Possible Mechanisms of Water Binding to the Oxygen-Evolving Complex during the S4-S0 Transition: A Theoretical Investigation

doi:10.6023/A17050214

Abstract

It has been acknowledged that molecular oxygen produced in photosynthesis originates from water, rather than carbon dioxide. Dioxygen releases in the S₄-S₀ transition immediately prior to a new water binding to the oxygen-evolving complex, but hardly any investigation has been carried out on the binding mechanism up to date. Based on the open-cubane oxo-oxyl coupling mechanism in the S₄ state of photosynthetic oxygen evolution, in this study we propose three possible pathways of water binding to the oxygen-evolving complex Mn₄CaO₄ during the S₄-S₀ transition, i.e. water binding to Ca trans to O5, water binding to Ca cis to O5, and water binding to Mn4 trans to O5. Broken-symmetry density functional theory (BS-DFT) calculations have demonstrated the thermodynamic feasibility for all these possible modes, without an overwhelming inclination for a certain manner. Besides, all these styles do not bring about any difference embodied in the experimental kinetic data on substrate water exchange in the S₁, S₂ and S₃ states, for the basically same structures of the S₀ state derived from these different routes. Therefore, it is considered that the alternative mechanisms could coexist coordinately in the connecting stage between S-state cycles. Importantly, diverse forms of substrate selectivity are deduced according to different water binding ways, which exert obvious influences on the present and later S-cycles. In the long run, however, it can be seen that the two waters binding in the S₄-S₀ and S₂-S₃ periods together constitute the components of the released O₂. What matters is variation of the time to become substrates for different water binding modes during the S₄-S₀ transition, either in the current cycle or in the following cycles. Meanwhile, it is indicated that the dangler Mn4(Ⅲ)/(IV) which possesses a five-coordinated pyramidal ligand field in both S'₀-S'₃ states, along with Ca(Ⅱ) on which the carrousel rearrangement of water ligands can also occur, are essential structural elements of the S-state advancement and oxygen evolution. Thus, Mn4 and Ca may be in charge of water delivery to the active sites of Mn₄CaO₅ from the nearby external water channels formed by crystal waters in hydrogen-bond interactions. On the whole, the geometric flexibility of the Mn cluster plays an important role in photosynthetic water oxidation. In the respects of water binding modes in the S₄-S₀ transition and corresponding substrate identifications for a specific S-cycle, we are looking forward to further confirmations or supplements from the experimental evidences of the targeted isotope labeling combined with mass spectrometry, infrared spectroscopy and site directed mutagenesis, etc. Our investigation may provide useful information and references for the mechanistic elucidations on photosynthetic water oxidation, especially in substrate water identifications.

Key words: photosynthesis, oxygen-evolving complex, S₄-S₀ transition, water binding mechanism, water channel, broken-symmetry density functional theory, thermodynamics, substrate selectivity

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Guo Yu, Liu Yu, Qi Juanjuan, Li Hui, He Lanlan, Lu Linan, Liu Cui, Gong Lidong, Zhao Dongxia, Yang Zhongzhi. Possible Mechanisms of Water Binding to the Oxygen-Evolving Complex during the S₄-S₀ Transition: A Theoretical Investigation[J]. Acta Chim. Sinica, 2017, 75(9): 914-921.

