1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Physical Chemistry
  4. Volume 74, 2023
  5. Article

Annual Review of Physical Chemistry

Volume 74, 2023

Ultrafast Dynamics of Photosynthetic Light Harvesting: Strategies for Acclimation Across Organisms

Abstract

Photosynthetic light harvesting exhibits near-unity quantum efficiency. The high efficiency is achieved through a series of energy and charge transfer steps within a network of pigment-containing proteins. Remarkably, high efficiency is conserved across many organisms despite differences in the protein structures and organization that allow each organism to respond to its own biological niche and the stressors within. In this review, we highlight recent progress toward understanding how organisms maintain optimal light-harvesting ability by acclimating to their environment. First, we review the building blocks of photosynthetic light harvesting, energy transfer, and time-resolved spectroscopic techniques. Then, we explore how three classes of photosynthetic organisms—purple bacteria, cyanobacteria, and green plants—optimize their light-harvesting apparatuses to their particular environment. Overall, research has shown that photosynthetic energy transfer is robust to changing environmental conditions, with each organism utilizing its own strategies to optimize photon capture in its particular biological niche.

Keyword(s): energy transfer, light harvesting, photosynthesis, ultrafast dynamics
Loading

Article metrics loading...

/content/journals/10.1146/annurev-physchem-083122-111318
2023-04-24
2024-04-27
Loading full text...

Full text loading...

/deliver/fulltext/physchem/74/1/annurev-physchem-083122-111318.html?itemId=/content/journals/10.1146/annurev-physchem-083122-111318&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Blankenship RE. 2014. Molecular Mechanisms of Photosynthesis Wiley-Blackwell. , 2nd ed..
  2. 2.
    Mirkovic T, Ostroumov EE, Anna JM, van Grondelle R, Govindjee, Scholes GD 2017. Light absorption and energy transfer in the antenna complexes of photosynthetic organisms. Chem. Rev. 117:2249–93
     [Google Scholar]
  3. 3.
    Grätzel M. 2001. Molecular photovoltaics that mimic photosynthesis. Pure Appl. Chem. 73:3459–67
     [Google Scholar]
  4. 4.
    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 103:132327–46
     [Google Scholar]
  5. 5.
    Fleming GR, Schlau-Cohen GS, Amarnath K, Zaks J. 2012. Design principles of photosynthetic light-harvesting. Faraday Discuss. 155:27–41
     [Google Scholar]
  6. 6.
    Madigan MT, Jung DO 2009. An overview of purple bacteria: systematics, physiology, and habitats. The Purple Phototrophic Bacteria CN Hunter, F Daldal, MC Thurnauer, JT Beatty 1–15. Dordrecht, Neth: Springer
     [Google Scholar]
  7. 7.
    Grossman AR, Schaefer MR, Chiang GG, Collier JL. 1994. The responses of cyanobacteria to environmental conditions: light and nutrients. The Molecular Biology of Cyanobacteria DA Bryant 641–75. Dordrecht, Neth: Springer
     [Google Scholar]
  8. 8.
    Bassi R, Dall'Osto L 2021. Dissipation of light energy absorbed in excess: the molecular mechanisms. Annu. Rev. Plant Biol. 72:47–76
     [Google Scholar]
  9. 9.
    Senge MO, Ryan AA, Letchford KA, MacGowan SA, Mielke T. 2014. Chlorophylls, symmetry, chirality, and photosynthesis. Symmetry 6:3781–843
     [Google Scholar]
  10. 10.
    Frank H, Cogdell R. 2012. Light capture in photosynthesis. Comprehensive Biophysics EH Egelman 94–114. Amsterdam: Elsevier
     [Google Scholar]
  11. 11.
    Gouterman M, Wagnière GH, Snyder LC. 1963. Spectra of porphyrins: Part II. Four orbital model. J. Mol. Spectrosc. 11:1–6108–27
     [Google Scholar]
  12. 12.
    Sirohiwal A, Berraud-Pache R, Neese F, Izsák R, Pantazis DA. 2020. Accurate computation of the absorption spectrum of chlorophyll a with pair natural orbital coupled cluster methods. J. Phys. Chem. B 124:408761–71
     [Google Scholar]
  13. 13.
    Natl. Renew. Energy Lab. (NREL) 2022. Reference air mass 1.5 spectra. NREL https://www.nrel.gov/grid/solar-resource/spectra-am1.5.html
    [Google Scholar]
  14. 14.
    Frank HA, Cogdell RJ. 1993. The photochemistry and function of carotenoids in photosynthesis. Carotenoids in Photosynthesis AJ Young, G Britton 252–326. Dordrecht, Neth: Springer
     [Google Scholar]
  15. 15.
    Moskalenko AA, Karapetyan NV. 1996. Structural role of carotenoids in photosynthetic membranes. Z. Naturforsch. C 51:11–12763–71
     [Google Scholar]
  16. 16.
    Polívka T, Sundström V. 2004. Ultrafast dynamics of carotenoid excited states–from solution to natural and artificial systems. Chem. Rev. 104:42021–71
     [Google Scholar]
  17. 17.
    Son M, Hart SM, Schlau-Cohen GS. 2021. Investigating carotenoid photophysics in photosynthesis with 2D electronic spectroscopy. Trends Chem. 3:9733–46
     [Google Scholar]
  18. 18.
    Polívka T, Sundström V. 2009. Dark excited states of carotenoids: consensus and controversy. Chem. Phys. Lett. 477:1–31–11
     [Google Scholar]
  19. 19.
    Gradinaru CC, Kennis JTM, Papagiannakis E, van Stokkum IHM, Cogdell RJ et al. 2001. An unusual pathway of excitation energy deactivation in carotenoids: singlet-to-triplet conversion on an ultrafast timescale in a photosynthetic antenna. PNAS 98:52364–69
     [Google Scholar]
  20. 20.
