted LH1 (hereafter we abbreviate this complex as Reβapo) (see Figure 1).

Figure 1. The 1 – T (transmission) spectra (black solid line), fluorescence spectra (green solid line) and fluorescence excitation spectra (red solid line) of Rebapo. The calculated EET efficiency (grey solid line) is also shown.

     We found that the EET efficiency of β-apo-8'-carotenal in Reβapo was up to 79 %. Comparing to the wild type LH1, this improvement is surprising. In addition, we measured the femtosecond time-resolved absorption spectra to investigate the EET dynamics in Reβapo. We applied the global and target analysis to the entire observed datasets of the transient absorption spectra in the visible to near infrared spectral region to investigate the lifetime of each excited-state component and could find the model that can fully explain the EET pathways in Reβapo. This was indeed painstaking work. When we first submitted this paper, we thought that β-apo-8'-carotenal in Reβapo has two forms (red and blue forms) of S1/ICT excited states and both states transfer the energy to the Qy state of Bchl a. Here, the S1/ICT excited state is known as the coupling state of the lowest excited singlet (S1) state and the ICT excited state of carbonyl containing carotenoids. However, this turned out to be wrong. One of the reviewers gave us a very perceptive comment and we analyzed all the data again. Then we were finally able to arrive at the really simple and reasonable conclusion. The EET from carotenoid to Bchl a was performed mainly via the S1/ICT excited state of β-apo-8'-carotenal (see Figure 2), and we did not have to suppose blue and red forms of the S1/ICT state of β-apo-8'-carotenal. This conclusion revealed the simple answer to the original question. The highly efficient EET from β-apo-8'-carotenal to Bchl a in Reβapo was primarily mediated by the S1/ICT excited state of β-apo-8'-carotenal, a result which suggests that the EET efficiency from carotenoid to Bchl a in the LH1 of Rsp. rubrum can be improved by harnessing the ICT character of carotenoids. We also measured the sub-nano second time-resolved absorption spectra and confirmed that β-apo-8'-carotenal in Reβapo also has the photoprotective function. This means that Reβapo is a robust pigment-protein complex.

Figure 2. The EET pathways in Reβapo.

     This study clearly demonstrates the strategy of how to improve the EET efficiency of photosynthetic antenna. This is expected to make a substantial contribution to the artificial photosynthesis research.

     For more information please be sure to check out the full paper on the website: https://www.nature.com/articles/s42004-022-00749-6.

References

  1. Nakagawa, K. et al. Probing the effect of the binding site on the electrostatic behavior of a series of carotenoids reconstituted into the light-harvesting 1 complex from purple photosynthetic bacterium Rhodospirillum rubrum detected by Stark spectroscopy. J. Phys. Chem. B 112, 9467-9475 (2008).
  2. Kosumi, D. et al. Excitation energy-transfer dynamics of brown algal photosynthetic antennas. J. Phys. Chem. Lett. 3, 2659-2664 (2012).

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