Photosynthesis Research

, Volume 124, Issue 1, pp 7–18 | Cite as

Metal ion oxidation state assignment based on coordinating ligand hyperfine interaction



In exchange-coupled mixed-valence spin systems, the magnitude and sign of the effective ligand hyperfine interaction (HFI) can be useful in determining the formal oxidation state of the coordinating metal ion, as well as provide information about the coordination geometry. This is due to the fact that the observed ligand HFI is a function of the projection factor (Clebsch-Gordon coefficient) that maps the site spin value Si of the local paramagnetic center onto the total spin of the exchange-coupled system, ST. Recently, this relationship has been successfully exploited in identifying the oxidation state of the Mn ion coordinated by the sole nitrogenous ligand to the oxygen-evolving complex in certain states of photosystem II. The origin and evolution of these efforts is described.


Electron paramagnetic resonance Photosystem II Hyperfine Exchange coupling Electronic structure 



The authors acknowledge the Division of Chemical Sciences, Geosciences, and Biosciences, Office of Basic Energy Sciences of the U.S. Department of Energy through Grant DE-FG02-11ER16282 for funding the PSII research conducted in the Britt Laboratory.


  1. Abdalla JAB, Bowen AM, Bell SG, Wong LL, Timmel CR, Harmer J (2012) Characterisation of the paramagnetic 2Fe–2S (+) centre in palustrisredoxin-B (PuxB) from Rhodopseudomonas palustris CGA009: g-matrix determination and spin coupling analysis. Phys Chem Chem Phys 14(18):6526–6537PubMedCrossRefGoogle Scholar
  2. Barynin VV, Whittaker MM, Antonyuk SV, Lamzin VS, Harrison PM, Artymiuk PJ, Whittaker JW (2001) Crystal structure of manganese catalase from Lactobacillus plantarum. Structure 9(8):725–738PubMedCrossRefGoogle Scholar
  3. Beinert H, Kennedy MC, Stout CD (1996) Aconitase as iron–sulfur protein, enzyme, and iron-regulatory protein. Chem Rev 96(7):2335–2373PubMedCrossRefGoogle Scholar
  4. Bencini A, Gatteschi D (1990) EPR of exchange coupled systems. Springer, BerlinGoogle Scholar
  5. Berkovitch F, Nicolet Y, Wan JT, Jarrett JT, Drennan CL (2004) Crystal structure of biotin synthase, an S-adenosylmethionine-dependent radical enzyme. Science 303(5654):76–79PubMedCentralPubMedCrossRefGoogle Scholar
  6. Berry EA, Guergova-Kuras M, Huang LS, Crofts AR (2000) Structure and function of cytochrome bc complexes. Annu Rev Biochem 69:1005–1075PubMedCrossRefGoogle Scholar
  7. Britt RD, Sauer K, Klein MP, Knaff DB, Kriauciunas A, Yu CA, Yu L, Malkin R (1991) Electron spin echo envelope modulation spectroscopy supports the suggested coordination of two histidine ligands to the Rieske iron–sulfur centers of the cytochrome b6f complex on spinach and the cytochrome bc1 complexes of Rhodospirillum rubrum, Rhodobacter sphaeroides R-26, and bovine heart mitochondria. Biochemistry 30(7):1892–1901PubMedCrossRefGoogle Scholar
  8. Brown E, Friemann R, Karlsson A, Parales J, Couture M, Eltis L, Ramaswamy S (2008) Determining Rieske cluster reduction potentials. J Biol Inorg Chem 13(8):1301–1313PubMedCrossRefGoogle Scholar
  9. Cammack R, Gay E, Shergill JK (1999) Studies of hyperfine interactions in 2Fe–2S proteins by EPR and double resonance spectroscopy. Coord Chem Rev 192:1003–1022CrossRefGoogle Scholar
