Excitation energy transfer in intact cells and in the phycobiliprotein antennae of the chlorophyll d containing cyanobacterium Acaryochloris marina

Journal of Plant Physiology

Volumn 168, Issue 12, 2011, Pages 1473-1487

  Theiss, Christoph ^a   Schmitt, Franz Josef ^a   Pieper, Jörg ^a,b   Nganou, Collins ^a   Grehn, Moritz ^a   Vitali, Marco ^a   Olliges, Rachel ^a   Eichler, Hans Joachim ^a   Eckert, Hann Jörg ^a  

^a TECHNISCHE UNIVERSITÄT BERLIN   (Germany)

^b UNIVERSITY OF TARTU   (Estonia)

Author keywords

Acaryochloris marina; Charge separation; Chl d; Excitation energy transfer; Photosystem II reactor center; Phycobiliproteins; Spectral hole burning

Indexed keywords

CHLOROPHYLL; CHLOROPHYLL D; PHYCOBILIPROTEIN;

BIOLOGICAL MODEL; CYANOBACTERIUM; CYTOLOGY; ENERGY TRANSFER; METABOLISM; PHOTOSYSTEM II; REVIEW;

CHLOROPHYLL; CYANOBACTERIA; ENERGY TRANSFER; MODELS, BIOLOGICAL; PHOTOSYSTEM II PROTEIN COMPLEX; PHYCOBILIPROTEINS;

ACARYOCHLORIS MARINA; CYANOBACTERIA;

EID: 79958766477     PISSN: 01761617     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jplph.2011.02.002     Document Type: Review

References (91)

