Carotenoid responds to excess energy dissipation in the LH2 complex from Rhodoblastus acidophilus

. 2022 Oct ; 154 (1) : 75-87. [epub] 20220906

Jazyk angličtina Země Nizozemsko Médium print-electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid36066816
Odkazy

PubMed 36066816
DOI 10.1007/s11120-022-00952-5
PII: 10.1007/s11120-022-00952-5
Knihovny.cz E-zdroje

The functions of both (bacterio) chlorophylls and carotenoids in light-harvesting complexes have been extensively studied during the past decade, yet, the involvement of BChl a high-energy Soret band in the cascade of light-harvesting processes still remains a relatively unexplored topic. Here, we present transient absorption data recorded after excitation of the Soret band in the LH2 complex from Rhodoblastus acidophilus. Comparison of obtained data to those recorded after excitation of rhodopin glucoside and B800 BChl a suggests that no Soret-to-Car energy transfer pathway is active in LH2 complex. Furthermore, a spectrally rich pattern observed in the spectral region of rhodopin glucoside ground state bleaching (420-550 nm) has been assigned to an electrochromic shift. The results of global fitting analysis demonstrate two more features. A 6 ps component obtained exclusively after excitation of the Soret band has been assigned to the response of rhodopin glucoside to excess energy dissipation in LH2. Another time component, ~ 450 ps, appearing independently of the excitation wavelength was assigned to BChl a-to-Car triplet-triplet transfer. Presented data demonstrate several new features of LH2 complex and its behavior following the excitation of the Soret band.

Zobrazit více v PubMed

Balevičius V, Abramavicius D, Polívka T et al (2016) A unified picture of S∗ in carotenoids. J Phys Chem Lett 7:3347–3352. https://doi.org/10.1021/acs.jpclett.6b01455 PubMed DOI PMC

Balevičius V, Wei T, Di Tommaso D et al (2019) The full dynamics of energy relaxation in large organic molecules: from photo-excitation to solvent heating. Chem Sci 10:4792–4804. https://doi.org/10.1039/c9sc00410f PubMed DOI

Billsten HH, Pan J, Sinha S et al (2005) Excited-state processes in the carotenoid zeaxanthin after excess energy excitation. J Phys Chem A 109:6852–6859. https://doi.org/10.1021/jp052227s PubMed DOI

Blankenship RE (2008) Molecular mechanisms of photosynthesis. Wiley, Hoboken

Bricker WP, Shenai PM, Ghosh A et al (2015) Non-radiative relaxation of photoexcited chlorophylls: theoretical and experimental study. Sci Rep 5:1–16. https://doi.org/10.1038/srep13625 DOI

Cong H, Niedzwiedzki DM, Gibson GN et al (2008) Ultrafast time-resolved carotenoid to-bacteriochlorophyll energy transfer in LH2 complexes from photosynthetic bacteria. J Phys Chem B 112:10689–10703. https://doi.org/10.1021/jp711946w PubMed DOI PMC

Croce R, Van Amerongen H (2014) Natural strategies for photosynthetic light harvesting. Nat Chem Biol 10:492–501. https://doi.org/10.1038/nchembio.1555 PubMed DOI

Croce R, Müller MG, Bassi R, Holzwarth AR (2001) Carotenoid-to-chlorophyll energy transfer in recombinant major light-harvesting complex (LHCII) of higher plants. I. Femtosecond transient absorpt measurements. Biophys J 80:901–915. https://doi.org/10.1016/S0006-3495(01)76069-9 PubMed DOI PMC

Ferrante C, Pontecorvo E, Cerullo G et al (2016) Direct observation of subpicosecond vibrational dynamics in photoexcited myoglobin. Nat Chem 8:1137–1143. https://doi.org/10.1038/nchem.2569 PubMed DOI

Gardiner AT, Naydenova K, Castro-Hartmann P et al (2021) The 2.4 Å cryo-EM structure of a heptameric light-harvesting 2 complex reveals two carotenoid energy transfer pathways. Sci Adv. https://doi.org/10.1126/sciadv.abe4650 PubMed DOI PMC

Gottfried DS, Steffen MA, Boxer SG (1991) Large protein-induced dipoles for a symmetric carotenoid in a photosynthetic antenna complex. Science 251:662–665. https://doi.org/10.1126/science.1992518 PubMed DOI

Gradinaru CC, Kennis JTM, Papagiannakis E et al (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 98:2364–2369. https://doi.org/10.1073/pnas.051501298 PubMed DOI PMC

Hashimoto H, Uragami C, Yukihira N et al (2018) Understanding/unravelling carotenoid excited singlet states. J R Soc Interface. https://doi.org/10.1098/rsif.2018.0026 PubMed DOI PMC