    Son M, Pinnola A, Bassi R, Schlau-Cohen GS. 2019. The electronic structure of lutein 2 is optimized for light harvesting in plants. Chem 5:3575–84
     [Google Scholar]
  21. 21.
    Mohan TMN, Leslie CH, Sil S, Rose JB, Tilluck RW, Beck WF. 2021. Broadband 2DES detection of vibrational coherence in the Sx state of canthaxanthin. J. Chem. Phys. 155:3035103
     [Google Scholar]
  22. 22.
    Chábera P, Fuciman M, Hříbek P, Polívka T. 2009. Effect of carotenoid structure on excited-state dynamics of carbonyl carotenoids. Phys. Chem. Chem. Phys. 11:398795–803
     [Google Scholar]
  23. 23.
    Beale SI. 1993. Biosynthesis of phycobilins. Chem. Rev. 93:2785–802
     [Google Scholar]
  24. 24.
    Croce R, van Amerongen H. 2014. Natural strategies for photosynthetic light harvesting. Nat. Chem. Biol. 10:7492–501
     [Google Scholar]
  25. 25.
    Cogdell RJ, Gall A, Köhler J. 2006. The architecture and function of the light-harvesting apparatus of purple bacteria: from single molecules to in vivo membranes. Q. Rev. Biophys. 39:3227–324
     [Google Scholar]
  26. 26.
    Milne BF, Kjær C, Houmøller J, Stockett MH, Toker Y et al. 2016. On the exciton coupling between two chlorophyll pigments in the absence of a protein environment: intrinsic effects revealed by theory and experiment. Angew. Chem. 128:216356–59
     [Google Scholar]
  27. 27.
    Brody SS, Rabinowitch E. 1957. Excitation lifetime of photosynthetic pigments in vitro and in vivo. Science 125:3247555
     [Google Scholar]
  28. 28.
    Niyogi KK. 1999. Photoprotection revisited: genetic and molecular approaches. Annu. Rev. Plant Physiol. 50:333–59
     [Google Scholar]
  29. 29.
    Ma YZ, Holt NE, Li XP, Niyogi KK, Fleming GR. 2003. Evidence for direct carotenoid involvement in the regulation of photosynthetic light harvesting. PNAS 100:84377–82
     [Google Scholar]
  30. 30.
    Ruban AV, Berera R, Ilioaia C, van Stokkum IHM, Kennis JTM et al. 2007. Identification of a mechanism of photoprotective energy dissipation in higher plants. Nature 450:7169575–78
     [Google Scholar]
  31. 31.
    Son M, Pinnola A, Gordon SC, Bassi R, Schlau-Cohen GS. 2020. Observation of dissipative chlorophyll-to-carotenoid energy transfer in light-harvesting complex II in membrane nanodiscs. Nat. Commun. 11:11295
     [Google Scholar]
  32. 32.
    Fraser NJ, Hashimoto H, Cogdell RJ. 2001. Carotenoids and bacterial photosynthesis: the story so far.…. Photosynth. Res. 70:3249–56
     [Google Scholar]
  33. 33.
    Chenu A, Scholes GD. 2015. Coherence in energy transfer and photosynthesis. Annu. Rev. Phys. Chem. 66:69–96
     [Google Scholar]
  34. 34.
    von Förster T. 1964. Delocalized excitation and excitation transfer Bull. 18, Div. Biol. Med., US Atomic Energy Comm. Washington, DC:
  35. 35.
    Scholes GD. 2003. Long-range resonance energy transfer in molecular systems. Annu. Rev. Phys. Chem. 54:57–87
     [Google Scholar]
  36. 36.
    Zaks J, Amarnath K, Sylak-Glassman EJ, Fleming GR 2013. Models and measurements of energy-dependent quenching. Photosynth. Res. 116:2389–409
     [Google Scholar]
  37. 37.
    Hess S, Feldchtein F, Babin A, Nurgaleev I, Pullerits T et al. 1993. Femtosecond energy transfer within the LH2 peripheral antenna of the photosynthetic purple bacteria Rhodobacter sphaeroides and Rhodopseudomonas palustris LL. Chem. Phys. Lett. 216:3–6247–57
     [Google Scholar]
  38. 38.
    Berera R, van Grondelle R, Kennis JTM. 2009. Ultrafast transient absorption spectroscopy: principles and application to photosynthetic systems. Photosynth. Res. 101:2–3105–18
     [Google Scholar]
  39. 39.
    van Stokkum IHM, Larsen DS, van Grondelle R. 2004. Global and target analysis of time-resolved spectra. Biochim. Biophys. Acta Bioenerg. 1657:282–104
     [Google Scholar]
  40. 40.
    Polívka T, Herek JL, Zigmantas D, Åkerlund HE, Sundström V. 1999. Direct observation of the (forbidden) S1 state in carotenoids. PNAS 96:94914–17
     [Google Scholar]
  41. 41.
    Park S, Fischer AL, Li Z, Bassi R, Niyogi KK, Fleming GR. 2017. Snapshot transient absorption spectroscopy of carotenoid radical cations in high-light-acclimating thylakoid membranes. J. Phys. Chem. Lett. 8:225548–54
     [Google Scholar]
  42. 42.
    Dall'Osto L, Cazzaniga S, Bressan M, Paleček D, Židek K et al. 2017. Two mechanisms for dissipation of excess light in monomeric and trimeric light-harvesting complexes. Nat. Plants 3:517033
     [Google Scholar]
  43. 43.
    Schlau-Cohen GS, Dawlaty JM, Fleming GR. 2012. Ultrafast multidimensional spectroscopy: principles and applications to photosynthetic systems. IEEE J. Sel. Topics Quantum Electron. 18:1283–95
     [Google Scholar]
  44. 44.