1. Adir N. Elucidation of the molecular structures of components of the phycobilisome: reconstructing a giant. Photosynth Res 2005, 85:15-32.
2. Bergmann A., Eichler H., Eckert H., Renger G. Picosecond laser-fluorometer with simultaneous time and wavelength resolution for monitoring decay spectra of photoinhibited Photosystem II particles at 277K and 10K. Photosynth Res 1998, 58:303-310.
3. Bjorn L., Papageorgiou G.C., Blankenship R.E., Govindjee A viewpoint: Why chlorophyll a?. Photosynth Res 2009, 99:85-98.
4. Blankenship R, Govindjee. Photosynthesis. The encyclopedia of science and technology, 10th ed., vol. 13; 2007. p. 468-75.
5. Chan Y., Nenninger A., Clokie S.J., Mann N.H., Scanlan D.J., Whitworth A.L., et al. Pigment composition and adaptation in free-living and symbiotic strains of Acaryochloris marina. FEMS Microbiol Ecol 2007, 61:65-73.
6. Chen M., Bibby T.S., Nield J., Larkum A.W.D., Barber J. Structure of a large photosystem II supercomplex from Acaryochloris marina. FEBS Lett 2005, 579:1306-1310.
7. Chen M., Bibby T.S. Photosynthetic apparatus of antenna-reaction centres supercomplexes in oxyphotobacteria: insight through significance of Pcb/IsiA proteins. Photosynth Res 2005, 86:165-173.
8. Chen M., Floetenmeyer M., Bibby T.S. Supramolecular organization of phycobiliproteins in the chlorophyll d-containing cyanobacterium Acaryochloris marina. FEBS Lett 2009, 583:2535-2539.
9. Chen M., Quinnell R.G., Larkum A.W.D. The major light-harvesting pigment protein of Acaryochloris marina. FEBS Lett 2002, 514:149-152.
10. Chen M., Schliep M., Willows R.D., Cai Z.L., Neilan B.A., Scheer H. A red-shifted chlorophyll. Science 2010, 329:1318-1319.
11. Clegg R.M., Sener M., Govindjee From Förster resonance energy transfer (FRET) to coherent resonance energy transfer (CRET) and back. Proc SPIE 2010, 7561:7561-7612.
12. Csatorday K., MacColl R., Csizmadia V., Grabowski J., Bagyinka C. Exciton interaction in allophycocyanin. Biochemistry 1984, 23:6466-6470.
13. De Los Ríos A., Grube M., Sancho L.G., Ascaso C. Ultrastructural and genetic characteristics of endolithic cyanobacterial biofilms colonizing Antarctic granite rocks. FEMS Microbiol Ecol 2007, 59:386.
14. Debreczeny M., Sauer K., Zhou J.H., Bryant D. Comparison of calculated and experimentally resolved rate constants for excitation energy transfer in C-phycocyanin. 1. Monomers. J Phys Chem 1995, 99:8412-8419.
15. Debreczeny M., Sauer K., Zhou J.H., Bryant D. Comparison of calculated and experimentally resolved rate constants for excitation energy transfer in C-phycocyanin. 2. Trimers. J Phys Chem 1995, 99:8420-8431.
16. Diner B.A., Schlodder E., Nixon P.J., Coleman W.J., Rappaport F., Lavergne J., et al. Site-directed mutations at D1-His198 and D2-His 97 of photosystem II in synechocystis PCC 6803: sites of primary charge separation and cation and triplet stabilization. Biochemistry 2001, 40:9265-9281.
17. Duxbury Z., Schliep M., Ritchie R.J., Larkum A.W.D., Chen M. Chromatic photoacclimation extends utilizable photosynthetically active radiation in the chlorophyll d-containing cyanobacterium Acaryochloris marina. Photosynth Res 2009, 101:69-75.
18. Ferreira K.N., Iverson T.M., Maghlaoui K., Barber J., Iwata S. Architecture of the photosynthetic oxygen-evolving center. Science 2004, 303:1831-1838.
19. Funfschilling J., Glatz D., Zschokkegranacher I. Hole-burning spectroscopy as a tool to eliminate inhomogeneous broadening. J Lumin 1986, 36:85-92.
20. Gantt E., Lipschultz C., Grabowski J., Zimmerman B. Phycobilisomes from blue-green and red algae - isolation criteria and dissociation characteristics. Plant Physiol 1979, 63:615-620.
21. Gillbro T., Sandström A., Sundström V., Wendler J., Holzwarth A.R. Picosecond study of energy transfer kinetics in phycobilisomes of Synechococcus 6301 and the Mutant AN 112. Biochim Biophys Acta 1985, 808:52-65.
22. Gillbro T., Sharkov A., Kryukov I., Khoroshilov E., Kryukov P., Fischer R., et al. Forster energy-transfer between neighboring chromophores in C-phycocyanin trimers. Biochim Biophys Acta 1993, 1140:321-326.
23. Govindjee, Kern JF, Messinger J, Whitmarsh J. Photosystem II. In: Encyclopedia of life sciences. Chichester: John Wiley & Sons; 2010. p. 1-15. doi:1010029780470015902a0000669pub2.
24. Hastings G., Wang R. Vibrational mode frequency calculations of chlorophyll-d for assessing (P740(+)-P740) FTIR difference spectra obtained using photosystem I particles from Acaryochloris marina. Photosynth Res 2008, 95:55-62.