  10. Chatterjee R, Milikisiyants S, Lakshmi KV (2012) Two-dimensional N-14 HYSCORE spectroscopy of the coordination geometry of ligands in dimanganese di-mu-oxo mimics of the oxygen evolving complex of photosystem II. Phys Chem Chem Phys 14(19):7090–7097CrossRefGoogle Scholar
  11. Cohen RO, Nixon PJ, Diner BA (2007) Participation of the C-terminal region of the D1-polypeptide in the first steps in the assembly of the Mn4Ca cluster of photosystem II. J Biol Chem 282(10):7209–7218PubMedCrossRefGoogle Scholar
  12. Cox N, Rapatskiy L, Su JH, Pantazis DA, Sugiura M, Kulik L, Dorlet P, Rutherford AW, Neese F, Boussac A, Lubitz W, Messinger J (2011) Effect of Ca2 +/Sr2 + substitution on the electronic structure of the oxygen-evolving complex of photosystem II: a combined multifrequency EPR, Mn-55-ENDOR, and DFT study of the S-2 state. J Am Chem Soc 133(10):3635–3648PubMedCrossRefGoogle Scholar
  13. Cox N, Retegan M, Neese F, Pantazis DA, Boussac A, Lubitz W (2014) Electronic structure of the oxygen-evolving complex in photosystem II prior to O–O bond formation. Science 345(6198):804–808PubMedCrossRefGoogle Scholar
  14. DeRose VJ, Yachandra VK, McDermott AE, Britt RD, Sauer K, Klein MP (1991) Nitrogen ligation to manganese in the photosynthetic oxygen-evolving complex: continuous-wave and pulsed EPR studies of photosystem II particles containing nitrogen-14 or nitrogen-15. Biochemistry 30(5):1335–1341PubMedCrossRefGoogle Scholar
  15. Dicus MM, Conlan A, Nechushtai R, Jennings PA, Paddock ML, Britt RD, Stoll S (2010) Binding of histidine in the (Cys)(3)(His)(1)-coordinated 2Fe–2S cluster of human mitoNEET. J Am Chem Soc 132(6):2037–2049PubMedCentralPubMedCrossRefGoogle Scholar
  16. Dikanov SA, Tsvetkov YD (1992) Electron Spin Echo Envelope Modulation (ESEEM) spectroscopy. CRC Press, Boca RatonGoogle Scholar
  17. Dikanov SA, Xun LY, Karpiel AB, Tyryshkin AM, Bowman MK (1996) Orientationally-selected two-dimensional ESEEM spectroscopy of the Rieske-type iron–sulfur cluster in 2,4,5-trichlorophenoxyacetate monooxygenase from Burkholderia cepacia AC1100. J Am Chem Soc 118(35):8408–8416CrossRefGoogle Scholar
  18. Dikanov SA, Shubin AA, Kounosu A, Iwasaki T, Samoilova RI (2004) A comparative, two-dimensional N-14 ESEEM characterization of reduced 2Fe–2S clusters in hyperthermophilic archaeal high- and low-potential Rieske-type proteins. J Biol Inorg Chem 9(6):753–767PubMedCrossRefGoogle Scholar
  19. Dikanov SA, Kolling DRJ, Endeward B, Samoilova RI, Prisner TF, Nair SK, Crofts AR (2006) Identification of hydrogen bonds to the Rieske cluster through the weakly coupled nitrogens detected by electron spin echo envelope modulation spectroscopy. J Biol Chem 281(37):27416–27425PubMedCrossRefGoogle Scholar
  20. Dunham WR, Bearden AJ, Salmeen IT, Palmer G, Sands RH, Ormejohn Wh, Beinert H (1971) 2-Iron ferredoxins in spinach, parsley, pig adrenal cortex, Azotobacter vinelandii, and Clostridium pasteurianum—studies by magnetic field Mossbauer spectroscopy. Biochim Biophys Acta 253(1):134–152PubMedCrossRefGoogle Scholar
  21. Dzyaloshinsky I (1958) A thermodynamic theory of weak ferromagnetism of antiferromagnetics. J Phys Chem Solids 4(4):241–255CrossRefGoogle Scholar
