In bacterial photosynthesis, the excitation energy transfer (EET) 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 (ICT) character, as found in light-harvesting systems of marine alga and diatoms. Here, we provide insights into the significance of ICT excited states following the incorporation of a higher plant carotenoid, β-apo-8'-carotenal, into the carotenoidless light-harvesting 1 (LH1) complex of the purple photosynthetic bacterium Rhodospirillum rubrum strain G9+. β-apo-8'-carotenal generates the ICT excited state in the reconstituted LH1 complex, achieving an efficiency of EET of up to 79%, which exceeds that found in the wild-type LH1 complex.

Department of Applied Chemistry for Environment Graduate School of Science and Technology Kwansei Gakuin University 1 Gakuen Uegahara Sanda Hyogo 669 1330 Japan

Institute of Industrial Nanomaterials Kumamoto University 2 39 1 Kurokami Chuou ku Kumamoto 860 8555 Japan

Institute of Molecular Cell and Systems Biology College of Medical Veterinary and Life Sciences University of Glasgow Glasgow G12 8QQ Scotland UK

Laboratory of Anoxygenic Phototrophs Institute of Microbiology Czech Academy of Sciences 379 81 Třeboň Czech Republic

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Green, B. R. & Parson, W. W. Light-Harvesting Antennas in Photosynthesis (Kluwer Academic Publishers, 2003).

Hashimoto H, Sugai Y, Uragami C, Gardiner AT, Cogdell RJ. Natural and artificial light-harvesting systems utilizing the functions of carotenoids. J. Photochem. Photobiol. C. 2015;25:46–70. doi: 10.1016/j.jphotochemrev.2015.07.004. DOI

Hunter, C. N., Daldal, F., Thurnauer, M. C. & Beatty, J. T. The Purple Phototrophic Bacteria (Springer, 2009).

Cogdell RJ, Gardiner AT, Yukihira N, Hashimoto H. Solar fuels and inspiration from photosynthesis. J. Photochem. Photobiol. A. 2018;353:645–653. doi: 10.1016/j.jphotochem.2017.09.013. DOI

Blankenship, R. E., Madigan, M. T. & Bauer, C. E. Anoxygenic Photosynthetic Bacteria (Kluwer Academic Publishers, 1995).

Tani, K. et al. Cryo-EM structure of the photosynthetic LH1-RC complex from Rhodospirillum rubrum. Biochemistry60, 2483–2491 (2021). PubMed

Hashimoto, H., Uragami, C. & Cogdell, R. J. Carotenoids in Nature Ch. 4 (Springer, 2016).

Qian P, et al. Time-dependent changes in the carotenoid composition and preferential binding of spirilloxanthin to the reaction center and anhydrorhodovibrin to the LH1 antenna complex in Rhodobium marinum. Photochem. Photobio. 2001;74:444–452. doi: 10.1562/0031-8655(2001)0740444TDCITC2.0.CO2. PubMed DOI

Kosumi D, et al. The dependence of the ultrafast relaxation kinetics of the S2 and S1 states in β-carotene homologs and lycopene on conjugation length studied by femtosecond time-resolved absorption and Kerr-gate fluorescence spectroscopies. J. Chem. Phys. 2009;130:214506. doi: 10.1063/1.3147008. PubMed DOI

Frank HA, et al. Carotenoid-to-bacteriochlorophyll singlet energy transfer in carotenoid-incorporated B850 light-harvesting complexes of Rhodobacter sphaeroides R-26.1. Photochem. Photobiol. 1993;57:49–55. doi: 10.1111/j.1751-1097.1993.tb02254.x. PubMed DOI

Desamero RZB, et al. Mechanism of energy transfer from carotenoids to bacteriochlorophyll: light-harvesting by carotenoids having different extents of π-electron conjugation incorporated into the B850 antenna complex from the carotenoidless bacterium Rhodobacter sphaeroides R-26.1. J. Phys. Chem. B. 1998;102:8151–8162. doi: 10.1021/jp980911j. DOI

Naruse M, Hashimoto H, Kuki M, Koyama Y. Triplet excitation of precursors of spirilloxanthin bound to the chromatophores of Rhodospirillum rubrum as detected by transient Raman spectroscopy. J. Mol. Struct. 1991;242:15–26. doi: 10.1016/0022-2860(91)87123-Y. DOI

