Abstract
Cyanobacterial photosynthetic systems efficiently capture sunlight using the pigment-protein megacomplexes, phycobilisome (PBS). The energy is subsequently transferred to photosystem I (PSI) and II (PSII), to produce electrochemical potentials. In the present study, we performed picosecond (ps) time-resolved fluorescence and femtosecond (fs) pump-probe spectroscopies on the intact PBS from a thermophilic cyanobacterium, Thermosynechococcus vulcanus, to reveal excitation energy transfer dynamics in PBS. The photophysical properties of the intact PBS were well characterized by spectroscopic measurements covering wide temporal range from femtoseconds to nanoseconds. The ps fluorescence measurements excited at 570 nm, corresponding to the higher energy of the phycocyanin (PC) absorption band, demonstrated the excitation energy transfer from the PC rods to the allophycocyanin (APC) core complex as well as the energy transfer in the APC core complex. Then, the fs pump-probe measurements revealed the detailed energy transfer dynamics in the PC rods taking place in an ultrafast time scale. The results obtained in this study provide the full picture of the funnel-type excitation energy transfer with rate constants of (0.57 ps)−1 → (7.3 ps)−1 → (53 ps)−1 → (180 ps)−1 → (1800 ps)−1.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.Abbreviations
- PBS:
-
Phycobilisome
- PSII:
-
Photosystem II
- PC:
-
Phycocyanin
- APC:
-
Allophycocyanin
- PSI:
-
Photosystem I
- PCB:
-
Phycocyanobilin
- OCP:
-
Orange carotenoid protein
- T. vulcanus :
-
Thermosynechococcus vulcanus
- IRF:
-
Instrument response function
- DAFS:
-
Decay-associated fluorescence spectra
- EAFS:
-
Evolution-associated fluorescence spectra
- DADS:
-
Decay-associated difference spectra
- EADS:
-
Evolution-associated difference spectra
References
Adir N, Bar-Zvi S, Harris D (2020) The amazing phycobilisome. Biochim Biophys Acta 1861:148047. https://doi.org/10.1016/j.bbabio.2019.07.002
Adir N, Dobrovetsky Y, Lerner N (2001) Structure of c-phycocyanin from the thermophilic cyanobacterium Synechococcus vulcanus at 2.5 A: structural implications for thermal stability in phycobilisome assembly. J Mol Biol 313:71–81. https://doi.org/10.1006/jmbi.2001.5030
Akimoto S, Yokono M, Yokono E, Aikawa S, Kondo A (2014) Short-term light adaptation of a cyanobacterium, Synechocystis sp. PCC 6803, probed by time-resolved fluorescence spectroscopy. Plant Physiol Biochem 81:149–154. https://doi.org/10.1016/j.plaphy.2014.01.007
Bar-Zvi S, Lahav A, Harris D, Niedzwiedzki DM, Blankenship RE, Adir N (2018) Structural heterogeneity leads to functional homogeneity in A. marina phycocyanin. Biochim Biophys Acta 1859:544–553. https://doi.org/10.1016/j.bbabio.2018.04.007
Barber J, Morris EP, da Fonseca PC (2003) Interaction of the allophycocyanin core complex with photosystem II. Photochem Photobiol Sci 2:536–541. https://doi.org/10.1039/b300063j
Bishop CL, Ulas S, Baena-Gonzalez E, Aro EM, Purton S, Nugent JH, Maenpaa P (2007) The PsbZ subunit of photosystem II in Synechocystis sp. PCC 6803 modulates electron flow through the photosynthetic electron transfer chain. Photosynth Res 93:139–147. https://doi.org/10.1007/s11120-007-9182-0
Blankenship RE (2014) Molecular mechanisms of photosynthesis. John Wiley & Sons, Missouri
Bryant DA, Canniffe DP (2018) How nature designs light-harvesting antenna systems: design principles and functional realization in chlorophototrophic prokaryotes. J Phys B 51:033001. https://doi.org/10.1088/1361-6455/aa9c3c
Chang L, Liu X, Li Y, Liu CC, Yang F, Zhao J, Sui SF (2015) Structural organization of an intact phycobilisome and its association with photosystem II. Cell Res 25:726–737. https://doi.org/10.1038/cr.2015.59
Collini E, Wong CY, Wilk KE, Curmi PM, Brumer P, Scholes GD (2010) Coherently wired light-harvesting in photosynthetic marine algae at ambient temperature. Nature 463:644–647. https://doi.org/10.1038/nature08811