  22. Fee JA, Findling KL, Yoshida T, Hille R, Tarr GE, Hearshen DO, Dunham WR, Day EP, Kent TA, Munck E (1984) Purification and characterization of the Rieske iron–sulfur protein from Thermus thermophilus—evidence for a 2Fe–2S cluster having non-cysteine ligands. J Biol Chem 259(1):124–133PubMedGoogle Scholar
  23. Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303(5665):1831–1838PubMedCrossRefGoogle Scholar
  24. Fiege R, Zweygart W, Bittl R, Adir N, Renger G, Lubitz W (1996) EPR and ENDOR studies of the water oxidizing complex of photosystem II. Photosynth Res 48(1–2):227–237PubMedCrossRefGoogle Scholar
  25. Frey PA, Hegeman AD, Ruzicka FJ (2008) The radical SAM superfamily. Crit Rev Biochem Mol Biol 43(1):63–88PubMedCrossRefGoogle Scholar
  26. Ghirardi ML, Lutton TW, Seibert M (1998) Effects of carboxyl amino acid modification on the properties of the high-affinity, manganese-binding site in photosystem II. Biochemistry 37(39):13559–13566PubMedCrossRefGoogle Scholar
  27. Gibson JF, Hall DO, Thornley JH, Whatley FR (1966) The iron complex in spinach ferredoxin. Proc Natl Acad Sci USA 56(3):987–990PubMedCentralPubMedCrossRefGoogle Scholar
  28. Gurbiel RJ, Batie CJ, Sivaraja M, True AE, Fee JA, Hoffman BM, Ballou DP (1989) Electron nuclear double resonance spectroscopy of 15N-enriched phthalate dioxygenase from Pseudomonas cepacia proves that 2 histidines are coordinated to the [2Fe–2S] Rieske-type clusters. Biochemistry 28(11):4861–4871PubMedCrossRefGoogle Scholar
  29. Gurbiel RJ, Ohnishi T, Robertson DE, Daldal F, Hoffman BM (1991) Q-Band ENDOR spectra of the Rieske protein from Rhodobacter capsulatus ubiquinol cytochrome-C oxidoreductase show 2 histidines coordinated to the 2Fe–2S cluster. Biochemistry 30(49):11579–11584PubMedCrossRefGoogle Scholar
  30. Gurbiel RJ, Doan PE, Gassner GT, Macke TJ, Case DA, Ohnishi T, Fee JA, Ballou DP, Hoffman BM (1996) Active site structure of Rieske-type proteins: electron nuclear double resonance studies of isotopically labeled phthalate dioxygenase from Pseudomonas cepacia and Rieske protein from Rhodobacter capsulatus and molecular modeling studies of a Rieske center. Biochemistry 35(24):7834–7845PubMedCrossRefGoogle Scholar
  31. Guskov A, Kern J, Gabdulkhakov A, Broser M, Zouni A, Saenger W (2009) Cyanobacterial photosystem II at 2.9-angstrom resolution and the role of quinones, lipids, channels and chloride. Nat Struct Mol Biol 16(3):334–342PubMedCrossRefGoogle Scholar
  32. Hagen WR, Silva PJ, Amorim MA, Hagedoorn PL, Wassink H, Haaker H, Robb FT (2000) Novel structure and redox chemistry of the prosthetic groups of the iron–sulfur flavoprotein sulfide dehydrogenase from Pyrococcus furiosus; evidence for a 2Fe–2S cluster with Asp(Cys)(3) ligands. J Biol Inorg Chem 5(4):527–534PubMedCrossRefGoogle Scholar
  33. Hofer P, Grupp A, Nebenfuhr H, Mehring M (1986) Hyperfine sublevel correlation (HYSCORE) spectroscopy—a 2D electron-spin-resonance investigation of the squaric acid radical. Chem Phys Lett 132(3):279–282CrossRefGoogle Scholar
  34. Holden HM, Jacobson BL, Hurley JK, Tollin G, Oh B-H, Skjeldal L, Chae YK, Cheng H, Xia B, Markley JL (1994) Structure–function studies of [2Fe–2S] ferredoxins. J Bioenerg Biomembr 26(1):67–88PubMedCrossRefGoogle Scholar