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[1] Mcintosh, C. L.; Blankenship, R. E., In Encyclopedia of Inorganic and Bioinorganic Chemistry, John Wiley & Sons, Ltd, St. Louis, 2014, pp. 1～27.
[2] Pokhrel, R.; Brudvig, G. W. In Comprehensive Inorganic Chemistry Ⅱ, Elsevier, New Haven, 2013, pp. 385～422.
[3] Mcevoy, J. P.; Brudvig, G. W. Chem. Rev. 2006, 106, 4455.
[4] Cox, N.; Pantazis, D. A.; Neese, F.; Lubitz, W. Acc. Chem. Res. 2013, 46, 1588.
[5] Ruben, S.; Randall, M.; Kamen, M.; Hyde, J. L. J. Am. Chem. Soc. 1941, 63, 877.
[6] Kok, B.; Forbush, B.; Mcgloin, M. Photochem. Photobiol. 1970, 11, 457.
[7] Navarro, M. P.; Neese, F.; Lubitz, W.; Pantazis, D. A.; Cox, N. Curr. Opin. Chem. Biol. 2016, 31, 113.
[8] Krewald, V.; Retegan, M.; Neese, F.; Lubitz, W.; Pantazis, D. A.; Cox, N. Inorg. Chem. 2016, 55, 488.
[9] Cox, N.; Messinger, J. Biochim. Biophys. Acta, Bioenergy 2013, 1827, 1020.
[10] Cox, N.; Retegan, M.; Neese, F.; Pantazis, D. A.; Boussac, A.; Lubitz, W. Science 2014, 345, 804.
[11] Siegbahn, P. E. M. Biochim. Biophys. Acta, Bioenergy 2013, 1827, 1003.
[12] Siegbahn, P. E. M. Acc. Chem. Res. 2009, 42, 1871.
[13] Nilsson, H.; Rappaport, F.; Boussac, A.; Messinger, J. Nat. Commun. 2014, 5, 4305.
[14] Vinyard, D. J.; Brudvig, G. W. Annu. Rev. Phys. Chem. 2017, 68, 101.
[15] Suga, M.; Akita, F.; Sugahara, M.; Kubo, M.; Nakajima, Y.; Nakane, T.; Yamashita, K.; Umena, Y.; Nakabayashi, M.; Yamane, T.; Nakano, T.; Suzuki, M.; Masuda, T.; Inoue, S.; Kimura, T.; Nomura, T.; Yonekura, S.; Yu, L.-J.; Sakamoto, T.; Motomura, T.; Chen, J.-H.; Kato, Y.; Noguchi, T.; Tono, K.; Joti, Y.; Kameshima, T.; Hatsui, T.; Nango, E.; Tanaka, R.; Naitow, H.; Matsuura, Y.; Yamashita, A.; Yamamoto, M.; Nureki, O.; Yabashi, M.; Ishikawa, T.; Iwata, S.; Shen, J.-R. Nature 2017, 543, 131.
[16] Suga, M.; Akita, F.; Hirata, K.; Ueno, G.; Murakami, H.; Nakajima, Y.; Shimizu, T.; Yamashita, K.; Yamamoto, M.; Ago, H.; Shen, J.-R. Nature 2015, 517, 99.
[17] Yano, J.; Yachandra, V. Chem. Rev. 2014, 114, 4175.
[18] Dau, H.; Zaharieva, I.; Haumann, M. Curr. Opin. Chem. Biol. 2012, 16, 3.
[19] Haumann, M.; Liebisch, P.; Müller, C.; Barra, M.; Grabolle, M.; Dau, H. Science 2005, 310, 1019.
[20] Britt, R. D.; Oyala, P. H. Science 2014, 345, 736.
[21] Narzi, D.; Bovi, D.; Guidoni, L. Proc. Natl. Acad. Sci. U. S. A. 2014, 111, 8723.
[22] Bovi, D.; Narzi, D.; Guidoni, L. Angew. Chem., Int. Ed. 2013, 52, 1.
[23] Siegbahn, P. E. M. Phys. Chem. Chem. Phys. 2012, 14, 4849.
[24] Retegan, M.; Krewald, V.; Mamedov, F.; Neese, F.; Lubitz, W.; Cox, N.; Pantazis, D. A. Chem. Sci. 2015, 7, 72.
[25] Askerka, M.; Wang, J.; Vinyard, D. J.; Brudvig, G. W.; Batista, V. S. Biochemistry 2016, 18, 181.
[26] Askerka, M.; Vinyard, D. J.; Brudvig, G. W.; Batista, V. S. Biochemistry 2015, 54, 5783.
[27] Askerka, M.; Brudvig, G. W.; Batista, V. S. Acc. Chem. Res. 2017, 50, 41.
[28] Nilsson, H.; Krupnik, T.; Kargul, J.; Messinger, J. Biochim. Biophys. Acta, Bioenergy 2014, 1837, 1257.