    Son M, Mosquera-Vázquez S, Schlau-Cohen GS. 2017. Ultrabroadband 2D electronic spectroscopy with high-speed, shot-to-shot detection. Opt. Express 25:1618950–62
     [Google Scholar]
  45. 45.
    Ma X, Dostál J, Brixner T. 2016. Broadband 7-fs diffractive-optic-based 2D electronic spectroscopy using hollow-core fiber compression. Opt. Express 24:1820781–91
     [Google Scholar]
  46. 46.
    Scheuring S, Sturgis JN. 2005. Chromatic adaptation of photosynthetic membranes. Science 309:5733484–87
     [Google Scholar]
  47. 47.
    Brixner T, Hildner R, Köhler J, Lambert C, Würthner F. 2017. Exciton transport in molecular aggregates – from natural antennas to synthetic chromophore systems. Adv. Energy Mater. 7:161700236
     [Google Scholar]
  48. 48.
    Tong AL, Fiebig OC, Nairat M, Harris D, Giansily M et al. 2020. Comparison of the energy-transfer rates in structural and spectral variants of the B800–850 complex from purple bacteria. J. Phys. Chem. B 124:81460–69
     [Google Scholar]
  49. 49.
    Cogdell RJ, Howard TD, Bittl R, Schlodder E, Geisenheimer I et al. 2000. How carotenoids protect bacterial photosynthesis. Philos. Trans. R. Soc. B 355:14021345–49
     [Google Scholar]
  50. 50.
    Ogren JI, Tong AL, Gordon SC, Chenu A, Lu Y et al. 2018. Impact of the lipid bilayer on energy transfer kinetics in the photosynthetic protein LH2. Chem. Sci. 9:123095–104
     [Google Scholar]
  51. 51.
    Thyrhaug E, Schröter M, Bukartė E, Kühn O, Cogdell R et al. 2021. Intraband dynamics and exciton trapping in the LH2 complex of Rhodopseudomonas acidophila. J. Chem. Phys. 154:445102
     [Google Scholar]
  52. 52.
    Jimenez R, Dikshit SN, Bradforth SE, Fleming GR. 1996. Electronic excitation transfer in the LH2 complex of Rhodobacter sphaeroides. J. Phys. Chem. 100:166825–34
     [Google Scholar]
  53. 53.
    Schlau-Cohen GS, Wang Q, Southall J, Cogdell RJ, Moerner WE. 2013. Single-molecule spectroscopy reveals photosynthetic LH2 complexes switch between emissive states. PNAS 110:2710899–903
     [Google Scholar]
  54. 54.
    Mascle-Allemand C, Duquesne K, Lebrun R, Scheuring S, Sturgis JN. 2010. Antenna mixing in photosynthetic membranes from Phaeospirillum molischianum. PNAS 107:125357–62
     [Google Scholar]
  55. 55.
    Hartigan N, Tharia HA, Sweeney F, Lawless AM, Papiz MZ. 2002. The 7.5-Å electron density and spectroscopic properties of a novel low-light B800 LH2 from Rhodopseudomonas palustris. Biophys. J. 82:2963–77
     [Google Scholar]
  56. 56.
    Evans K, Fordham-Skelton AP, Mistry H, Reynolds CD, Lawless AM, Papiz MZ. 2005. A bacteriophytochrome regulates the synthesis of LH4 complexes in Rhodopseudomonas palustris. Photosynth. Res. 85:2169–80
     [Google Scholar]
  57. 57.
    McLuskey K, Prince SM, Cogdell RJ, Isaacs NW. 2001. The crystallographic structure of the B800-820 LH3 light-harvesting complex from the purple bacteria Rhodopseudomonas acidophila strain 7050. Biochemistry 40:308783–89
     [Google Scholar]
  58. 58.
    Montemayor D, Rivera E, Jang SJ. 2018. Computational modeling of exciton-bath Hamiltonians for light harvesting 2 and light harvesting 3 complexes of purple photosynthetic bacteria at room temperature. J. Phys. Chem. B 122:143815–25
     [Google Scholar]
  59. 59.
    Zigmantas D, Read EL, Mančal T, Brixner T, Gardiner AT et al. 2006. Two-dimensional electronic spectroscopy of the B800–B820 light-harvesting complex. PNAS 103:3412672–77
     [Google Scholar]
  60. 60.
    Koolhaas MHC, Frese RN, Fowler GJS, Bibby TS, Georgakopoulou S 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 37:144693–98
     [Google Scholar]
  61. 61.
    Scheuring S, Gonçalves RP, Prima V, Sturgis JN. 2006. The photosynthetic apparatus of Rhodopseudomonas palustris: structures and organization. J. Mol. Biol. 358:183–96
     [Google Scholar]
  62. 62.
    Fixen KR, Oda Y, Harwood CS, Newman DK. 2019. Redox regulation of a light-harvesting antenna complex in an anoxygenic phototroph. mBio 10:602838–19
     [Google Scholar]
  63. 63.
    Southall J, Henry SL, Gardiner AT, Roszak AW, Mullen W et al. 2018. Characterisation of a pucBA deletion mutant from Rhodopseudomonas palustris lacking all but the pucBAd genes. Photosynth. Res. 135:1–39–21
     [Google Scholar]
  64. 64.
    Read EL, Schlau-Cohen GS, Engel GS, Georgiou T, Papiz MZ, Fleming GR. 2009. Pigment organization and energy level structure in light-harvesting complex 4: insights from two-dimensional electronic spectroscopy. J. Phys. Chem. B 113:186495–504
     [Google Scholar]
  65. 65.
    Moulisová V, Luer L, Hoseinkhani S, Brotosudarmo THP, Collins AM et al. 2009. Low light adaptation: energy transfer processes in different types of light harvesting complexes from Rhodopseudomonas palustris. Biophys. J. 97:113019–28
     [Google Scholar]
  66. 66.