Herek JL, Polívka T, Pullerits T et al (1998) Ultrafast carotenoid band shifts probe structure and dynamics in photosynthetic antenna complexes. Biochemistry 37:7057–7061. https://doi.org/10.1021/bi980118g PubMed DOI

Herek JL, Wendling M, He Z et al (2004) Ultrafast carotenoid band shifts: experiment and theory. J Phys Chem B 108:10398–10403. https://doi.org/10.1021/jp040094p DOI

Jailaubekov AE, Song SH, Vengris M et al (2010) Using narrowband excitation to confirm that the S* state in carotenoids is not a vibrationally-excited ground state species. Chem Phys Lett 487:101–107. https://doi.org/10.1016/j.cplett.2010.01.014 DOI

Kennis JTM, Streltsov AM, Vulto SIE et al (1997) Femtosecond dynamics in isolated LH2 complexes of various species of purple bacteria. J Phys Chem B 101:7827–7834. https://doi.org/10.1021/jp963359b DOI

Khan T, Litvín R, Šebelík V, Polívka T (2021) Excited-state evolution of keto-carotenoids after excess energy excitation in the UV region. Chem Phys Chem 22:471–480. https://doi.org/10.1002/cphc.202000982 PubMed DOI

Kholodenko Y, Volk M, Gooding E, Hochstrasser RM (2000) Energy dissipation and relaxation processes in deoxy myoglobin after photoexcitation in the soret region. Chem Phys 259:71–87. https://doi.org/10.1016/S0301-0104(00)00182-8 DOI

Konold PE, Van Stokkum IHM, Muzzopappa F et al (2019) Photoactivation mechanism, timing of protein secondary structure dynamics and carotenoid translocation in the orange carotenoid protein. J Am Chem Soc 141:520–530. https://doi.org/10.1021/jacs.8b11373 PubMed DOI

Koolhaas MHC, Frese RN, Fowler GJS et al (1998) Identification of the upper exciton component of the b850 bacteriochlorophylls of the LH2 antenna complex, using a B800-free mutant of Rhodobacter sphaeroides. Biochemistry 37:4693–4698. https://doi.org/10.1021/bi973036l DOI

Kosumi D, Maruta S, Fujii R et al (2011a) Ultrafast excited state dynamics of monomeric bacteriochlorophyll a. Phys Status Solidi C 8:92–95. https://doi.org/10.1002/pssc.201000684 DOI

Kosumi D, Maruta S, Horibe T et al (2011b) Ultrafast energy-transfer pathway in a purple-bacterial photosynthetic core antenna, as revealed by femtosecond time-resolved spectroscopy. Angew Chem Int Ed 50:1097–1100. https://doi.org/10.1002/anie.201003771 DOI

Kosumi D, Nakagawa K, Sakai S et al (2013) Ultrafast intramolecular relaxation dynamics of Mg- and Zn-bacteriochlorophyll a. J Chem Phys 139:1–8. https://doi.org/10.1063/1.4813526 DOI

Kosumi D, Horibe T, Sugisaki M et al (2016) Photoprotection mechanism of light-harvesting antenna complex from purple bacteria. J Phys Chem B 120:951–956. https://doi.org/10.1021/acs.jpcb.6b00121 PubMed DOI

Kvíčalová Z, Alster J, Hofmann E et al (2016) Triplet-triplet energy transfer from chlorophylls to carotenoids in two antenna complexes from dinoflagellate Amphidinium carterae. Biochim Biophys Acta 1857:341–349. https://doi.org/10.1016/j.bbabio.2016.01.008 PubMed DOI

Lenzer T, Ehlers F, Scholz M et al (2010) Assignment of carotene S* state features to the vibrationally hot ground electronic state. Phys Chem Chem Phys 12:8832–8839. https://doi.org/10.1039/b925071a PubMed DOI

Levantino M, Schirò G, Lemke HT et al (2015) Ultrafast myoglobin structural dynamics observed with an X-ray free-electron laser. Nat Commun 6:1–6. https://doi.org/10.1038/ncomms7772 DOI

Ma YZ, Cogdell RJ, Gillbro T (1997) Energy transfer and exciton annihilation in the B800–850 antenna complex of the photosynthetic purple bacterium Rhodopseudomonas acidophila (strain 10050). A femtosecond transient absorption study. J Phys Chem B 101:1087–1095. https://doi.org/10.1021/jp962470e DOI

Macpherson AN, Arellano JB, Fraser NJ et al (2001) Efficient energy transfer from the carotenoid S2state in a photosynthetic light-harvesting complex. Biophys J 80:923–930. https://doi.org/10.1016/S0006-3495(01)76071-7 PubMed DOI PMC

Magdaong NM, Lafountain AM, Greco JA et al (2014) High efficiency light harvesting by carotenoids in the LH2 complex from photosynthetic bacteria: Unique adaptation to growth under low-light conditions. J Phys Chem B 118:11172–11189. https://doi.org/10.1021/jp5070984 PubMed DOI PMC