  35. Hou X, Liu R, Ross S, Smart EJ, Zhu H, Gong W (2007) Crystallographic studies of human MitoNEET. J Biol Chem 282(46):33242–33246PubMedCrossRefGoogle Scholar
  36. Hunsicker-Wang LM, Heine A, Chen Y, Luna EP, Todaro T, Zhang YM, Williams PA, McRee DE, Hirst J, Stout CD, Fee JA (2003) High-resolution structure of the soluble, respiratory-type Rieske protein from Thermus thermophilus: analysis and comparison. Biochemistry 42(24):7303–7317PubMedCrossRefGoogle Scholar
  37. Iwasaki T, Kounosu A, Kolling DRJ, Crofts AR, Dikanov SA, Jin A, Imai T, Urushiyama A (2004) Characterization of the pH-dependent resonance Raman transitions of archaeal and bacterial Rieske 2Fe–2S proteins. J Am Chem Soc 126(15):4788–4789PubMedCrossRefGoogle Scholar
  38. Iwasaki T, Kounosu A, Kolling DRJ, Lhee S, Crofts AR, Dikanov SA, Uchiyama T, Kumasaka T, Ishikawa H, Kono M, Imai T, Urushiyama A (2006a) Resonance Raman characterization of archaeal and bacterial Rieske protein variants with modified hydrogen bond network around the 2Fe–2S center. Protein Sci 15(8):2019–2024PubMedCentralPubMedCrossRefGoogle Scholar
  39. Iwasaki T, Kounosu A, Samoilova RI, Dikanov SA (2006b) 15 N HYSCORE characterization of the fully deprotonated, reduced form of the archaeal rieske [2Fe–2S] center. J Am Chem Soc 128(7):2170–2171PubMedCrossRefGoogle Scholar
  40. Iwasaki T, Samoilova RI, Kounosu A, Ohmori D, Dikanov SA (2009) Continuous-wave and pulsed EPR characterization of the [2Fe–2S](Cys)3(His)1 cluster in rat MitoNEET. J Am Chem Soc 131(38):13659–13667PubMedCentralPubMedCrossRefGoogle Scholar
  41. Kamiya N, Shen JR (2003) Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7-angstrom resolution. Proc Natl Acad Sci USA 100(1):98–103PubMedCentralPubMedCrossRefGoogle Scholar
  42. Kent TA, Huynh BH, Munck E (1980) Iron-sulfur proteins—spin-coupling model for 3-iron clusters. Proc Natl Acad Sci USA 77(11):6574–6576PubMedCentralPubMedCrossRefGoogle Scholar
  43. Kent TA, Emptage MH, Merkle H, Kennedy MC, Beinert H, Munck E (1985) Mossbauer studies of aconitase-substrate and inhibitor binding, reaction intermediates, and hyperfine interactions of reduced Fe-3 and Fe-4 clusters. J Biol Chem 260(11):6871–6881PubMedGoogle Scholar
  44. Kevan L, Kispert LD (1976) Electron spin double resonance spectroscopy. Wiley, New YorkGoogle Scholar
  45. Khangulov S, Sivaraja M, Barynin VV, Dismukes GC (1993) The dimanganese(III,IV) oxidation-state of catalase from Thermus thermophilus—electron nuclear double-resonance analysis of water and protein ligands in the active-site. Biochemistry 32(18):4912–4924PubMedCrossRefGoogle Scholar
  46. Krebs C, Broderick WE, Henshaw TF, Broderick JB, Huynh BH (2002) Coordination of adenosylmethionine to a unique iron site of the 4Fe–4S of pyruvate formate-lyase activating enzyme: a Mossbauer spectroscopic study. J Am Chem Soc 124(6):912–913PubMedCrossRefGoogle Scholar
  47. Kuila D, Fee JA, Schoonover JR, Woodruff WH, Batie CJ, Ballou DP (1987) Resonance Raman-spectra of the 2Fe–2S clusters of the Rieske protein from thermus and phthalate dioxygenase from Pseudomonas. J Am Chem Soc 109(5):1559–1561CrossRefGoogle Scholar