25. Hillmann B., Schlodder E. Electron-transfer reactions in photosystem-II core complexes from Synechococcus at low-temperature - difference spectrum of P680(+) Q(a)(-)/p680 Q(a) at 77K. Biochim Biophys Acta-Bioenerg 1995, 1231:76-88.
26. Holzwarth A., Bittersmann E., Reuter W., Wehrmeyer W. Studies on chromophore coupling in isolated phycobiliproteins. Biophys J 1990, 57:133-145.
27. Holzwarth A.R. Structure-function relationships and energy transfer in phycobiliprotein antennae. Physiol Plant 1991, 83:518-528.
28. Hu Q., Marquardt J., Iwasaki I., Kurano H., Miyashita N., Mörschel E., et al. Molecular structure localization and function of biliproteins in the chlorophyll a/d containing oxygenic photosynthetic procaryote Acaryochloris marina. Biochim Biophys Acta 1999, 1412:250-261.
29. Hu Q., Miyashita H., Iwasaki I., Kurano N., Miyachi S., Iwaki M., et al. A photosystem I reaction center driven by chlorophyll d in oxygenic photosynthesis. Proc Natl Acad Sci 1998, 95:13319-13323.
30. Itoh S., Mino H., Itoh K., Shigenaga T., Uzumaki T., Iwaki M. Function of chlorophyll d in reaction centers of photosysterns I and II of the oxygenic photosynthesis of Acaryochloris marina. Biochemistry 2007, 46:12473-12481.
31. Jaaniso R. Determination of homogenous spectra and the inhomogeneous distribution function by hole burning method. Proc Acad Sci Estonian SSR Phys Math 1985, 277-283.
32. Jankowiak R., Hayes J.M., Small G.J. Spectral hole burning spectroscopy in amorphous molecular solids and proteins. J Chem Rev 1993, 93:1471-1502.
33. Kashiyama Y., Miyashita H., Ohkubo S., Ogawa N.O., Chikaraishi Y., Takano Y., et al. Evidence of global chlorophyll d. Science 2008, 321:658-1658.
34. Kobayashi M., Ohashi S., Iwamoto K., Shiraiwa Y., Kato Y., Watanabe T. Redox potential of chlorophyll d in vitro. Biochim Biophys Acta-Bioenerg 2007, 1767:596-602.
35. Kobayashi M., Watanabe S., Gotoh T., Koizumi H., Itoh Y., Akiyama M., et al. Minor but key chlorophylls in Photosystem II. Photosynth Res 2005, 84:201-207.
36. Krumova S.B., Laptenok S.P., Borst J.W., Ughy B., Gombos Z., Ajlani G., et al. Monitoring photosynthesis in individual cells of Synechocystis sp. PCC 6803 on a picosecond timescale. Biophys J 2010, 99:2006-2015.
37. Lakowicz JR. Principles of fluorescence spectroscopy, vol. XXIII. New York [u.a.]: Kluwer Academic/Plenum Publ; 1999. 698S.
38. Larkum A.W.D., Kühl M. Chlorophyll d: the puzzle resolved. Trends Plant Sci 2005, 10/8:355-357.
39. Lee I., Hayes J.M., Small G.J. Hole and antihole profiles in nonphotochemical hole-burned spectra. J Chem Phys 1989, 91:3463-3469.
40. Liu L.N., Chen X.L., Zhang Y.Z., Zhou B.C. Characterization, structure and function of linker polypeptides in phycobilisomes of cyanobacteria and red algae: An overview. Biochim Biophys Acta-Bioenerg 2005, 1708:133-142.
41. Lokstein H., Steglich C., Hess W.R. Light-harvesting antenna function of phycoerythrin in Prochlorococcus marinus. Biochim Biophys Acta-Bioenerg 1999, 1410:97-98.
42. Loll B., Kern J., Zouni A., Saenger W., Biesiadka J., Irrgang K. The antenna systems of PS II from Thermosynechococcus elongatus at 3.2Å resolution. Photosynth Res 2005, 86:175-184.
43. Lundell D., Glazer A. Molecular architecture of a light-harvesting antenna - structure of the 18-S core-rod subassembly of the Synechococcus-6301 phycobilisome. J Biol Chem 1983, 258:894-901.
44. MacColl R. Allophycocyanin and energy transfer. Biochim Biophys Acta-Bioenerg 2004, 1657:73-81.
45. MacColl R. Cyanobacterial phycobilisomes. J Struct Biol 1998, 124:311-334.
46. Marquardt J., Moerschel E., Rhiel E., Westerman M. Ultrastrucutre of Acaryochloris marina, an oxyphotobacterium containing mainly chlorophyll d. Arch Microbiol 2000, 174:181-188.
47. Marquardt J., Senger H., Miyashita H., Miyachi S., Mörschel E. Isolation and characterisation of biliprotein aggregates from Acaryochloris marina, a prochloron-like prokaryote containing mainly chlorophyll d. FEBS Lett 1997, 410:428-432.
48. Mi D., Chen M., Lin S., Lince M., Larkum A.W.D., Blankenship R.E., et al. Excitation dynamics in the core antenna in the photosystem i reaction center of the chlorophyll d-containing photosynthetic prokaryote Acaryochloris marina. J Phys Chem B 2003, 107:1452-1457.
49. Miller S.R., Augustine S., Olson T.L., Blankenship R.E., Selker J., Wood A.M. Discovery of a free-living chlorophyll d-producing cyanobacterium with a hybrid proteobacterial/cyanobacterial small-subunit rRNA gene. Proc Natl Acad Sci 2005, 102:850-855.