McDermott G, Prince SM, Freer AA et al (1995) Crystal structure of an integral membrane light-harvesting complex from photosynthetic bacteria. Nature 374:517–521 DOI

Mirkovic T, Ostroumov EE, Anna JM et al (2017) Light absorption and energy transfer in the antenna complexes of photosynthetic organisms. Chem Rev 117:249–293. https://doi.org/10.1021/acs.chemrev.6b00002 PubMed DOI

Niedzwiedzki DM, Blankenship RE (2010) Singlet and triplet excited state properties of natural chlorophylls and bacteriochlorophylls. Photosynth Res 106:227–238. https://doi.org/10.1007/s11120-010-9598-9 PubMed DOI

Niedzwiedzki DM, Hunter CN, Blankenship RE (2016) Evaluating the nature of so-called S∗-state feature in transient absorption of carotenoids in light-harvesting complex 2 (LH2) from purple photosynthetic bacteria. J Phys Chem B 120:11123–11131. https://doi.org/10.1021/acs.jpcb.6b08639 PubMed DOI PMC

Papagiannakis E, Kennis JTM, Van Stokkum IHM et al (2002) An alternative carotenoid-to-bacteriochlorophyll energy transfer pathway in photosynthetic light harvesting. Proc Natl Acad Sci USA 99:6017–6022. https://doi.org/10.1073/pnas.092626599 PubMed DOI PMC

Papagiannakis E, Van Stokkum IHM, Vengris M et al (2006) Excited-state dynamics of carotenoids in light-harvesting complexes. 1. Exploring the relationship between the S1 and S* states. J Phys Chem B 110:5727–5736. https://doi.org/10.1021/jp054633h PubMed DOI

Polívka T, Frank HA (2010) Molecular factors controlling photosynthetic light harvesting by carotenoids. Acc Chem Res 43:1125–1134. https://doi.org/10.1021/ar100030m PubMed DOI PMC

Polívka T, Sundström V (2004) Ultrafast dynamics of carotenoid excited states-from solution to natural and artificial systems. Chem Rev 104:2021–2071. https://doi.org/10.1021/cr020674n PubMed DOI

Polívka T, Pullerits T, Frank HA et al (2004) Ultrafast formation of a carotenoid radical in LH2 antenna complexes of purple bacteria. J Phys Chem B 108:15398–15407. https://doi.org/10.1021/jp0483019 DOI

Razjivin AP, Lukashev EP, Kompanets VO et al (2017) Excitation energy transfer from the bacteriochlorophyll soret band to carotenoids in the LH2 light-harvesting complex from Ectothiorhodospira haloalkaliphila is negligible. Photosynth Res 133:289–295. https://doi.org/10.1007/s11120-017-0341-7 PubMed DOI

Razjivin A, Götze J, Lukashev E et al (2021) Lack of excitation energy transfer from the bacteriochlorophyll soret band to carotenoids in photosynthetic complexes of purple bacteria. J Phys Chem B 125:3538–3545. https://doi.org/10.1021/acs.jpcb.1c00719 PubMed DOI

Schödel R, Irrgang KD, Voigt J, Renger G (1998) Rate of carotenoid triplet formation in solubilized light-harvesting complex II (LHCII) from spinach. Biophys J 75:3143–3153. https://doi.org/10.1016/S0006-3495(98)77756-2 PubMed DOI PMC

Shi Y, Liu JY, Han KL (2005) Investigation of the internal conversion time of the chlorophyll a from S3, S2 to S1. Chem Phys Lett 410:260–263. https://doi.org/10.1016/j.cplett.2005.05.017 DOI

Sundström V, Pullerits T, Van Grondelle R (1999) Photosynthetic light-harvesting: reconciling dynamics and structure of purple bacterial LH2 reveals function of photosynthetic unit. J Phys Chem B 103:2327–2346. https://doi.org/10.1021/jp983722+ DOI

Tretiak S, Middleton C, Chernyak V, Mukamel S (2000) Bacteriochlorophyll and carotenoid excitonic couplings in the LH2 system of purple bacteria. J Phys Chem B 104:9540–9553. https://doi.org/10.1021/jp001585m DOI

Visser HM, Somsen OJ, van Mourik F et al (1995) Direct observation of sub-picosecond equilibration of excitation energy in the light-harvesting antenna of Rhodospirillum rubrum. Biophys J 69:1083–1099. https://doi.org/10.1016/S0006-3495(95)79982-9 PubMed DOI PMC

Zang C, Stevens JA, Link JJ et al (2009) Ultrafast proteinquake dynamics in cytochrome c. J Am Chem Soc 131:2846–2852. https://doi.org/10.1021/ja8057293 PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...