Comparisons of Electron Transfer Reactions in a Cyanobacterial Tetrameric and Trimeric Photosystem I Complexes

Photosystem I (PSI) is a Type‐I reaction center and is the largest photosynthetic complex to be characterized. In cyanobacteria, PSI is organized as a trimer with a three‐fold axis of symmetry. Recently, a tetrameric form of PSI has been identified in cyanobacteria. Plastids in plants and algae only contain monomeric PSI, suggesting that tetrameric PSI may be key in the transition from ancestral cyanobacterial trimeric PSI to plant/algal monomeric PSI. We have investigated the kinetics of electron transfer to the initial acceptor in PSI tetramer isolated from Chroococcidiopsis TS‐821. Using a pump–probe technique with 25 fs low‐energy, 720 nm pump pulses, we measure the ultrafast (<100 fs) conversion of a delocalized exciton into a charge‐separated state between the primary donor P700 and the primary acceptor A0. Comparison with previous pump–probe analysis of the trimeric PSI complexes from Synechocystis sp PCC 6803 (Shelaev et al. [2010] Biochim Biophys Acta, 1797, 1410–1420) reveals that the tetrameric (PSI) complexes from Chroococcidiopsis sp TS‐821 are quite similar. The transfer of an electron from the A0 to the following acceptor A1 (phylloquinone) takes place in a time frame of about 30 ps, which is slightly longer compared to PSI trimeric complex (~24 ps). The slight spectral differences between trimeric and tetrameric PSI complexes are discussed.

[1]  V. Shuvalov,et al.  Mechanism of adiabatic primary electron transfer in photosystem I: Femtosecond spectroscopy upon excitation of reaction center in the far-red edge of the QY band. , 2017, Biochimica et biophysica acta. Bioenergetics.

[2]  M. Li,et al.  Cryo-EM structure of a tetrameric cyanobacterial photosystem I complex reveals novel subunit interactions. , 2016, Biochimica et biophysica acta.

[3]  Amy K. Manocchi,et al.  Comparative photoactivity and stability of isolated cyanobacterial monomeric and trimeric Photosystem I. , 2014, The journal of physical chemistry. B.

[4]  R. Jankowiak,et al.  Mechanism of Primary Charge Separation in Photosynthetic Reaction Centers , 2014 .

[5]  E. Schlodder,et al.  Red antenna states of Photosystem I trimers from Arthrospira platensis revealed by single-molecule spectroscopy. , 2012, Biochimica et biophysica acta.

[6]  I. V. van Stokkum,et al.  Cofactors involved in light-driven charge separation in photosystem I identified by subpicosecond infrared spectroscopy. , 2011, Biochemistry.

[7]  M. Ikeuchi,et al.  Novel supercomplex organization of photosystem I in Anabaena and Cyanophora paradoxa. , 2011, Plant & cell physiology.

[8]  V. Shuvalov,et al.  Femtosecond primary charge separation in Synechocystis sp. PCC 6803 photosystem I. , 2010, Biochimica et biophysica acta.

[9]  B. Warscheid,et al.  Structure and function of intact photosystem 1 monomers from the cyanobacterium Thermosynechococcus elongatus. , 2010, Biochemistry.

[10]  Rajiv Luthra,et al.  Independent initiation of primary electron transfer in the two branches of the photosystem I reaction center , 2010, Proceedings of the National Academy of Sciences.

[11]  P. Frymier,et al.  Self-organized photosynthetic nanoparticle for cell-free hydrogen production. , 2010, Nature nanotechnology.

[12]  J. Golbeck,et al.  Protein-cofactor interactions in bioenergetic complexes: the role of the A1A and A1B phylloquinones in Photosystem I. , 2009, Biochimica et biophysica acta.

[13]  Nathan Nelson,et al.  The structure of a plant photosystem I supercomplex at 3.4 Å resolution , 2007, Nature.

[14]  W. Lubitz,et al.  Ultrafast transient absorption studies on photosystem I reaction centers from Chlamydomonas reinhardtii. 2: mutations near the P700 reaction center chlorophylls provide new insight into the nature of the primary electron donor. , 2006, Biophysical journal.

[15]  J. Golbeck.  Photosystem I : the light-driven plastocyanin : ferredoxin oxidoreductase , 2006 .

[16]  S. Savikhin.  Ultrafast Optical Spectroscopy of Photosystem I , 2006 .

[17]  E. Boekema,et al.  Photosystem I: a search for green plant trimers , 2005, Photochemical & photobiological sciences : Official journal of the European Photochemistry Association and the European Society for Photobiology.

[18]  Petra Fromme,et al.  Structure of cyanobacterial Photosystem I , 2005, Photosynthesis Research.

[19]  Lothar Jänsch,et al.  Proteomic approach to characterize the supramolecular organization of photosystems in higher plants. , 2004, Phytochemistry.

[20]  E. Boekema,et al.  Photosystem I from the unusual cyanobacterium Gloeobacter violaceus , 2004, Photosynthesis Research.

[21]  Nathan Nelson,et al.  Crystal structure of plant photosystem I , 2003, Nature.

[22]  W Leibl,et al.  Electron transfer in photosystem I. , 2001, Biochimica et biophysica acta.

[23]  Petra Fromme,et al.  Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution , 2001, Nature.

[24]  P. Joliot,et al.  Evidence for two active branches for electron transfer in photosystem I , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[25]  R. Nechushtai,et al.  Monomeric and trimeric forms of photosystem I reaction center of Mastigocladus laminosus: crystallization and preliminary characterization. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[26]  P. Sétif,et al.  Identification of electron-transfer reactions involving the acceptor A1 of photosystem I at room temperature , 1989 .

[27]  K. Brettel.  Electron transfer from A− 1 to an iron‐sulfur center with t = 200 ns at room temperature in photosystem I Characterization by flash absorption spectroscopy , 1988 .

[28]  M. van Heel,et al.  Evidence for a trimeric organization of the photosystem I complex from the thermophilic cyanobacterium Synechococcus sp. , 1987 .