Gradinaru CC, et al. 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. USA. 2001;98:2364–2369. doi: 10.1073/pnas.051501298. PubMed DOI PMC

Papagiannakis E, et al. A near-infrared transient absorption study of the excited-state dynamics of the carotenoid spirilloxanthin in solution and in the LH1 complex of Rhodospirillum rubrum. J. Phys. Chem. B. 2003;107:11216–11223. doi: 10.1021/jp034931j. DOI

Rondonuwu FS, Watanabe Y, Fujii R, Koyama Y. A first detection of singlet to triplet conversion from the 11Bu- to the 13Ag state and triplet internal conversion from the 13Ag to the 13Bu state in carotenoids: dependence on the conjugation length. Chem. Phys. Lett. 2003;376:292–301. doi: 10.1016/S0009-2614(03)00983-7. DOI

Koyama, Y. & Kakitani, Y. Chlorophylls and Bacteriochlorophylls Ch. 30 (Springer, 2006).

Kosumi D, et al. Ultrafast energy-transfer pathway in a purple-bacterial photosynthetic core antenna, as revealed by femtosecond time-resolved spectroscopy. Angew. Chem. Int. Ed. 2011;50:1097–1100. doi: 10.1002/anie.201003771. PubMed DOI

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. 2008;112:9467–9475. doi: 10.1021/jp801773j. PubMed DOI

Akahane J, Rondonuwu FS, Fiedor L, Watanabe Y, Koyama Y. Dependence of singlet-energy transfer on the conjugation length of carotenoids reconstituted into the LH1 complex from Rhodospirillum rubrum G9. Chem. Phys. Lett. 2004;393:184–191. doi: 10.1016/j.cplett.2004.06.021. DOI

Yamamoto M, et al. Reassociation of all-trans-3,4-dihydroanhydrorhodovibrin with LH1 subunits isolated from Rhodospirillum rubrum: Selective binding of all-trans isomer from mixture of cis- and trans-isomers. B. Chem. Soc. JPN. 2013;86:121–128. doi: 10.1246/bcsj.20120230. DOI

Kakitani Y, et al. Selective binding of carotenoids with a shorter conjugated chain to the LH2 antenna complex and those with a longer conjugated chain to the reaction center from Rubrivivax gelatinosus. Biochemistry. 2007;46:7302–7313. doi: 10.1021/bi602485x. PubMed DOI

Hashimoto H, Uragami C, Yukihira N, Gardiner AT, Cogdell RJ. Understanding/unravelling carotenoid excited singlet states. J. R. Soc. Interface. 2018;15:20180026. doi: 10.1098/rsif.2018.0026. PubMed DOI PMC

Polívka T, Sundström V. Ultrafast dynamics of carotenoids excited states—from solution to natural and artificial systems. Chem. Rev. 2004;104:2021–2071. doi: 10.1021/cr020674n. PubMed DOI

Kosumi D, et al. Characterization of the intramolecular transfer state of marine carotenoid fucoxanthin by femtosecond pump–probe spectroscopy. Photosynth. Res. 2014;121:61–68. doi: 10.1007/s11120-014-9995-6. PubMed DOI

Kosumi D, et al. One- and two-photon pump–probe optical spectroscopic measurements reveal the S1 and intramolecular charge transfer states are distinct in fucoxanthin. Chem. Phys. Lett. 2009;483:95–100. doi: 10.1016/j.cplett.2009.10.077. DOI

Cogdell RJ, Frank HA. How carotenoids function in photosynthetic bacteria. Biochim. Biophys. Acta. 1987;895:63–79. doi: 10.1016/S0304-4173(87)80008-3. PubMed DOI

Kosumi D, et al. Excitation energy-transfer dynamics of brown algal photosynthetic antennas. J. Phys. Chem. Lett. 2012;3:2659–2664. doi: 10.1021/jz300612c. PubMed DOI

Wagner NL, Greco JA, Enriquez MM, Frank HA, Birge RR. The nature of the intramolecular charge transfer state in peridinin. Biophys. J. 2013;104:1314–1325. doi: 10.1016/j.bpj.2013.01.045. PubMed DOI PMC