[29] Hendry, G.; Wydrzynski, T. Biochemistry 2003, 42, 6209.
[30] Hendry, G.; Wydrzynski, T. Biochemistry 2002, 41, 13328.
[31] Capone, M.; Narzi, D.; Bovi, D.; Guidoni, L. J. Phys. Chem. Lett. 2016, 7, 592.
[32] Umena, Y.; Kawakami, K.; Shen, J.-R.; Kamiya, N. Nature 2011, 473, 55.
[33] Guo, Y.; Yao, Y.; Li, H.; He, L.-L.; Zhu, Z.-W.; Yang, Z.-Z.; Gong, L.-D.; Liu, C.; Zhao, D.-X. Acta Chim. Sinica 2017, DOI: 10. 6023/A17040151. (郭宇, 姚远, 李慧, 赫兰兰, 朱尊伟, 杨忠志, 宫利东, 刘翠, 赵东霞, 化学学报, 2017, DOI: 10. 6023/A17040151.)
[34] Noodleman, L.; Case, D. A. Adv. Inorg. Chem. 1992, 38, 423.
[35] Noodleman, L.; Peng, C. Y.; Case, D. A.; Mouesca, L.-M. Coord. Chem. Rev. 1995, 144, 199.
[36] Noodleman, L.; Case, D. A.; Aizman, A. J. Am. Chem. Soc. 1988, 110, 1001.
[37] Noodleman, L. J. Chem. Phys. 1981, 74, 5737.
[38] Marenich, A. V.; Cramer, C. J.; Truhlar, D. G. J. Phys. Chem. B 2009, 113, 6378.
[39] Grimme, S.; Ehrlich, S.; Goerigk, L. J. Comput. Chem. 2011, 32, 1456.
[40] Guo, Y.; He, L.-L.; Zhao, D.-X.; Gong, L.-D.; Liu, C.; Yang, Z.-Z. Phys. Chem. Chem. Phys. 2016, 18, 31551.
[41] Guo, Y.; Li, H.; He, L.-L.; Zhao, D.-X.; Gong, L.-D.; Yang, Z.-Z. Phys. Chem. Chem. Phys. 2017, 19, 13909.
[42] Frisch, M. J.; Trucks, G. W.; Schlegel, H. B.; Scuseria, G. E.; Robb, M. A.; Cheeseman, J. R.; Scalmani, G.; Barone, V.; Mennucci, B.; Petersson, G. A.; Nakatsuji, H.; Caricato, M.; Li, X.; Hratchian, H. P.; Izmaylov, A. F.; Bloino, J.; Zheng, G.; Sonnenberg, J. L.; Hada, M.; Ehara, M.; Toyota, K.; Fukuda, R.; Hasegawa, J.; Ishida, M.; Nakajima, T.; Honda, Y.; Kitao, O.; Nakai, H.; Vreven, T.; Montgomery Jr., J. A.; Peralta, J. E.; Ogliaro, F.; Bearpark, M. J.; Heyd, J.; Brothers, E. N.; Kudin, K. N.; Staroverov, V. N.; Kobayashi, R.; Normand, J.; Raghavachari, K.; Rendell, A. P.; Burant, J. C.; Iyengar, S. S.; Tomasi, J.; Cossi, M.; Rega, N.; Millam, N. J.; Klene, M.; Knox, J. E.; Cross, J. B.; Bakken, V.; Adamo, C.; Jaramillo, J.; Gomperts, R.; Stratmann, R. E.; Yazyev, O.; Austin, A. J.; Cammi, R.; Pomelli, C.; Ochterski, J. W.; Martin, R. L.; Morokuma, K.; Zakrzewski, V. G.; Voth, G. A.; Salvador, P.; Dannenberg, J. J.; Dapprich, S.; Daniels, A. D.; Farkas,, Foresman, J. B.; Ortiz, J. V.; Cioslowski, J.; Fox, D. J., Gaussian 09, Revision D. 01, Gaussian, Inc., Wallingford, CT, USA, 2013.
[43] Suzuki, H.; Sugiura, M.; Noguchi, T. J. Am. Chem. Soc. 2009, 131, 7849.
[44] Krewald, V.; Retegan, M.; Cox, N.; Messinger, J.; Lubitz, W.; Debeer, S.; Neese, F.; Pantazis, D. A. Chem. Sci. 2015, 6, 1676.
[45] Pal, R.; Negre, C. F. A.; Vogt, L.; Pokhrel, R.; Ertem, M. Z.; Brudvig, G. W.; Batista, V. S. Biochemistry 2013, 52, 7703.
[46] Ames, W.; Pantazis, D. A.; Krewald, V.; Cox, N.; Messinger, J.; Lubitz, W.; Neese, F. J. Am. Chem. Soc. 2011, 133, 19743.
[47] Pantazis, D. A.; Ames, W.; Cox, N.; Lubitz, W.; Neese, F. Angew. Chem., Int. Ed. 2012, 51, 9935
[48] Capone, M.; Bovi, D.; Narzi, D.; Guidoni, L. Biochemistry 2015, 54, 6439.