    Ilioaia C, Krüger TPJ, Ilioaia O, Robert B, van Grondelle R, Gall A. 2018. Apoprotein heterogeneity increases spectral disorder and a step-wise modification of the B850 fluorescence peak position. Biochim. Biophys. Acta Bioenerg. 1859:2137–44
     [Google Scholar]
  67. 67.
    Sturgis JN, Tucker JD, Olsen JD, Hunter CN, Niederman RA. 2009. Atomic force microscopy studies of native photosynthetic membranes. Biochemistry 48:173679–98
     [Google Scholar]
  68. 68.
    Adams PG, Hunter CN. 2012. Adaptation of intracytoplasmic membranes to altered light intensity in Rhodobacter sphaeroides. Biochim. Biophys. Acta Bioenerg. 1817:91616–27
     [Google Scholar]
  69. 69.
    Kotecha A, Georgiou T, Papiz MZ. 2013. Evolution of low-light adapted peripheral light-harvesting complexes in strains of Rhodopseudomonas palustris. Photosynth. Res. 114:3155–64
     [Google Scholar]
  70. 70.
    Agarwal R, Rizvi AH, Prall BS, Olsen JD, Hunter CN, Fleming GR. 2002. Nature of disorder and inter-complex energy transfer in LH2 at room temperature: a three pulse photon echo peak shift study. J. Phys. Chem. A 106:337573–78
     [Google Scholar]
  71. 71.
    Dahlberg PD, Ting PC, Massey SC, Allodi MA, Martin EC et al. 2017. Mapping the ultrafast flow of harvested solar energy in living photosynthetic cells. Nat. Commun. 8:1988
     [Google Scholar]
  72. 72.
    Niedzwiedzki DM, Gardiner AT, Blankenship RE, Cogdell RJ. 2018. Energy transfer in purple bacterial photosynthetic units from cells grown in various light intensities. Photosynth. Res. 137:3389–402
     [Google Scholar]
  73. 73.
    Nagatsuma S, Gotou K, Yamashita T, Yu LJ, Shen JR et al. 2019. Phospholipid distributions in purple phototrophic bacteria and LH1-RC core complexes. Biochim. Biophys. Acta Bioenerg. 1860:6461–68
     [Google Scholar]
  74. 74.
    Tsuzuki M, Moskvin OV, Kuribayashi M, Sato K, Retamal S et al. 2011. Salt stress-induced changes in the transcriptome, compatible solutes, and membrane lipids in the facultatively phototrophic bacterium Rhodobacter sphaeroides. Appl. Environ. Microbiol. 77:217551–59
     [Google Scholar]
  75. 75.
    Jones MR, Fyfe PK, Roszak AW, Isaacs NW, Cogdell RJ. 2002. Protein–lipid interactions in the purple bacterial reaction centre. Biochim. Biophys. Acta Biomembr. 1565:2206–14
     [Google Scholar]
  76. 76.
    Sumino A, Dewa T, Noji T, Nakano Y, Watanabe N et al. 2013. Influence of phospholipid composition on self-assembly and energy-transfer efficiency in networks of light-harvesting 2 complexes. J. Phys. Chem. B 117:3610395–404
     [Google Scholar]
  77. 77.
    Dewa T, Sumino A, Watanabe N, Noji T, Nango M. 2013. Energy transfer and clustering of photosynthetic light-harvesting complexes in reconstituted lipid membranes. Chem. Phys. 419:200–4
     [Google Scholar]
  78. 78.
    Swainsbury DJ, Scheidelaar S, Van Grondelle R, Killian JA, Jones MR. 2014. Bacterial reaction centers purified with styrene maleic acid copolymer retain native membrane functional properties and display enhanced stability. Angew. Chem. Int. Ed. Engl. 126:4411997–2001
     [Google Scholar]
  79. 79.
    Lu Y, Zhang H, Niedzwiedzki DM, Jiang J, Blankenship RE, Gross ML. 2016. Fast photochemical oxidation of proteins maps the topology of intrinsic membrane proteins: light-harvesting complex 2 in a nanodisc. Anal. Chem. 88:178827–34
     [Google Scholar]
  80. 80.
    Castenholz RW, Wilmotte A, Herdman M, Rippka R, Waterbury JB et al. 2001. Phylum BX. Cyanobacteria. Bergey's Manual of Systematic Bacteriology, Vol. 1: The Archaea and the Deeply Branching and Phototrophic Bacteria DR Boone, RW Castenholz, GM Garrity 473–599. New York: Springer Science+Business Media
     [Google Scholar]
  81. 81.
    Harris D, Bar-Zvi S, Lahav A, Goldshmid I, Adir N 2018. The structural basis for the extraordinary energy-transfer capabilities of the phycobilisome. Membrane Protein Complexes: Structure and Function JR Harris, EJ Boekema 57–82. Singapore: Springer
     [Google Scholar]
  82. 82.
    Komenda J, Sobotka R. 2016. Cyanobacterial high-light-inducible proteins—protectors of chlorophyll–protein synthesis and assembly. Biochim. Biophys. Acta Bioenerg. 1857:3288–95
     [Google Scholar]
  83. 83.
    Staleva H, Komenda J, Shukla MK, Šlouf V, Kaňa R et al. 2015. Mechanism of photoprotection in the cyanobacterial ancestor of plant antenna proteins. Nat. Chem. Biol. 11:4287–91
     [Google Scholar]
  84. 84.
    Chen HY, Bandyopadhyay A, Pakrasi HB. 2018. Function, regulation and distribution of IsiA, a membrane-bound chlorophyll a-antenna protein in cyanobacteria. Photosynthetica 56:322–33
     [Google Scholar]
  85. 85.