50. Mimuro M., Akimoto S., Gotoh T., Yokono M., Akiyama M., Tsuchiya T., et al. Identification of the primary electron donor in PS II of the Chl d -dominated cyanobacterium Acaryochloris marina. FEBS Lett 2004, 556:95-98.
51. Mimuro M., Akimoto S., Yamazaki I., Miyachi H., Miyashita S. Fluorescence properties of chlorophyll d-dominating prokaryotic algae, Acaryochloris marina: studies using time-resolved fluorescence spectroscopy on intact cells. Biochim Biophys Acta 1999, 1412:37-46.
52. Mimuro M., Füglistaller P., Rümbeli R., Zuber H. Functional assignment of chromophores and energy transfer in C phycocyanin isolated from the thermophilic cyanobacterium Mastigocladus laminosus. Biochim Biophys Acta 1986, 848:155-166.
53. Mimuro M., Lipschultz C., Gantt E. Energy flow in the phycobilisome core of Nostoc sp. (MAC): two independent terminal pigments. Biochim Biophys Acta 1986, 852:126-132.
54. Mimuro M., Yamazaki I., Tamai N., Katoh T. Excitation energy transfer in phycobilisomes at -196°C isolated from the cyanobacterium Anabaena variabilis (M-3): evidence for the plural transfer pathways to the terminal emitters. Biochim Biophys Acta 1989, 973:153-162.
55. Mimuro M. Photon capture, exciton trapping and fluorescence emission in cyanobacteria and red algae. Chlorophyll a fluorescence: a signature of photosynthesis 2004, 173-195. Springer, Dordrecht.
56. Miyashita H., Ikemoto H., Kurano N., Adachi K., Chihara M., Miyachi S. Chlorophyll d as a major pigment. Nature 1996, 383:402-1402.
57. Mullineaux C.W., Holzwarth A.R. Kinetics of excitation energy transfer in the cyanobacterial phycobilisome-photosystem II complex. Biochim Biophys Acta 1991, 1098:68-78.
58. Murakami A., Miyashita H., Iseki M., Adachi K., Mimuro M. Chlorophyll d in an epiphytic cyanobacterium of red algae. Science 2004, 303:1633-11633.
59. Nieuwenburg P., Clarke R.J., Cai Z.L., Chen M., Larkum A.W.D., Cabral N.M., et al. Examination of the photophysical processes of chlorophyll d leading to a clarification of proposed uphill energy transfer processes in cells of Acaryochloris marina. Photochem Photobiol 2003, 77:628-637.
60. Ohashi S., Miyashita H., Okada N., Iemura T., Watanabe T., Kobayashi M. Unique photosystems in Acaryochloris marina. Photosynth Res 2008, 98:141-149.
61. Petrasek Z., Schmitt F.J., Theiss C., Huyer J., Chen M., Larkum A., et al. 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 2005, 12:1116-1122.
62. Pieper J., Schödel R., Irrgang K., Voigt J., Renger G. Electron-phonon coupling in solubilized LHC II complexes of green plants investigated by line-narrowing and temperature-dependent fluorescence spectroscopy. J Phys Chem B 2001, 105:7115-7124.
63. Pieper J., Voigt J., Renger G., Small G. Analysis of phonon structure in line-narrowed optical spectra. Chem Phys Lett 1999, 310:296-302.
64. Pieper J, Rätsep M, Eichler HJ, Eckert HJ. Low-energy level structure and electron-phonon coupling of phycobiliproteins of the cyanobacterium Acaryochloris marina investigated by site-selective spectroscopy. J Phys Chem D 2011; submitted.
65. Purchase R., Völker S. Spectral hole burning: examples from photosynthesis. Photosynth Res 2009, 101:245-266.
66. Rätsep M., Freiberg A. Electron-phonon and vibronic couplings in the FMO bacteriochlorophyll a antenna complex studied by difference fluorescence line narrowing. J Lumin 2007, 127:251-259.
67. Rätsep M., Freiberg A. Resonant emission from the B870 exciton state and electron-phonon coupling in the LH2 antenna chromoprotein. Chem Phys Lett 2003, 377:371-376.
68. Rätsep M., Pieper J., Irrgang K., Freiberg A. Excitation wavelength-dependent electron-phonon and electron-vibrational coupling in the CP29 antenna complex of green plants. J Phys Chem B 2008, 112:110-118.
69. Razeghifard M.R., Chen M., Hughes J.L., Freeman J., Krausz E., Wydrzynski T. Spectroscopic studies of photosystem II in chlorophyll d-containing Acaryochloris marina. Biochemistry 2005, 44:11178-11187.
70. Renger T., Madjet M.E., Muh F., Trostmann I., Schmitt F.J., Theiss C., et al. Thermally activated superradiance and intersystem crossing in the water-soluble chlorophyll binding protein. J Phys Chem B 2009, 113:9948-9957.
71. Renger T., Schlodder E. Primary photophysical processes in photosystem II: bridging the gap between crystal structure and optical spectra. Chem Phys Chem 2010, 11:1141-1153.
72. Renger T., Schlodder E. The primary electron donor of photosystem II of the cyanobacterium Acaryochloris marina is a chlorophyll d and the water oxidation is driven by a chlorophyll a/chlorophyll d heterodimer. J Phys Chem B 2008, 112:7351-7354.