[49] Klauss, A.; Haumann, M.; Dau, H. J. Phys. Chem. B 2014, 119, 2677.
[50] Klauss, A.; Haumann, M.; Dau, H. Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 16035.
[51] Dau, H.; Haumann, M. Biochim. Biophys. Acta, Bioenergy 2007, 1767, 472.
[52] Siegbahn, P. E. M. Chem. Eur. J. 2006, 12, 9217.
[53] Vinyard, D. J.; Khan, S.; Brudvig, G. W. Faraday Discuss. 2015, 185, 37.
[54] Sproviero, E. M.; Gascón, J. A.; Mcevoy, J. P.; Brudvig, G. W.; Batista, V. S. J. Am. Chem. Soc. 2008, 130, 3428.
[55] Navarro, M. P.; Ames, W. M.; Nilsson, H.; Lohmiller, T.; Pantazis, D. A.; Rapatskiy, L.; Nowaczyk, M. M.; Neese, F.; Boussac, A.; Messinger, J.; Lubitz, W.; Cox, N. Proc. Natl. Acad. Sci. U. S. A. 2013, 110, 15561.
[56] Siegbahn, P. E. M. Proc. Natl. Acad. Sci. U. S. A. 2017, 114, 4966.
[57] Kostelansky, M. S.; Lounes, K. C.; Ping, L. F.; Dickerson, S. K.; Gorkun, O. V.; Lord, S. T. Biochemistry 2004, 43, 2475.
[58] Rosta, E.; Yang, W.; Hummer, G. J. Am. Chem. Soc. 2014, 136, 3137.
[59] Whittaker, M. M.; Ekberg, C. A.; Edwards, R. A.; Baker, E. N.; Jameson, G. B.; Whittaker, J. W. J. Phys. Chem. B 1998, 102, 4668.
[60] Campbell, K. A.; Yikilmaz, E.; Grant, C. V.; Gregor, W.; Miller, A.-F.; Britt, R. D. J. Am. Chem. Soc. 1999, 121, 4714.
[61] Brunold, T. C.; Gamelin, D. R.; Stemmler, T. L.; Mandal, S. K.; Armstrong, W. H.; Penner-Hahn, J. E.; Solomon, E. I. J. Am. Chem. Soc. 1998, 120, 8724.
[62] Aromí, G.; Knapp, M. J.; Claude, J.-P.; Huffman, J. C.; Hendrickson, D. N.; Christou, G. J. Am. Chem. Soc. 1999, 121, 5489.
[63] Spasojevic, I.; Batinic-Haberle, I.; Stevens, R. D.; Hambright, P.; Thorpe, A. N.; Grodkowski, J.; Neta, P.; Fridovich, I. Inorg. Chem. 2001, 40, 726.
[64] Coggins, M. K.; Sun, X.; Kwak, Y.; Solomon, E. I.; Rybak-Akimova, E.; Kovacs, J. A. J. Am. Chem. Soc. 2013, 1355631.
[65] Sabater, M. J.; lvaro, M.; García, H.; Palomares, E.; Scaiano, J. C. J. Am. Chem. Soc. 2001, 123, 7074.
[66] Amin, M.; Vogt, L.; Vassiliev, S.; Rivalta, I.; Sultan, M. M.; Bruce, D.; Brudvig, G. W.; Batista, V. S.; Gunner, M. R. J. Phys. Chem. B 2013, 117, 6217.
[67] Wang, T.; Brudvig, G. W.; Batista, V. S. J. Chem. Theory Comput. 2010, 6, 2395.
[68] Li, X.; Siegbahn, P. E. M. Phys. Chem. Chem. Phys. 2015, 17, 12168.
[69] Hammond, G. S. J. Am. Chem. Soc. 1955, 77, 334.
[70] Rivalta, I.; Amin, M.; Luber, S.; Vassiliev, S.; Pokhrel, R.; Umena, Y.; Kawakami, K.; Shen, J.-R.; Kamiya, N.; Bruce, D.; Brudvig, G. W.; Gunner, M. R.; Batista, V. S. Biochemistry 2011, 50, 6312.
[71] Kim, C. J.; Debus, R. J. Biochemistry 2017, 56, 2558.
[72] Ugur, I.; Rutherford, A. W.; Kaila, V. R. I. Biochim. Biophys. Acta, Bioenergy 2016, 1857740.
[73] Retegan, M.; Pantazis, D. A. Chem. Sci. 2016, 7, 6463.

S₄-S₀转化期水结合至放氧复合体可能机制的理论研究

Possible Mechanisms of Water Binding to the Oxygen-Evolving Complex during the S₄-S₀ Transition: A Theoretical Investigation

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S4-S0转化期水结合至放氧复合体可能机制的理论研究