Carotenoid to bacteriochlorophyll energy transfer in the RC–LH1–PufX complex from Rhodobacter sphaeroides containing the extended conjugation keto-carotenoid diketospirilloxanthin
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RC–LH1–PufX complexes from a genetically modified strain of Rhodobacter sphaeroides that accumulates carotenoids with very long conjugation were studied by ultrafast transient absorption spectroscopy. The complexes predominantly bind the carotenoid diketospirilloxanthin, constituting about 75% of the total carotenoids, which has 13 conjugated C=C bonds, and the conjugation is further extended to two terminal keto groups. Excitation of diketospirilloxanthin in the RC–LH1–PufX complex demonstrates fully functional energy transfer from diketospirilloxanthin to BChl a in the LH1 antenna. As for other purple bacterial LH complexes having carotenoids with long conjugation, the main energy transfer route is via the S2–Qx pathway. However, in contrast to LH2 complexes binding diketospirilloxanthin, in RC–LH1–PufX we observe an additional, minor energy transfer pathway associated with the S1 state of diketospirilloxanthin. By comparing the spectral properties of the S1 state of diketospirilloxanthin in solution, in LH2, and in RC–LH1–PufX, we propose that the carotenoid-binding site in RC–LH1–PufX activates the ICT state of diketospirilloxanthin, resulting in the opening of a minor S1/ICT-mediated energy transfer channel.
KeywordsLight-harvesting Carotenoids Ultrafast spectroscopy Purple bacteria Energy transfer Intramolecular charge transfer state
The research in Czech Republic was supported by the grant P501/12/G055 from the Czech Science Foundation. D.J.K.S., E.C.M., and C.N.H. gratefully acknowledge financial support from the Biotechnology and Biological Sciences Research Council (BBSRC UK), award number BB/M000265/1. CNH was also supported by an Advanced Award 338895 from the European Research Council. This work was also supported as part of the Photosynthetic Antenna Research Center (PARC), an Energy Frontier Research Center funded by the U.S. Department of Energy, Office of Science, Office of Basic Energy Sciences under Award Number DE-SC 0001035. The role of PARC role was to provide partial support for CNH.
- Bullough PA, Qian P, Hunter CN (2008) Reaction center-light-harvesting core complexes of purple bacteria. In: Hunter CN, Daldal F, Thurnauer MC, Beatty JT (eds) The Purple Phototrophic Bacteria. Springer, Dordrecht, pp 155–179Google Scholar
- Chi SC, Mothersole DJ, Dilbeck PL, Niedzwiedzki DM, Zhang H, Qian P, Vasilev C, Grayson KJ, Jackson PJ, Martin EC, Li Y, Holten D, Hunter CN (2015) Assembly of functional photosystem complexes in Rhodobacter sphaeroides incorporating carotenoids from the spirilloxanthin pathway. BBA-Bioenergetics 1847:189–201CrossRefPubMedPubMedCentralGoogle Scholar
- Christensen RL, Enriquez MM, Wagner NL, Peacock-Villada AY, Scriban C, Schrock RR, Polívka T, Frank HA, Birge RR (2013) Energetics and dynamics of the low-lying electronic states of constrained polyenes: implications for infinite polyenes. J Phys Chem A 117:1449–1465CrossRefPubMedPubMedCentralGoogle Scholar
- Dilbeck PL, Tang Q, Mothersole DJ, Martin EC, Hunter CN, Bocian DF, Holten D, Niedzwiedzki DM (2016) Quenching capabilities of long-chain carotenoids in light-harvesting-2 complexes from Rhodobacter sphaeroides with an engineered carotenoid synthesis pathway. J Phys Chem B 120:5429–5443. doi: 10.1021/acs.jpcb.6b03305 CrossRefPubMedPubMedCentralGoogle Scholar
- Gerjets T, Steiger, S, Sandmann G (2009) Catalytic properties of the expressed acyclic carotenoid 2-ketolases from Rhodobacter capsulatus and Rubrivivax gelatinosus. BBA-Bioenegetics 1791:125–131.Google Scholar
- Gradinaru CC, Kennis JTM, Papagiannakis E, van Stokkum IHM, Cogdell RJ, Fleming GR, Niederman RA, van Grondelle R (2001) 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 98:2364–2369CrossRefPubMedPubMedCentralGoogle Scholar
- Kosumi D, Fujiwara M, Fujii R, Cogdell RJ, Hashimoto H, Yoshizawa M (2009) 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 130:214506CrossRefPubMedGoogle Scholar
- Niedzwiedzki DM, Dilbeck PL, Tang Q, Mothersole DJ, Martin EC, Li Y, Bocian DF, Holten D, Hunter CN (2015) Functional characteristics of spirilloxanthin and longer-chain keto-bearing analogues in light-harvesting LH2 complexes from Rhodobacter sphaeroides with a genetically modified carotenoid bioynthesis pathway. BBA-Bioenergetics 1847:640–655CrossRefPubMedGoogle Scholar