73. Renger T., Trostmann I., Theiss C., Madjet M.E., Richter M., Paulsen H., et al. Refinement of a structural model of a pigment-protein complex by accurate optical line shape theory and experiments. J Phys Chem B 2007, 111:10487-10501.
74. Reppert M., Naibo V., Jankowiak R. Accurate modeling of fluorescence line narrowing difference spectra: direct measurement of the single-site fluorescence spectrum. J Chem Phys 2010, 133:1-9. 014506.
75. Reppert M., Naibo V., Jankowiak R. Analytical formulas for low-fluence non-line-narrowed hole-burned spectra in an excitonically coupled dimer. J Chem Phys 2009, 131:1-11. 234104.
76. Rogl H., Schodel R., Lokstein H., Kuhlbrandt W., Schubert A. Assignment of spectral substructures to pigment-binding sites in higher plant light-harvesting complex LHC-II. Biochemistry 2002, 41:2281-2287.
77. Sarcina M., Tobin M.J., Mullineaux C.W. Diffusion of phycobilisomes on the thylakoid membranes of the cyanobacterium Synechococcus 7942-effects of phycobilisome size, temperature, and membrane lipid composition. J Biol Chem 2001, 276:46830-46834.
78. Sauer K., Scheer H. Exciton transfer in C-phycocyanin. Förster transfer rate and excitonic calculations based on new crystal structure data for C-phycocyanins from Agmenellum quadruplicatum and Mastigocladus laminosus. Biochim Biophys Acta 1988, 936:157-170.
79. Scheer H, Schneider S. Photosynthetic light harvesting systems. Organization and function, vol. XV. Berlin [u.a.]: de Gruyter; 1988. p. 631.
80. Schlodder E., Cetin M., Eckert H., Schmitt F., Barber J., Telfer A. Both chlorophylls a and d are essential for the photochemistry in photosystem II of the cyanobacteria, Acaryochloris marina. Biochim Biophys Acta-Bioenerg 2007, 1767:589-595.
81. Schmitt F.J., Trostmann I., Theiss C., Pieper J., Renger T., Fuesers J., et al. Excited state dynamics in recombinant water-soluble chlorophyll proteins (WSCP) from cauliflower investigated by transient fluorescence spectroscopy. J Phys Chem B 2008, 112:13951-13961.
82. Schmitt F.J., Wache K., Fuesers J., Andree S., Handojo A., Karradt A., et al. Investigation of the excited states dynamics in the Chl d-containing cyanobacterium Acaryochloris marina by time- and wavelength correlated single-photon counting. Proc SPIE 2006, 6386:6386-6387.
83. Sharkov A., Kryukov I., Khoroshilov E., Kryukov P., Fischer R., Scheer H., et al. Femtosecond spectral and anisotropy study of excitation-energy transfer between neighboring alpha-80 and beta-81 chromophores of allophycocyanin trimers. Biochim Biophys Acta-Bioenerg 1994, 1188:349-356.
84. Shen J., Umena Y., Kawakami K., Kamiya N. Crystal structure of oxygen evolving photosystem II at an atomic resolution. Proceedings of the 15th international congress of photosynthesis, photosynthesis, research for food, fuel and the future 2010, 87-88.
85. Suter G.W., Holzwarth A.R. A kinetic-model for the energy-transfer in phycobilisomes. Biophys J 1987, 52:673-683.
86. Theiss C., Leupold D., Moskalenko A.A., Razjivin A.P., Eichler H.J., Lokstein H. Femtosecond spectroscopy of native and carotenoidless purple-bacterial LH2 clarifies functions of carotenoids. Biophys J 2008, 94:4808-4811.
87. Theiss C., Schmitt F.J., Andree S., Cardenas-Chavez C., Wache K., Fuesers J., et al. Excitation energy transfer in the phycobiliprotein antenna of Acaryochloris marina studied by transient fs absorption and fluorescence spectroscopy. Photosynthesis: energy from the sun. 14th International Congress on Photosynthesis 2008, 339-342. Springer, Dordrecht.
88. Theiss C., Trostmann I., Andree S., Schmitt F.J., Renger T., Eichler H.J., et al. Pigment-pigment and pigment-protein interactions in recombinant water-soluble chlorophyll proteins (WSCP) from cauliflower. J Phys Chem B 2007, 111:13325-13335.
89. Theiss C. Transiente femtosekunden-absorptionsspektroskopie des anregungs-energietransfers in isolierten pigment-proteinkomplexen des photosyntheseapparates 2006, Mensch-und-Buch-Verlag, Berlin.
90. Tomo T., Okubo T., Akimoto S., Yokono M., Miyashita H., Tsuchiya T., et al. Identification of the special pair of photosystem II in a chlorophyll d-dominated cyanobacterium. Proc Natl Acad Sci 2007, 104:7283-7288.
91. Xie X., Du M., Mets L., Fleming G. Femtosecond fluorescence depolarization study of photosynthetic antenna proteins: observation of ultrafast energy transfer in trimeric C-phycocyanin and allophycocyanin. Time-resolved laser spectroscopy in biochemistry III. Proc SPIE 1992, 690-706.