    Engelken J, Brinkmann H, Adamska I. 2010. Taxonomic distribution and origins of the extended LHC (light-harvesting complex) antenna protein superfamily. BMC Evol. Biol. 10:1233
     [Google Scholar]
  86. 86.
    Sui SF. 2021. Structure of phycobilisomes. Annu. Rev. Biophys. 50:53–72
     [Google Scholar]
  87. 87.
    Adir N, Bar-Zvi S, Harris D 2020. The amazing phycobilisome. Biochim. Biophys. Acta Bioenerg. 1861:4148047
     [Google Scholar]
  88. 88.
    Gan F, Zhang S, Rockwell NC, Martin SS, Lagarias JC, Bryant DA. 2014. Extensive remodeling of a cyanobacterial photosynthetic apparatus in far-red light. Science 345:62021312–17
     [Google Scholar]
  89. 89.
    Chen M, Blankenship RE. 2011. Expanding the solar spectrum used by photosynthesis. Trends Plant Sci. 16:8427–31
     [Google Scholar]
  90. 90.
    Ho MY, Gan F, Shen G, Bryant DA. 2017. Far-red light photoacclimation (FaRLiP) in Synechococcus sp. PCC 7335. II. Characterization of phycobiliproteins produced during acclimation to far-red light. Photosynth. Res. 131:2187–202
     [Google Scholar]
  91. 91.
    Li Y, Lin Y, Garvey CJ, Birch D, Corkery RW et al. 2016. Characterization of red-shifted phycobilisomes isolated from the chlorophyll f-containing cyanobacterium Halomicronema hongdechloris. Biochim. Biophys. Acta Bioenerg. 1857:1107–14
     [Google Scholar]
  92. 92.
    Moya R, Norris AC, Kondo T, Schlau-Cohen GS. 2022. Observation of robust energy transfer in the photosynthetic protein allophycocyanin using single-molecule pump–probe spectroscopy. Nat. Chem. 14:2153–59
     [Google Scholar]
  93. 93.
    Womick JM, Moran AM. 2009. Exciton coherence and energy transport in the light-harvesting dimers of allophycocyanin. J. Phys. Chem. B 113:4815747–59
     [Google Scholar]
  94. 94.
    Womick JM, Miller SA, Moran AM. 2010. Toward the origin of exciton electronic structure in phycobiliproteins. J. Chem. Phys. 133:2024507
     [Google Scholar]
  95. 95.
    Womick JM, Moran AM. 2011. Vibronic enhancement of exciton sizes and energy transport in photosynthetic complexes. J. Phys. Chem. B 115:61347–56
     [Google Scholar]
  96. 96.
    Acuña AM, Lemaire C, van Grondelle R, Robert B, van Stokkum IHM 2018. Energy transfer and trapping in Synechococcus WH 7803. Photosynth. Res. 135:1115–24
     [Google Scholar]
  97. 97.
    Fălămaş A, Porav SA, Tosa V. 2020. Investigations of the energy transfer in the phycobilisome antenna of Arthrospira Platensis using femtosecond spectroscopy. Appl. Sci. 10:114045
     [Google Scholar]
  98. 98.
    Mascoli V, Bhatti AF, Bersanini L, van Amerongen H, Croce R. 2022. The antenna of far-red absorbing cyanobacteria increases both absorption and quantum efficiency of photosystem II. Nat. Commun. 13:13562
     [Google Scholar]
  99. 99.
    Lou W, Niedzwiedzki DM, Jiang RJ, Blankenship RE, Liu H. 2020. Binding of red form of orange carotenoid protein (OCP) to phycobilisome is not sufficient for quenching. Biochim. Biophys. Acta Bioenerg. 1861:3148155
     [Google Scholar]
  100. 100.
    Kirilovsky D, Kerfeld CA. 2012. The orange carotenoid protein in photoprotection of photosystem II in cyanobacteria. Biochim. Biophys. Acta Bioenerg. 1817:1158–66
     [Google Scholar]
  101. 101.
    Kirilovsky D, Kerfeld CA. 2016. Cyanobacterial photoprotection by the orange carotenoid protein. Nat. Plants 2:1216180
     [Google Scholar]
  102. 102.
    Harris D, Tal O, Jallet D, Wilson A, Kirilovsky D, Adir N. 2016. Orange carotenoid protein burrows into the phycobilisome to provide photoprotection. PNAS 113:12E1655–62
     [Google Scholar]
  103. 103.
    Tian L, Gwizdala M, van Stokkum I, Koehorst R, 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. 102:71692–700
     [Google Scholar]
  104. 104.
    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 Bioenerg. 1817:81418–27
     [Google Scholar]
  105. 105.
    Dominguez-Martin MA, Sauer PV, Sutter M, Kirst H, Bina D et al. 2021. Structure of the quenched cyanobacterial OCP-phycobilisome complex. bioRxiv 2021.11.15.468719. https://doi.org/10.1101/2021.11.15.468719
  106. 106.
    Bibby TS, Nield J, Barber J. 2001. Iron deficiency induces the formation of an antenna ring around trimeric photosystem I in cyanobacteria. Nature 412:6848743–45
     [Google Scholar]
  107. 107.
    Toporik H, Li J, Williams D, Chiu PL, Mazor Y. 2019. The structure of the stress-induced photosystem I–IsiA antenna supercomplex. Nat. Struct. Mol. Biol. 26:6443–49
     [Google Scholar]
  108. 108.
    Andrizhiyevskaya EG, Frolov D, Van Grondelle R, Dekker JP. 2004. Energy transfer and trapping in the Photosystem I complex of Synechococcus PCC 7942 and in its supercomplex with IsiA. Biochim. Biophys. Acta Bioenerg. 1656:2–3104–13
     [Google Scholar]
  109. 109.