David L, Marx A, Adir N (2011) High-resolution crystal structures of trimeric and rod phycocyanin. J Mol Biol 405:201–213. https://doi.org/10.1016/j.jmb.2010.10.036
David L, Prado M, Arteni AA, Elmlund DA, Blankenship RE, Adir N (2014) Structural studies show energy transfer within stabilized phycobilisomes independent of the mode of rod-core assembly. Biochim Biophys Acta 1837:385–395. https://doi.org/10.1016/j.bbabio.2013.12.014
Glazer AN, Chan C, Williams RC, Yeh SW, Clark JH (1985) Kinetics of energy flow in the phycobilisome core. Science 230:1051–1053. https://doi.org/10.1126/science.230.4729.1051
Grossman AR, Schaefer MR, Chiang GG, Collier JL (1993) The phycobilisome, a light-harvesting complex responsive to environmental conditions. Microbiol Rev 57:725–749
Gwizdala M, Berera R, Kirilovsky D, van Grondelle R, Krüger TPJ (2016) Controlling light harvesting with light. J Am Chem Soc 138:11616–11622. https://doi.org/10.1021/jacs.6b04811
Gwizdala M, Krüger TPJ, Wahadoszamen M, Gruber JM, van Grondelle R (2018) Phycocyanin: one complex two states, two functions. J Phys Chem Lett 9:1365–1371. https://doi.org/10.1021/acs.jpclett.8b00621
Ho MY, Niedzwiedzki DM, MacGregor-Chatwin C, Gerstenecker G, Hunter CN, Blankenship RE, Bryant DA (2020) Extensive remodeling of the photosynthetic apparatus alters energy transfer among photosynthetic complexes when cyanobacteria acclimate to far-red light. Biochim Biophys Acta 1861:148064. https://doi.org/10.1016/j.bbabio.2019.148064
Hohmann-Marriott MF, Blankenship RE (2011) Evolution of Photosynthesis. Annu Rev Plant Biol 62:515–548. https://doi.org/10.1146/annurev-arplant-042110-103811
Holzwarth AR, Wendler J, Suter GW (1987) Studies on chromophore coupling in isolated phycobiliproteins. Biophys J 51:1–12. https://doi.org/10.1016/s0006-3495(87)83306-4
Jallet D, Gwizdala M, Kirilovsky D (2012) ApcD, ApcF and ApcE are not required for the orange carotenoid protein related phycobilisome fluorescence quenching in the cyanobacterium Synechocystis PCC 6803. Biochim Biophys Acta 1817:1418–1427. https://doi.org/10.1016/j.bbabio.2011.11.020
Karapetyan NV (2007) Non-photochemical quenching of fluorescence in cyanobacteria. Biochemistry 72:1127–1135. https://doi.org/10.1134/s0006297907100100
Kawakami K, Shen JR (2018) Purification of fully active and crystallizable photosystem II from thermophilic cyanobacteria. Methods Enzymol 613:1–16. https://doi.org/10.1016/bs.mie.2018.10.002
Kawakami K, Nagao R, Tahara OY, Hamaguchi T, Suzuki T, Dohmae N, Kosumi D, Shen JR, Miyata M, Yonekura K, Kamiya N (2021) Structural implications for a phycobilisome complex from a thermophilic cyanobacterium Thermosynechococcus vulcanus, submitted
Kojima R, Yamamoto H, Azai C, Uragami C, Hashimoto H, Kosumi D, Oh-oka H (2020) Energy transfer and primary charge separation upon selective femtosecond excitation at 810 nm in the reaction center complex from Heliobacterium modesticaldum. J Photochem Photobiol A Chem 401:112758. https://doi.org/10.1016/j.jphotochem.2020.112758
Kosumi D, Abe K, Karasawa H, Fujiwara M, Cogdell RJ, Hashimoto H, Yoshizawa M (2010) Ultrafast relaxation kinetics of the dark S1 state in all-trans-β-carotene explored by one- and two-photon pump–probe spectroscopy. Chem Phys 373:33–37. https://doi.org/10.1016/j.chemphys.2009.12.013
Kromdijk J, Glowacka K, Leonelli L, Gabilly ST, Iwai M, Niyogi KK, Long SP (2016) Improving photosynthesis and crop productivity by accelerating recovery from photoprotection. Science 354:857–861. https://doi.org/10.1126/science.aai8878
Li Z, Wakao S, Fischer BB, Niyogi KK (2009) Sensing and responding to excess light. Annu Rev Plant Biol 60:239–260. https://doi.org/10.1146/annurev.arplant.58.032806.103844
Liu H, Zhang H, Niedzwiedzki DM, Prado M, He G, Gross ML, Blankenship RE (2013) Phycobilisomes supply excitations to both photosystems in a megacomplex in cyanobacteria. Science 342:1104–1107. https://doi.org/10.1126/science.1242321