Zigmantas D, Hiller RG, Sundström V, Polívka T. Carotenoid to chlorophyll energy transfer in the peridinin-chlorophyll-a-protein complex involves an intramolecular charge transfer state. Proc. Natl Acad. Sci. USA. 2002;99:16760–16765. doi: 10.1073/pnas.262537599. PubMed DOI PMC

Yukihira N, et al. Strategies to enhance the excitation energy-transfer efficiency in a light-harvesting system using the intra-molecular charge transfer character of carotenoids. Faraday Discuss. 2017;198:59–71. doi: 10.1039/C6FD00211K. PubMed DOI

Nakagawa K, et al. Probing binding site of bacteriochlorophyll a and carotenoid in the reconstituted LH1 complex from Rhodospirillum rubrum S1 by Stark spectroscopy. Photosynth. Res. 2008;95:339–344. doi: 10.1007/s11120-007-9261-2. PubMed DOI

Britton, G. Carotenoids Volume 1B: Spectroscopy Ch. 2 (Birkhauser Verlag, 1995).

Wang X-F, et al. Effects of plant carotenoid spacers on the performance of a dye-sensitized solar cell using a chlorophyll derivative: Enhancement of photocurrent determined by one electron-oxidation potential of each carotenoid. Chem. Phys. Lett. 2006;423:470–475. doi: 10.1016/j.cplett.2006.04.008. DOI

Ragnoni E, Di Donato M, Iagatti A, Lapini A, Righini R. Mechanism of the intramolecular charge transfer state formation in all-trans-β-apo-8’-carotenal: influence of solvent polarity and polarizability. J. Phys. Chem. B. 2015;119:420–432. doi: 10.1021/jp5093288. PubMed DOI

Zhang L. Femtosecond time-resolved difference absorption spectroscopy of all-trans-β-Apo-8’-carotenal. Sci. China Ser. G. 2004;47:208–222. doi: 10.1360/03yw0241. DOI

Durchan M, Fuciman M, Slouf V, Kesan G, Polivka T. Excited-state dynamics of monomeric and aggregated carotenoid 8‘-Apo-b-carotenal. J. Phys. Chem. A. 2012;116:12330–12338. doi: 10.1021/jp310140k. PubMed DOI

Kopczynski M, Ehlers F, Lenzer T, Oum K. Evidence for an intramolecular charge transfer state in 12’-Apo-β-caroten-12’-al and 8’-Apo-β-caroten-8’-al: influence of solvent polarity and temperature. J. Phys. Chem. A. 2007;111:5370–5381. doi: 10.1021/jp0672252. PubMed DOI

van Stokkum IHM, Larsen DS, van Grondelle R. Global and target analysis of time-resolved spectra. Biochim. Biophys. Acta. 2004;1657:82–104. doi: 10.1016/j.bbabio.2004.04.011. PubMed DOI

Snellenburg JJ, Laptenok SP, Seger R, Mullen KM, Stokkum IHMV. Glotaran: a Java-Based graphical user interface for the R package TIMP. J. Stat. Softw. 2012;49:1–22. doi: 10.18637/jss.v049.i03. DOI

Kosumi D, et al. Ultrafast intramolecular relaxation dynamics of Mg- and Zn-bacteriochlorophyll a. J. Chem. Phys. 2013;139:034311. doi: 10.1063/1.4813526. PubMed DOI

Redeckas K, Voiciuk V, Zigmantas D, Hiller RG, Vengris M. Unveiling the excited state energy transfer pathways in peridinin-chlorophyll a-protein by ultrafast multi-pulse transient absorption spectroscopy. Biochim. Biophys. Acta. 2017;1858:297–307. doi: 10.1016/j.bbabio.2017.01.014. PubMed DOI

Uragami C, et al. Photoprotective mechanisms in the core LH1 antenna pigment-protein complex from the purple photosynthetic bacterium, Rhodospirillum rubrum. J. Photochem. Photobiol. A. 2020;400:112628. doi: 10.1016/j.jphotochem.2020.112628. DOI

