Abstract
Angular dependence of the proton matrix electron nuclear double resonance (ENDOR) spectra was investigated in the oriented Ca2+-depleted Photosystem II (PS II). Six pairs of the proton signals have been previously detected in the untreated PS II and one of the six pairs has been disappeared in the Ca2+-depleted PS II (Nagashima and Mino, J Biol Chem 290:28166–28174, 2015), where the proton signals with 4 MHz separation were lost and assigned to the proton closest to the terminal Mn, labeled as Mn4 in the Mn cluster. In the oriented Ca2+-depleted PS II, the proton signal with 4 MHz separation was disappeared when the external magnetic field is parallel to the membrane normal n (θ = 0°). A pair of broad ENDOR signals with 1.4–2.0 MHz hyperfine coupling was detected in the oriented Ca2+-depleted PS II at θ = 90°. These results indicate the Ca2+-depletion derives the rearrangement of the hydrogen bonding of the water molecule surrounded Mn cluster.
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N. Nelson, C.F. Yocum, Annu. Rev. Plant Biol. 57, 521–565 (2006)
D.J. Vinyard, G.M. Ananyev, G.C. Dismukes, Annu. Rev. Biochem. 82, 577–606 (2013)
J.P. McEvoy, G.W. Brudvig, Chem. Rev. 106, 4455–4483 (2006)
J.R. Shen, Annu. Rev. Plant Biol. 66, 23–48 (2015)
Y. Umena, K. Kawakami, J.-R. Shen, N. Kamiya, Nature 473, 55–60 (2011)
M. Suga, F. Akita, K. Hirata, G. Ueno, H. Murakami, Y. Nakajima, T. Shimizu, K. Yamashita, M. Yamamoto, H. Ago, J.-R. Shen, Nature 517, 99–103 (2015)
M. Suga, F. Akita, M. Sugahara, M. Kubo, Y. Nakajima, T. Nakane, K. Yamashita, Y. Umena, M. Nakabayashi, T. Yamane, T. Nakano, M. Suzuki, T. Masuda, S. Inoue, T. Kimura, T. Nomura, S. Yonekura, L.J. Yu, T. Sakamoto, T. Motomura, J.H. Chen, Y. Kato, T. Noguchi, K. Tono, Y. Joti, T. Kameshima, T. Hatsui, E. Nango, R. Tanaka, H. Naitow, Y. Matsuura, A. Yamashita, M. Yamamoto, O. Nureki, M. Yabashi, T. Ishikawa, S. Iwata, J.R. Shen, Nature 543, 131–135 (2017)
I.D. Young, M. Ibrahim, R. Chatterjee, S. Gul, F.D. Fuller, S. Koroidov, A.S. Brewster, R. Tran, R. Alonso-Mori, T. Kroll, T. Michels-Clark, H. Laksmono, R.G. Sierra, C.A. Stan, R. Hussein, M. Zhang, L. Douthit, M. Kubin, C. de Lichtenberg, L. Vo Pham, H. Nilsson, M.H. Cheah, D. Shevela, C. Saracini, M.A. Bean, I. Seuffert, D. Sokaras, T.C. Weng, E. Pastor, C. Weninger, T. Fransson, L. Lassalle, P. Brauer, P. Aller, P.T. Docker, B. Andi, A.M. Orville, J.M. Glownia, S. Nelson, M. Sikorski, D. Zhu, M.S. Hunter, T.J. Lane, A. Aquila, J.E. Koglin, J. Robinson, M. Liang, S. Boutet, A.Y. Lyubimov, M. Uervirojnangkoorn, N.W. Moriarty, D. Liebschner, P.V. Afonine, D.G. Waterman, G. Evans, P. Wernet, H. Dobbek, W.I. Weis, A.T. Brunger, P.H. Zwart, P.D. Adams, A. Zouni, J. Messinger, U. Bergmann, N.K. Sauter, J. Kern, V.K. Yachandra, J. Yano, Nature 540, 453–457 (2016)
J. Messinger, J.H. Robblee, W.O. Yu, K. Sauer, V.K. Yachandra, M.P. Klein, J. Am. Chem. Soc. 119, 11349–11350 (1997)
A. Boussac, M. Sugiura, A.W. Rutherford, P. Dorlet, J. Am. Chem. Soc. 131, 5050–5051 (2009)
G.C. Dismukes, Y. Siderer, Proc. Natl. Acad. Sci. USA 78, 274–278 (1981)
H. Mino, A. Kawamori, Biochim. Biophys. Acta 1503, 112–122 (2001)
T. Matsukawa, H. Mino, D. Yoneda, A. Kawamori, Biochemistry 38, 4072–4077 (1999)
T. Yamauchi, H. Mino, T. Matsukawa, A. Kawamori, T. Ono, Biochemistry 36, 7520–7526 (1997)
N. Cox, L. Rapatskiy, J.-H. Su, D.A. Pantazis, M. Sugiura, L.V. Kulik, P. Dorlet, A.W. Rutherford, F. Neese, A. Boussac, W. Lubitz, J. Messinger, J. Am. Chem. Soc. 133, 3635–3648 (2011)