Ma J, You X, Sun S, Wang X, Qin S, Sui S-F (2020) Structural basis of energy transfer in Porphyridium purpureum phycobilisome. Nature 579:146–151. https://doi.org/10.1038/s41586-020-2020-7
MacColl R (1998) Cyanobacterial Phycobilisomes. J Struct Biol 124:311–334. https://doi.org/10.1006/jsbi.1998.4062
MacColl R (2004) Allophycocyanin and energy transfer. Biochim Biophys Acta 1657:73–81. https://doi.org/10.1016/j.bbabio.2004.04.005
Marx A, Adir N (2013) Allophycocyanin and phycocyanin crystal structures reveal facets of phycobilisome assembly. Biochim Biophys Acta 1827:311–318. https://doi.org/10.1016/j.bbabio.2012.11.006
Maxson P, Sauer K, Zhou JH, Bryant DA, Glazer AN (1989) Spectroscopic studies of cyanobacterial phycobilisomes lacking core polypeptides. Biochim Biophys Acta 977:40–51. https://doi.org/10.1016/s0005-2728(89)80007-6
Muller P, Li XP, Niyogi KK (2001) Non-photochemical quenching A Response to Excess Light Energy. Plant Physiol 125:1558–1566. https://doi.org/10.1104/pp.125.4.1558
Nganou AC, David L, Adir N, Pouhe D, Deen MJ, Mkandawire M (2015) Evidence of additional excitation energy transfer pathways in the phycobiliprotein antenna system of Acaryochloris marina. Photochem Photobiol Sci 14:429–438. https://doi.org/10.1039/c4pp00352g
Nganou C, David L, Adir N, Mkandawire M (2016) Linker proteins enable ultrafast excitation energy transfer in the phycobilisome antenna system of Thermosynechococcus vulcanus. Photochem Photobiol Sci 15:31–44. https://doi.org/10.1039/c5pp00285k
Niedzwiedzki DM, Bar-Zvi S, Blankenship RE, Adir N (2019) Mapping the excitation energy migration pathways in phycobilisomes from the cyanobacterium Acaryochloris marina. Biochim Biophys Acta 1860:286–296. https://doi.org/10.1016/j.bbabio.2019.01.002
Peng PP et al (2014) The structure of allophycocyanin B from Synechocystis PCC 6803 reveals the structural basis for the extreme redshift of the terminal emitter in phycobilisomes. Biol Crystallogr 70:2558–2569. https://doi.org/10.1107/S1399004714015776
Petrasek Z et al (2005) Excitation energy transfer from phycobiliprotein to chlorophyll d in intact cells of acaryochloris marina studied by time- and wavelength-resolved fluorescence spectroscopy. Photochem Photobiol Sci off J Eur Photochem Assoc Eur Soc Photobiol 4:1016–1022. https://doi.org/10.1039/b512350j
Pieper J, Ratsep M, Golub M, Schmitt FJ, Artene P, Eckert HJ (2017) Excitation energy transfer in phycobiliproteins of the cyanobacterium Acaryochloris marina investigated by spectral hole burning. Photosynth Res 133:225–234. https://doi.org/10.1007/s11120-017-0396-5
Sandström Å, Gillbro T, Sundström V, Fischer R, Scheer H (1988) Picosecond time-resolved energy transfer within C-phycocyanin aggregates of Mastigocladus laminosus. Biochim Biophys Acta 933:42–53. https://doi.org/10.1016/0005-2728(88)90054-0
Shen J-R, Kawakami K, Koike H (2011) Purification and crystallization of oxygen-evolving photosystem ii core complex from thermophilic cyanobacteria. In: Carpentier R (ed) Photosynthesis research protocols. Humana Press, Totowa, NJ, pp 41–51. https://doi.org/10.1007/978-1-60761-925-3_5
Stadnichuk IN, Krasil’nikov PM, Zlenko DV (2015a) Cyanobacterial Phycobilisomes and Phycobiliproteins. Microbiology 84:131–143. https://doi.org/10.1134/S0026261715020150
Stadnichuk VI, Lukashev EP, Yanyushin MF, Zlenko DV, Muronez EM, Stadnichuk IN, Krasilnikov PM (2015b) Energy transfer pathways among phycobilin chromophores and fluorescence emission spectra of the phycobilisome core at 293 and 77 K Doklady. Biochem Biophys 465:401–405. https://doi.org/10.1134/S1607672915060149
Stec B, Troxler RF, Teeter MM (1999) Crystal structure of C-phycocyanin from Cyanidium caldarium provides a new perspective on phycobilisome assembly. Biophys J 76:2912–2921. https://doi.org/10.1016/S0006-3495(99)77446-1