    Melkozernov AN, Bibby TS, Lin S, Barber J, Blankenship RE. 2003. Time-resolved absorption and emission show that the CP43′ antenna ring of iron-stressed Synechocystis sp. PCC6803 is efficiently coupled to the photosystem I reaction center core.. Biochemistry 42:133893–903
     [Google Scholar]
  110. 110.
    Berera R, Van Stokkum IHM, d'Haene S, Kennis JTM, Van Grondelle R, Dekker JP. 2009. A mechanism of energy dissipation in cyanobacteria. Biophys. J. 96:62261–67
     [Google Scholar]
  111. 111.
    Berera R, van Stokkum IHM, Kennis JTM, van Grondelle R, Dekker JP. 2010. The light-harvesting function of carotenoids in the cyanobacterial stress-inducible IsiA complex. Chem. Phys. 373:1–265–70
     [Google Scholar]
  112. 112.
    Chen HYS, Liberton M, Pakrasi HB, Niedzwiedzki DM. 2017. Reevaluating the mechanism of excitation energy regulation in iron-starved cyanobacteria. Biochim. Biophys. Acta Bioenerg. 1858:3249–58
     [Google Scholar]
  113. 113.
    Chen H-YS, Niedzwiedzki DM, Bandyopadhyay A, Biswas S, Pakrasi HB. 2021. A novel mode of photoprotection mediated by a cysteine residue in the chlorophyll protein IsiA. mBio 12:1e03663–20
     [Google Scholar]
  114. 114.
    Orf GS, Saer RG, Niedzwiedzki DM, Zhang H, McIntosh CL et al. 2016. Evidence for a cysteine-mediated mechanism of excitation energy regulation in a photosynthetic antenna complex. PNAS 113:31E4486–93
     [Google Scholar]
  115. 115.
    He Q, Dolganov N, Björkman O, Grossman AR. 2001. The high light-inducible polypeptides in Synechocystis PCC6803: expression and function in high light. J. Biol. Chem. 276:1306–14
     [Google Scholar]
  116. 116.
    Yao D, Kieselbach T, Komenda J, Promnares K, Prieto MAH et al. 2007. Localization of the small cab-like proteins in photosystem II. J. Biol. Chem. 282:1267–76
     [Google Scholar]
  117. 117.
    Niedzwiedzki DM, Tronina T, Liu H, Staleva H, Komenda J et al. 2016. Carotenoid-induced non-photochemical quenching in the cyanobacterial chlorophyll synthase-HliC/D complex. Biochim. Biophys. Acta Bioenerg. 1857:91430–39
     [Google Scholar]
  118. 118.
    Liu Z, Yan H, Wang K, Kuang T, Zhang J et al. 2004. Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution. Nature 428:6980287–92
     [Google Scholar]
  119. 119.
    Guarnetti Prandi I, Sláma V, Pecorilla C, Cupellini L, Mennucci B 2022. Structure of the stress-related LHCSR1 complex determined by an integrated computational strategy. Commun. Biol. 5:1145
     [Google Scholar]
  120. 120.
    Dall'Osto L, Cazzaniga S, Zappone D, Bassi R. 2020. Monomeric light harvesting complexes enhance excitation energy transfer from LHCII to PSII and control their lateral spacing in thylakoids. Biochim. Biophys. Acta Bioenerg. 1861:4148035
     [Google Scholar]
  121. 121.
    Su X, Ma J, Pan X, Zhao X, Chang W et al. 2019. Antenna arrangement and energy transfer pathways of a green algal photosystem-I–LHCI supercomplex. Nat. Plants 5:3273–81
     [Google Scholar]
  122. 122.
    Croce R, van Amerongen H. 2020. Light harvesting in oxygenic photosynthesis: structural biology meets spectroscopy. Science 369:6506eaay2058
     [Google Scholar]
  123. 123.
    Le Quiniou C, Tian L, Drop B, Wientjes E, van Stokkum IHM et al. 2015. PSI–LHCI of Chlamydomonas reinhardtii: increasing the absorption cross section without losing efficiency. Biochim. Biophys. Acta Bioenerg. 1847:4458–67
     [Google Scholar]
  124. 124.
    Gobets B, van Grondelle R. 2001. Energy transfer and trapping in photosystem I. Biochim. Biophys. Acta Bioenerg. 1507:180–99
     [Google Scholar]
  125. 125.
    Caffarri S, Broess K, Croce R, van Amerongen H. 2011. Excitation energy transfer and trapping in higher plant photosystem II complexes with different antenna sizes. Biophys. J. 100:92094–103
     [Google Scholar]
  126. 126.
    Bennett DIG, Amarnath K, Fleming GR. 2013. A structure-based model of energy transfer reveals the principles of light harvesting in photosystem II supercomplexes. J. Am. Chem. Soc. 135:249164–73
     [Google Scholar]
  127. 127.
    Wientjes E, Roest G, Croce R. 2012. From red to blue to far-red in Lhca4: How does the protein modulate the spectral properties of the pigments?. Biochim. Biophys. Acta Bioenerg. 1817:5711–17
     [Google Scholar]
  128. 128.
    Son M, Pinnola A, Schlau-Cohen GS. 2020. Zeaxanthin independence of photophysics in light-harvesting complex II in a membrane environment. Biochim. Biophys. Acta Bioenerg. 1861:5148115
     [Google Scholar]
  129. 129.
    Son M, Moya R, Pinnola A, Bassi R, Schlau-Cohen GS. 2021. Protein–protein interactions induce pH-dependent and zeaxanthin-independent photoprotection in the plant light-harvesting complex, LHCII. J. Am. Chem. Soc. 143:4217577–86
     [Google Scholar]
  130. 130.