  48. Kulik LV, Epel B, Lubitz W, Messinger J (2007) Electronic structure of the Mn4OxCa cluster in the S0 and S2 States of the oxygen-evolving complex of photosystem II based on pulse 55Mn-ENDOR and EPR spectroscopy. J Am Chem Soc 129(44):13421–13435PubMedCrossRefGoogle Scholar
  49. Link TA (1999) The structures of Rieske and Rieske-type proteins. Adv Inorg Chem 47:83–157CrossRefGoogle Scholar
  50. Lohmiller T, Krewald V, Navarro MP, Retegan M, Rapatskiy L, Nowaczyk MM, Boussac A, Neese F, Lubitz W, Pantazis DA, Cox N (2014) Structure, ligands and substrate coordination of the oxygen-evolving complex of photosystem II in the S2 state: a combined EPR and DFT study. Phys Chem Chem Phys 16(24):11877–11892PubMedCrossRefGoogle Scholar
  51. Loll B, Kern J, Saenger W, Zouni A, Biesiadka J (2005) Towards complete cofactor arrangement in the 3.0 angstrom resolution structure of photosystem II. Nature 438(7070):1040–1044PubMedCrossRefGoogle Scholar
  52. Manchanda R, Brudvig GW, Crabtree RH (1995) High-valent oxomanganese clusters: structural and mechanistic work relevant to the oxygen-evolving center in photosystem II. Coord Chem Rev 144:1–38CrossRefGoogle Scholar
  53. McConnell IL, Grigoryants VM, Scholes CP, Myers WK, Chen P-Y, Whittaker JW, Brudvig GW (2012) EPR-ENDOR characterization of (O-17, H-1, H-2) water in manganese catalase and its relevance to the oxygen-evolving complex of photosystem II. J Am Chem Soc 134(3):1504–1512PubMedCentralPubMedCrossRefGoogle Scholar
  54. Mitou G, Higgins C, Wittung-Stafshede P, Conover RC, Smith AD, Johnson MK, Gaillard J, Stubna A, Münck E, Meyer J (2003) An ISC-type extremely thermostable [2Fe–2S] ferredoxin from Aquifex aeolicus. Biochemical, spectroscopic, and unfolding studies. Biochemistry 42(5):1354–1364PubMedCrossRefGoogle Scholar
  55. Moriya T (1960) Anisotropic superexchange interaction and weak ferromagnetism. Phys Rev 120(1):91–98CrossRefGoogle Scholar
  56. Morton JR, Preston KF (1978) Atomic parameters for paramagnetic resonance data. J Magn Reson 30(3):577–582Google Scholar
  57. Mullins CS, Pecoraro VL (2008) Reflections on small molecule manganese models that seek to mimic photosynthetic water oxidation chemistry. Coord Chem Rev 252(3–4):416–443PubMedCentralPubMedCrossRefGoogle Scholar
  58. Navarro MP, Ames WM, Nilsson H, Lohmiller T, Pantazis DA, Rapatskiy L, Nowaczyk MM, Neese F, Boussac A, Messinger J, Lubitz W, Cox N (2013) Ammonia binding to the oxygen-evolving complex of photosystem II identifies the solvent-exchangeable oxygen bridge (mu-oxo) of the manganese tetramer. Proc Natl Acad Sci USA 110(39):15561–15566CrossRefGoogle Scholar
  59. Paddock ML, Wiley SE, Axelrod HL, Cohen AE, Roy M, Abresch EC, Capraro D, Murphy AN, Nechushtai R, Dixon JE, Jennings PA (2007) MitoNEET is a uniquely folded 2Fe–2S outer mitochondrial membrane protein stabilized by pioglitazone. Proc Natl Acad Sci USA 104(36):14342–14347PubMedCentralPubMedCrossRefGoogle Scholar
  60. Palmer G, Dunham WR, Fee JA, Sands RH, Iizuka T, Yonetani T (1971) Magnetic susceptibility of spinach ferredoxin from 77–250 degrees K—measurement of antiferromagnetic coupling between 2 iron atoms. Biochim Biophys Acta 245(1):201–207PubMedCrossRefGoogle Scholar