van Stokkum IHM, Gwizdala M, Tian L, Snellenburg JJ, van Grondelle R, van Amerongen H, Berera R (2018) A functional compartmental model of the Synechocystis PCC 6803 phycobilisome. Photosynth Res 135:87–102. https://doi.org/10.1007/s11120-017-0424-5
Tang K et al (2015) The terminal phycobilisome emitter, LCM: A light-harvesting pigment with a phytochrome chromophore. Proc Natl Acad Sci USA 112:15880–15885. https://doi.org/10.1073/pnas.1519177113
Tian L, Gwizdala M, van Stokkum IH, Koehorst RB, Kirilovsky D, van Amerongen H (2012) Picosecond kinetics of light harvesting and photoprotective quenching in wild-type and mutant phycobilisomes isolated from the cyanobacterium Synechocystis PCC 6803. Biophys J 102:1692–1700. https://doi.org/10.1016/j.bpj.2012.03.008
Tian L, van Stokkum IH, Koehorst RB, Jongerius A, Kirilovsky D, van Amerongen H (2011) Site, rate, and mechanism of photoprotective quenching in cyanobacteria. J Am Chem Soc 133:18304–18311. https://doi.org/10.1021/ja206414m
Wahadoszamen M, Kruger TPJ, Ara AM, van Grondelle R, Gwizdala M (2020) Charge transfer states in phycobilisomes. Biochim Biophys Acta Bioenerg 1861:148187. https://doi.org/10.1016/j.bbabio.2020.148187
Wang Q, Moerner WE (2015) Dissecting pigment architecture of individual photosynthetic antenna complexes in solution. Proc Natl Acad Sci U S A 112:13880–13885. https://doi.org/10.1073/pnas.1514027112
Watanabe M, Ikeuchi M (2013) Phycobilisome: architecture of a light-harvesting supercomplex. Photosynth Res 116:265–276. https://doi.org/10.1007/s11120-013-9905-3
Womick JM, Moran AM (2009) Nature of excited states and relaxation mechanisms in C-phycocyanin. J Phys Chem B 113:15771–15782. https://doi.org/10.1021/jp908093x
Wong CY et al (2012) Electronic coherence lineshapes reveal hidden excitonic correlations in photosynthetic light harvesting. Nat Chem 4:396–404. https://doi.org/10.1038/nchem.1302
Yamamoto H, Taomoto M, Ito A, Kosumi D (2020) Electron-transfer behaviors between photoexcited metal complex and methyl viologen codoped in ionic nanospheres. J Photochem Photobiol A Chem 401:112771. https://doi.org/10.1016/j.jphotochem.2020.112771
Yamanaka G, Glazer AN (1980) dynamic aspects of phycobilisome structure—phycobilisome turnover during nitrogen starvation in Synechococcus Sp. Arch Microbiol 124:39–47. https://doi.org/10.1007/Bf00407026
Zhang J, Ma J, Liu D, Qin S, Sun S, Zhao J, Sui SF (2017) Structure of phycobilisome from the red alga Griffithsia pacifica. Nature 551:57–63. https://doi.org/10.1038/nature24278
Zhang JM, Zhao JQ, Jiang LJ, Zheng XG, Zhao FL, Wang HZ (1997) Studies on the energy transfer among the rod-core complex from phycobilisome of Anabaena variabilis by time resolved fluorescence emission and anisotropy spectra. Biochim Biophys Acta 1320:285–296. https://doi.org/10.1016/S0005-2728(97)00032-7
Zilinskas BA, Greenwald LS (1986) Phycobilisome Structure and Function. Photosynth Res 10:7–35. https://doi.org/10.1007/bf00024183
Acknowledgements
This work was supported in part by the Grant-in-Aid for Challenging Exploratory Research (No. 16K13863) and Scientific Research on Innovative Areas “Innovations for Light-Energy Conversion (I4LEC)” (Nos. 17H06434 and 18H05173). DK thanks Iketani Science and Technology Foundation Research Support (No. 0281020-A). This work was also partly suppurated by the Joint Usage/Research of Institute of Pulsed Power Science, Kumamoto University (to KK and DK, 2017–2020).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflicts of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Hirota, Y., Serikawa, H., Kawakami, K. et al. Ultrafast energy transfer dynamics of phycobilisome from Thermosynechococcus vulcanus, as revealed by ps fluorescence and fs pump-probe spectroscopies. Photosynth Res 148, 181–190 (2021). https://doi.org/10.1007/s11120-021-00844-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11120-021-00844-0