    Schlau-Cohen GS, Calhoun TR, Ginsberg NS, Read EL, Ballottari M et al. 2009. Pathways of energy flow in LHCII from two-dimensional electronic spectroscopy. J. Phys. Chem. B 113:4615352–63
     [Google Scholar]
  131. 131.
    Wells KL, Lambrev PH, Zhang Z, Garab G, Tan HS. 2014. Pathways of energy transfer in LHCII revealed by room-temperature 2D electronic spectroscopy. Phys. Chem. Chem. Phys. 16:2311640–46
     [Google Scholar]
  132. 132.
    Son M, Schlau-Cohen GS. 2019. Flipping a protein switch: carotenoid-mediated quenching in plants. Chem 5:112749–50
     [Google Scholar]
  133. 133.
    Artes Vivancos JM, van Stokkum IHM, Saccon F, Hontani Y, Kloz M et al. 2020. Unraveling the excited-state dynamics and light-harvesting functions of xanthophylls in light-harvesting complex II using femtosecond stimulated Raman spectroscopy. J. Am. Chem. Soc. 142:4117346–55
     [Google Scholar]
  134. 134.
    Russo M, Petropoulos V, Molotokaite E, Cerullo G, Casazza AP et al. 2020. Ultrafast excited-state dynamics in land plants photosystem I core and whole supercomplex under oxidised electron donor conditions. Photosynth. Res. 144:2221–33
     [Google Scholar]
  135. 135.
    Liguori N, Novoderezhkin V, Roy LM, van Grondelle R, Croce R 2016. Excitation dynamics and structural implication of the stress-related complex LHCSR3 from the green alga Chlamydomonas reinhardtii. Biochim. Biophys. Acta Bioenerg. 1857:91514–23
     [Google Scholar]
  136. 136.
    Nicol L, Nawrocki WJ, Croce R. 2019. Disentangling the sites of non-photochemical quenching in vascular plants. Nat. Plants 5:111177–83
     [Google Scholar]
  137. 137.
    Townsend AJ, Saccon F, Giovagnetti V, Wilson S, Ungerer P, Ruban AV. 2018. The causes of altered chlorophyll fluorescence quenching induction in the Arabidopsis mutant lacking all minor antenna complexes. Biochim. Biophys. Acta Bioenerg. 1859:9666–75
     [Google Scholar]
  138. 138.
    Mascoli V, Liguori N, Xu P, Roy LM, van Stokkum IHM, Croce R. 2019. Capturing the quenching mechanism of light-harvesting complexes of plants by zooming in on the ensemble. Chem 5:112900–12
     [Google Scholar]
  139. 139.
    Ruban AV, Young AJ, Horton P. 1993. Induction of nonphotochemical energy dissipation and absorbance changes in leaves (evidence for changes in the state of the light-harvesting system of photosystem II in vivo). Plant Physiol. 102:3741–50
     [Google Scholar]
  140. 140.
    Wientjes E, Philippi J, Borst JW, van Amerongen H. 2017. Imaging the photosystem I/photosystem II chlorophyll ratio inside the leaf. Biochim. Biophys. Acta Bioenerg. 1858:3259–65
     [Google Scholar]
  141. 141.
    van Oort B, Roy LM, Xu P, Lu Y, Karcher D et al. 2018. Revisiting the role of xanthophylls in nonphotochemical quenching. J. Phys. Chem. Lett. 9:2346–52
     [Google Scholar]
  142. 142.
    Park S, Fischer AL, Steen CJ, Iwai M, Morris JM et al. 2018. Chlorophyll-carotenoid excitation energy transfer in high-light-exposed thylakoid membranes investigated by snapshot transient absorption spectroscopy. J. Am. Chem. Soc. 140:3811965–73
     [Google Scholar]
  143. 143.
    Pinnola A, Staleva-Musto H, Capaldi S, Ballottari M, Bassi R, Polívka T. 2016. Electron transfer between carotenoid and chlorophyll contributes to quenching in the LHCSR1 protein from Physcomitrella patens. Biochim. Biophys. Acta Bioenerg. 1857:121870–78
     [Google Scholar]
  144. 144.
    Liguori N, Xu P, van Stokkum IHM, van Oort B, Lu Y et al. 2017. Different carotenoid conformations have distinct functions in light-harvesting regulation in plants. Nat. Commun. 8:11994
     [Google Scholar]
  145. 145.
    Nowak J, Füller J, Walla PJ. 2022. Combined contributions of carotenoids and chlorophylls in two-photon spectra of photosynthetic pigment-protein complexes–a new way to quantify carotenoid dark state to chlorophyll energy transfer?. J. Chem. Phys. 156:19191103
     [Google Scholar]
  146. 146.
    Šebelík V, Kuznetsova V, Lokstein H, Polívka T. 2021. Transient absorption of chlorophylls and carotenoids after two-photon excitation of LHCII. J. Phys. Chem. Lett. 12:123176–81
     [Google Scholar]
  147. 147.
    Ahn TK, Avenson TJ, Ballottari M, Cheng YC, Niyogi KK et al. 2008. Architecture of a charge-transfer state regulating light harvesting in a plant antenna protein. Science 320:5877794–97
     [Google Scholar]
  148. 148.
    Park S, Steen CJ, Lyska D, Fischer AL, Endelman B et al. 2019. Chlorophyll–carotenoid excitation energy transfer and charge transfer in Nannochloropsis oceanica for the regulation of photosynthesis. PNAS 116:93385–90
     [Google Scholar]
  149. 149.
    Miloslavina Y, Wehner A, Lambrev PH, Wientjes E, Reus M et al. 2008. Far-red fluorescence: a direct spectroscopic marker for LHCII oligomer formation in NPQ. FEBS Lett. 582:25–263625–31
     [Google Scholar]
  150. 150.
