Singlet fission occurs through intermolecular heterofission in purple bacterial photosynthetic complexes and contributes to solar energy harvesting James Pidgeon , Shuangqing Wang, George A. Sutherland, C. Neil Hunter, Jenny Clark University of Sheffield, UK Singlet fission is the spin-allowed generation of two triplet electronic excited states from a singlet state. 1,2 Ultrafast (~100 fs) singlet fission forming long-lived (>µs) triplets has been shown to occur in light-harvesting complexes in photosynthetic purple bacteria. 3,4 Such timescales are key for applications of singlet fission, such as improving photovoltaic efficiency beyond the Shockley-Queisser limit, but the mechanism of singlet fission in these complexes is under debate. It has been hypothesised to occur on individual carotenoid molecules; a twist of the carotenoid conjugated backbone out-of-plane (giving a v 4 ≈ 980 cm -1 resonance Raman peak) is said to be the determinant for this intramolecular singlet fission. 4 As the light-harvesting complexes contain multiple carotenoids and bacteriochlorophylls in close contact, a more direct test of this hypothesis is required. We first study the orange carotenoid protein (OCP) from cyanobacteria as a means to test the intramolecular singlet fission hypothesis. OCP exists in two forms: in its orange form (OCPo), the single bound carotenoid is twisted ( v 4 resonance Raman peak present), whereas in its red form (OCPr), the carotenoid is relatively planar ( v 4 peak diminished), providing a simpler system. Using transient absorption spectroscopy, we show that there is no evidence of long-lived triplet generation through intramolecular singlet fission, despite the carotenoid twist in OCPo. We conclude that the singlet fission observed in light-harvesting complexes does not occur on single carotenoid molecules in an intramolecular scheme. 5 To determine the mechanism of singlet fission in the light-harvesting complexes, we subsequently study the RC- LH1 light-harvesting complex of the purple bacterium Rhodobacter sphaeroides binding carotenoids with different effective conjugation lengths. Using transient absorption and photoluminescence spectroscopy, we show that singlet fission proceeds through an intermolecular heterofission mechanism between adjacent carotenoid and bacteriochlorophyll molecules. We also find that singlet fission augments the energy transfer efficiency between the carotenoid and bacteriochlorophyll molecules by up to 27% (13% in wild-type RC-LH1), improving the light- harvesting function of the purple bacteria. This is in spite of the risk of oxidative damage to the organism. References 1. M. B. Smith, J. Michl, ‘Recent Advances in Singlet Fission’, Annu. Rev. Phys. Chem. 64 , 361–386 (2013). 2. A. J. Musser, J. Clark, ‘Triplet-Pair States in Organic Semiconductors’, Annu. Rev. Phys. Chem. 70 , 323–351 (2019). 3. C. C. Gradinaru, J. T. M. Kennis, E. Papagiannakis, I. H. M. van Stokkum, R. J. Cogdell, G. R. Fleming, R. A. Niederman, R. van Grondelle, ‘An unusual pathway of excitation energy deactivation in carotenoids: Singlet-to-triplet conversion on an ultrafast timescale in a photosynthetic antenna’, Proc. Natl. Acad. Sci. U.S.A. 98 , 2364–2369 (2001). 4. J. Yu, L.-M. Fu, L.-J. Yu, Y. Shi, P. Wang, Z.-Y. Wang-Otomo, J.-P. Zhang, ‘Carotenoid Singlet Fission Reactions in Bacterial Light Harvesting Complexes As Revealed by Triplet Excitation Profiles’, J. Am. Chem. Soc. 139 , 15984–15993 (2017). 5. G. A. Sutherland, J. P. Pidgeon, H. K. H. Lee, M. S. Proctor, A. Hitchcock, S. Wang, D. Chekulaev, W. C. Tsoi, M. P. Johnson, C. N. Hunter, J. Clark, ‘Twisted carotenoids do not support efficient intramolecular singlet fission in the orange carotenoid protein’, arXiv preprint arXiv:2211.13439 (2022).
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