Niedzwiedzki DM, Swainsbury DJK, Canniffe DP, Hunter CN, Hitchcock A. A photosynthetic antenna complex foregoes unity carotenoid-to-bacteriochlorophyll energy transfer efficiency to ensure photoprotection. Proc. Natl Acad. Sci. USA. 2020;117:6502–6508. doi: 10.1073/pnas.1920923117. PubMed DOI PMC

Tumbarello F, et al. The energy transfer yield between carotenoids and chlorophylls in peridinin chlorophyll a protein is robust against mutations. Int. J. Mol. Sci. 2022;23:35563456. doi: 10.3390/ijms23095067. PubMed DOI PMC

Mendes-Pinto MM, et al. Electronic absorption and ground state structure of carotenoid molecules. J. Phys. Chem. B. 2013;117:11015–11021. doi: 10.1021/jp309908r. PubMed DOI

Marcolin G, Collini E. Solvent-dependent characterization of fucoxanthin through 2D electronic spectroscopy reveals new details on the intramolecular charge-transfer state dynamics. J. Phys. Chem. Lett. 2021;12:4833–4840. doi: 10.1021/acs.jpclett.1c00851. PubMed DOI PMC

Kusumoto T, et al. Stark absorption spectroscopy of peridinin and allene-modified analogues. Chem. Phys. 2010;373:71–79. doi: 10.1016/j.chemphys.2010.01.018. PubMed DOI PMC

Slouf V, et al. Carotenoid charge transfer states and their role in energy transfer processes in LH1-RC complexes from aerobic anoxygenic phototrophs. J. Phys. Chem. B. 2013;117:10987–10999. doi: 10.1021/jp309278y. PubMed DOI

Kosumi D, Horibe T, Sugisaki M, Cogdell RJ, Hashimoto H. Photoprotection mechanism of light-harvesting antenna complex from purple bacteria. J. Phys. Chem. B. 2016;120:951–956. doi: 10.1021/acs.jpcb.6b00121. PubMed DOI

Cohen-Bazire G, Sistrom WR, Stanier RY. Kinetic studies of pigment synthesis by non-sulfur purple bacteria. J. Cell. Physiol. 1957;49:25–68. doi: 10.1002/jcp.1030490104. PubMed DOI

Nakagawa K, et al. Electrostatic effect of surfactant molecules on bacteriochlorophyll a and carotenoid binding sites in the LH1 complex isolated from Rhodospirillum rubrum S1 probed by Stark spectroscopy. Photosynth. Res. 2008;95:345–351. doi: 10.1007/s11120-007-9257-y. PubMed DOI

Kumble R, Palese S, Visschers RW, Leslie Dutton P, Hochstrasser RM. Ultrafast dynamics within the B820 subunit from the core (LH-1) antenna complex of Rs. rubrum. Chem. Phys. Lett. 1996;261:396–404. doi: 10.1016/0009-2614(96)01021-4. DOI

Creemers TMH, De Caro CA, Visschers RW, van Grondelle R, Völker S. Spectral hole burning and fluorescence line narrowing in subunits of the light-harvesting complex LH1 of purple bacteria. J. Phys. Chem. B. 1999;103:9770–9776. doi: 10.1021/jp990805x. DOI

Lambrev PH, et al. Excitation energy trapping and dissipation by Ni-substituted bacteriochlorophyll a in reconstituted LH1 complexes from Rhodospirillum rubrum. J. Phys. Chem. B. 2013;117:11260–11271. doi: 10.1021/jp4020977. PubMed DOI

Fiedor L, Scheer H. Trapping of an assembly intermediate of photosynthetic LH1 antenna beyond B820 subunit: significance for the assembly of photosynthetic LH1 antenna. J. Biol. Chem. 2005;280:20921–20926. doi: 10.1074/jbc.M501212200. PubMed DOI

Fiedor L, Akahane J, Koyama Y. Carotenoid-induced cooperative formation of bacterial photosynthetic LH1 complex. Biochemistry. 2004;43:16487–16496. doi: 10.1021/bi0481287. PubMed DOI

Duan S, et al. Hydroquinone redox mediator enhances the photovoltaic performances of chlorophyll-based bio-inspired solar cells. Commun. Chem. 2021;4:118. doi: 10.1038/s42004-021-00556-5. PubMed DOI PMC