  61. Peloquin JM, Campbell KA, Randall DW, Evanchik MA, Pecoraro VL, Armstrong WH, Britt RD (2000) 55Mn ENDOR of the S2-state multiline EPR signal of photosystem II: implications on the structure of the tetranuclear Mn cluster. J Am Chem Soc 122(44):10926–10942CrossRefGoogle Scholar
  62. Randall DW (1998) Pulsed EPR studies of tyrosine radicals and manganese complexes: insights into photosynthetic oxygen evolution. PhD Thesis, University of California-DavisGoogle Scholar
  63. Randall DW, Gelasco A, Caudle MT, Pecoraro VL, Britt RD (1997) ESE-ENDOR and ESEEM characterization of water and methanol ligation to a dinuclear Mn(III)Mn(IV) complex. J Am Chem Soc 119(19):4481–4491CrossRefGoogle Scholar
  64. Rapatskiy L, Cox N, Savitsky A, Ames WM, Sander J, Nowaczyk MM, Roegner M, Boussac A, Neese F, Messinger J, Lubitz W (2012) Detection of the water-binding sites of the oxygen-evolving complex of photosystem II using W-Band O-17 electron-electron double resonance-detected NMR spectroscopy. J Am Chem Soc 134(40):16619–16634PubMedCrossRefGoogle Scholar
  65. Rieske JS, MacLennan DH, Coleman R (1964) Isolation and properties of an iron-protein from the (reduced coenzyme Q)-cytochrome C reductase complex of the respiratory chain. Biochem Biophys Res Commun 15(4):338–344CrossRefGoogle Scholar
  66. Samoilova RI, Kolling D, Uzawa T, Iwasaki T, Crofts AR, Dikanov SA (2002) The interaction of the Rieske iron–sulfur protein with occupants of the Q(o)-site of the bc(1) complex, probed by electron spin echo envelope modulation. J Biol Chem 277(7):4605–4608PubMedCrossRefGoogle Scholar
  67. Schweiger A, Jeschke G (2001) Principles of pulse electron paramagnetic resonance. Oxford University Press, New YorkGoogle Scholar
  68. Shergill JK, Cammack R (1994) ESEEM and ENDOR studies of the Rieske iron–sulfur protein in bovine heart mitochondrial-membranes. Biochim Biophys Acta 1185(1):35–42PubMedCrossRefGoogle Scholar
  69. Shimomura Y, Wada K, Fukuyama K, Takahashi Y (2008) The asymmetric trimeric architecture of 2Fe–2S IscU: implications for its scaffolding during iron–sulfur cluster biosynthesis. J Mol Biol 383(1):133–143PubMedCrossRefGoogle Scholar
  70. Sinnecker S, Neese F, Noodleman L, Lubitz W (2004) Calculating the electron paramagnetic resonance parameters of exchange coupled transition metal complexes using broken symmetry density functional theory: application to a MnIII/MnIV model compound. J Am Chem Soc 126(8):2613–2622PubMedCrossRefGoogle Scholar
  71. Sinnecker S, Neese F, Lubitz W (2005) Dimanganese catalase-spectroscopic parameters from broken-symmetry density functional theory of the superoxidized MnIII/MnIV state. J Biol Inorg Chem 10(3):231–238PubMedCrossRefGoogle Scholar
  72. Stemmler TL, Sturgeon BE, Randall DW, Britt RD, Penner-Hahn JE (1997) Spectroscopic characterization of inhibitor interactions with the Mn(III)/Mn(IV) core in Lactobacillus plantarum manganese catalase. J Am Chem Soc 119(39):9215–9225CrossRefGoogle Scholar
  73. Stich TA, Whittaker JW, Britt RD (2010) Multifrequency EPR studies of manganese catalases provide a complete description of proteinaceous nitrogen coordination. J Phys Chem B 114(45):14178–14188PubMedCentralPubMedCrossRefGoogle Scholar