    Chmeliov J, Gelzinis A, Songaila E, Augulis R, Duffy CDP et al. 2016. The nature of self-regulation in photosynthetic light-harvesting antenna. Nat. Plants 2:516045
     [Google Scholar]
  151. 151.
    Ishizaki A, Calhoun TR, Schlau-Cohen GS, Fleming GR 2010. Quantum coherence and its interplay with protein environments in photosynthetic electronic energy transfer. Phys. Chem. Chem. Phys. 12:277319–37
     [Google Scholar]
  152. 152.
    Liguori N, Periole X, Marrink SJ, Croce R. 2015. From light-harvesting to photoprotection: structural basis of the dynamic switch of the major antenna complex of plants (LHCII). Sci. Rep. 5:15661
     [Google Scholar]
  153. 153.
    Cignoni E, Lapillo M, Cupellini L, Acosta-Gutiérrez S, Gervasio FL, Mennucci B. 2021. A different perspective for nonphotochemical quenching in plant antenna complexes. Nat. Commun. 12:17152
     [Google Scholar]
  154. 154.
    Schlau-Cohen GS, Yang HY, Krüger TPJ, Xu P, Gwizdala M et al. 2015. Single-molecule identification of quenched and unquenched states of LHCII. J. Phys. Chem. Lett. 6:5860–67
     [Google Scholar]
  155. 155.
    Kondo T, Pinnola A, Chen WJ, Dall'Osto L, Bassi R, Schlau-Cohen GS. 2017. Single-molecule spectroscopy of LHCSR1 protein dynamics identifies two distinct states responsible for multi-timescale photosynthetic photoprotection. Nat. Chem. 9:8772–78
     [Google Scholar]
  156. 156.
    Troiano JM, Perozeni F, Moya R, Zuliani L, Baek K et al. 2021. Identification of distinct pH- and zeaxanthin-dependent quenching in LHCSR3 from Chlamydomonas reinhardtii. eLife 10:e60383
     [Google Scholar]
  157. 157.
    Manna P, Davies T, Hoffmann M, Johnson MP, Schlau-Cohen GS. 2021. Membrane-dependent heterogeneity of LHCII characterized using single-molecule spectroscopy. Biophys. J. 120:153091–102
     [Google Scholar]
  158. 158.
    Krüger TPJ, Ilioaia C, van Grondelle R. 2011. Fluorescence intermittency from the main plant light-harvesting complex: resolving shifts between intensity levels. J. Phys. Chem. B 115:185071–82
     [Google Scholar]
  159. 159.
    Johnson MP, Goral TK, Duffy CDP, Brain APR, Mullineaux CW, Ruban AV. 2011. Photoprotective energy dissipation involves the reorganization of photosystem II light-harvesting complexes in the grana membranes of spinach chloroplasts. Plant Cell 23:41468–79
     [Google Scholar]
  160. 160.
    Akhtar P, Görföl F, Garab G, Lambrev PH. 2019. Dependence of chlorophyll fluorescence quenching on the lipid-to-protein ratio in reconstituted light-harvesting complex II membranes containing lipid labels. Chem. Phys. 522:242–48
     [Google Scholar]
  161. 161.
    Nicol L, Croce R. 2021. The PsbS protein and low pH are necessary and sufficient to induce quenching in the light-harvesting complex of plants LHCII. Sci. Rep. 11:17415
     [Google Scholar]
  162. 162.
    Grieco M, Suorsa M, Jajoo A, Tikkanen M, Aro EM. 2015. Light-harvesting II antenna trimers connect energetically the entire photosynthetic machinery—including both photosystems II and I. Biochim. Biophys. Acta Bioenerg. 1847:6607–19
     [Google Scholar]
  163. 163.
    Mekala NR, Suorsa M, Rantala M, Aro EM, Tikkanen M. 2015. Plants actively avoid state transitions upon changes in light intensity: role of light-harvesting complex II protein dephosphorylation in high light. Plant Physiol. 168:2721–34
     [Google Scholar]
  164. 164.
    Peers G, Truong TB, Ostendorf E, Busch A, Elrad D et al. 2009. An ancient light-harvesting protein is critical for the regulation of algal photosynthesis. Nature 462:7272518–21
     [Google Scholar]
  165. 165.
    Gerotto C, Alboresi A, Giacometti G, Bassi R, Morosinotto T. 2011. Role of PSBS and LHCSR in Physcomitrella patens acclimation to high light and low temperature. Plant Cell Environ. 34:6922–32
     [Google Scholar]
  166. 166.
    Pinnola A. 2019. The rise and fall of Light-Harvesting Complex Stress-Related proteins as photoprotection agents during evolution. J. Exp. Bot. 70:205527–35
     [Google Scholar]
  167. 167.
    de la Cruz Valbuena G, Camargo FVA, Borrego-Varillas R, Perozeni F, D'Andrea C et al. 2019. Molecular mechanisms of nonphotochemical quenching in the LHCSR3 protein of Chlamydomonas reinhardtii. J. Phys. Chem. Lett. 10:102500–5
     [Google Scholar]
  168. 168.
    Kondo T, Gordon JB, Pinnola A, Dall'Osto L, Bassi R, Schlau-Cohen GS. 2019. Microsecond and millisecond dynamics in the photosynthetic protein LHCSR1 observed by single-molecule correlation spectroscopy. PNAS 116:2311247–52
     [Google Scholar]
/content/journals/10.1146/annurev-physchem-083122-111318
Loading
Ultrafast Dynamics of Photosynthetic Light Harvesting: Strategies for Acclimation Across Organisms
Annual Review of Physical Chemistry 74, 493 (2023); https://doi.org/10.1146/annurev-physchem-083122-111318
/content/journals/10.1146/annurev-physchem-083122-111318
/content/journals/10.1146/annurev-physchem-083122-111318
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error