J.M. Peloquin, K.A. Campbell, D.W. Randall, M.A. Evanchik, V.L. Pecoraro, W.H. Armstrong, R.D. Britt, J. Am. Chem. Soc. 122, 10926–10942 (2000)
T. Lohmiller, V. Krewald, A. Sedoud, A.W. Rutherford, F. Neese, W. Lubitz, D.A. Pantazis, N. Cox, J. Am. Chem. Soc. 139, 14412–14424 (2017)
T.A. Stich, G.J. Yeagle, R.J. Service, R.J. Debus, R.D. Britt, Biochemistry 50, 7390–7404 (2011)
G.J. Yeagle, M.L. Gilchrist, R.M. McCarrick, R.D. Britt, Inorg. Chem. 47, 1803–1814 (2008)
M. Asada, H. Nagashima, F.H.M. Koua, J.-R. Shen, A. Kawamori, H. Mino, Biochim. Biophys. Acta 1827, 438–445 (2013)
H. Nagashima, H. Mino, Biochim. Biophys. Acta 1827, 1165–1173 (2013)
H. Nagashima, Y. Nakajima, J.-R. Shen, H. Mino, J. Biol. Chem. 290, 28166–28174 (2015)
H. Nagashima, H. Mino, J. Phys. Chem. Lett. 8, 621–625 (2017)
H. Yamada, H. Mino, S. Itoh, Biochim. Biophys. Acta 1767, 197–203 (2007)
L. Rapatskiy, N. Cox, A. Savitsky, W.M. Ames, J. Sander, M.M. Nowaczyk, M. Rögner, A. Boussac, F. Neese, J. Messinger, W. Lubitz, J. Am. Chem. Soc. 134, 16619–16634 (2012)
W.M. Ames, D.A. Pantazis, V. Krewald, N. Cox, J. Messinger, W. Lubitz, F. Neese, J. Am. Chem. Soc. 133, 19743–19757 (2011)
S. Nakamura, T. Noguchi, J. Am. Chem. Soc. 139, 9364–9375 (2017)
K. Saito, A.W. Rutherford, H. Ishikita, Nat. Commun. 6, 8488 (2015)
M. Askerka, D.J. Vinyard, J.M. Wang, G.W. Brudvig, V.S. Batista, Biochemistry 54, 1713–1716 (2015)
H. Isobe, M. Shoji, J.R. Shen, K. Yamaguchi, J. Phys. Chem. B 119, 13922–13933 (2015)
C.F. Yocum, Coord. Chem. Rev. 252, 296–305 (2008)
V.K. Yachandra, J. Yano, J. Photochem. Photobiol. 104, 51–59 (2011)
M. Miqyass, H.J. van Gorkom, C.F. Yocum, Photosynth. Res. 92, 275–287 (2007)
T. Ono, Y. Inoue, Biochim. Biophys. Acta 850, 380–389 (1986)
M. Sivaraja, J. Tso, G.C. Dismukes, Biochemistry 28, 9459–9464 (1989)
A. Boussac, J.-L. Zimmermann, A.W. Rutherford, Biochemistry 28, 8984–8989 (1989)
T. Ono, Y. Inoue, Arch. Biochem. Biophys. 275, 440–448 (1989)
T. Ono, Y. Inoue, FEBS Lett. 227, 147–152 (1988)
T.A. Ono, Y. Inoue, Biochim. Biophys. Acta 1015, 373–377 (1990)
T. Ono, Y. Inoue, Biochim. Biophys. Acta 1020, 269–277 (1990)
D.F. Ghanotakis, G.T. Babcock, C.F. Yocum, FEBS Lett. 167, 127–130 (1984)
D.F. Ghanotakis, J.N. Topper, G.T. Babcock, C.F. Yocum, FEBS Lett. 170, 169–173 (1984)
A. Boussac, A.W. Rutherford, Biochemistry 27, 3476–3483 (1988)
J. Tso, M. Sivaraja, J.S. Philo, G.C. Dismukes, Biochemistry 30, 4740–4747 (1991)
A. Haddy, B.M. Ore, Biochemistry 49, 3805–3814 (2010)
F.H.M. Koua, Y. Umena, K. Kawakami, J.-R. Shen, Proc. Natl. Acad. Sci. USA 110, 3889–3894 (2013)
K. Saito, H. Ishikita, Biochim. Biophys. Acta 1837, 159–166 (2014)
D.A. Berthold, G.T. Babcock, C.F. Yocum, FEBS Lett. 134, 231–234 (1981)
K. Hasegawa, M. Kusunoki, Y. Inoue, T. Ono, Biochemistry 37, 9457–9465 (1998)
H. Mino, A. Ishii, T. Ono, Biochim. Biophys. Acta 1606, 127–136 (2003)
T. Lohmiller, N. Cox, J.-H. Su, J. Messinger, W. Lubitz, J. Biol. Chem. 287, 24721–24733 (2012)
A. Kawamori, T. Inui, T. Ono, Y. Inoue, FEBS Lett. 254, 219–224 (1989)
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This work was supported by a Grant-in-Aid for Scientific Research (No. 17J01125) for H.N.
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Nagashima, H., Mino, H. Local Structural Modification of Ca2+-Depleted Photosystem II Detected by Proton Matrix ENDOR. Appl Magn Reson 49, 803–812 (2018). https://doi.org/10.1007/s00723-018-1006-1
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DOI: https://doi.org/10.1007/s00723-018-1006-1