  74. Stich TA, Yeagle GJ, Service RJ, Debus RJ, Britt RD (2011) Ligation of D1-His332 and D1-Asp170 to the manganese cluster of photosystem II from Synechocystis assessed by multifrequency pulse EPR spectroscopy. Biochemistry 50(34):7390–7404PubMedCentralPubMedCrossRefGoogle Scholar
  75. Stull JA, Stich TA, Service RJ, Debus RJ, Mandal SK, Armstrong WH, Britt RD (2010) C-13 ENDOR reveals that the D1 polypeptide C-terminus is directly bound to Mn in the photosystem II oxygen evolving complex. J Am Chem Soc 132(2):446–447PubMedCentralPubMedCrossRefGoogle Scholar
  76. Tan XL, Gultneh Y, Sarneski JE, Scholes CP (1991) EPR-ENDOR of the electronic structure from 2 nitrogenously ligated bis(m-oxo)MnIIIMnIV model complexes spectroscopically relevant to the multi-manganese center of photosytem II. J Am Chem Soc 113(21):7853–7858CrossRefGoogle Scholar
  77. Tiago de Oliveira F, Bominaar EL, Hirst J, Fee JA, Münck E (2004) Antisymmetric exchange in [2Fe–2S]1 + clusters: EPR of the Rieske protein from Thermus thermophilus at pH 14. J Am Chem Soc 126(17):5338–5339PubMedCrossRefGoogle Scholar
  78. Tirrell TF, Paddock ML, Conlan AR, Smoll EJ, Nechushtai R, Jennings PA, Kim JE (2009) Resonance Raman studies of the (His)(Cys)3 2Fe–2S cluster of MitoNEET: comparison to the (Cys)4 mutant and implications of the effects of pH on the labile metal center. Biochemistry 48(22):4747–4752PubMedCentralPubMedCrossRefGoogle Scholar
  79. Ullmann M, Noodleman L, Case D (2002) Density functional calculation of pKa values and redox potentials in the bovine Rieske iron–sulfur protein. J Biol Inorg Chem 7(6):632–639PubMedCrossRefGoogle Scholar
  80. Umena Y, Kawakami K, Shen J-R, Kamiya N (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature 473(7345):55–60PubMedCrossRefGoogle Scholar
  81. Usov OM, Grigoryants VM, Tagore R, Brudvig GW, Scholes CP (2007) Hyperfine coupling to the bridging O-17 in the di-mu-oxo core of a Mn-III–Mn-IV model significant to the core electronic structure of the O-2-evolving complex in photosystem II. J Am Chem Soc 129(39):11886–11887PubMedCrossRefGoogle Scholar
  82. Walsby CJ, Hong W, Broderick WE, Cheek J, Ortillo D, Broderick JB, Hoffman BM (2002) Electron-nuclear double resonance spectroscopic evidence that S-adenosylmethionine binds in contact with the catalytically active [4Fe-4S] + cluster of pyruvate formate-lyase activating enzyme. J Am Chem Soc 124(12):3143–3151PubMedCrossRefGoogle Scholar
  83. Werst MM, Kennedy MC, Beinert H, Hoffman BM (1990a) Oxygen-17, proton, and deuterium electron nuclear double resonance characterization of solvent, substrate, and inhibitor binding to the iron–sulfur [4Fe–4S] + cluster of aconitase. Biochemistry 29(46):10526–10532PubMedCrossRefGoogle Scholar
  84. Werst MM, Kennedy MC, Houseman ALP, Beinert H, Hoffman BM (1990b) Characterization of the iron-sulfur [4Fe-4S] + cluster at the active site of aconitase by iron-57, sulfur-33, and nitrogen-14 electron nuclear double resonance spectroscopy. Biochemistry 29(46):10533–10540PubMedCrossRefGoogle Scholar
  85. Wiley SE, Paddock ML, Abresch EC, Gross L, van der Geer P, Nechushtai R, Murphy AN, Jennings PA, Dixon JE (2007) The outer mitochondrial membrane protein mitoNEET contains a novel redox-active 2Fe–2S cluster. J Biol Chem 282(33):23745–23749PubMedCrossRefGoogle Scholar
  86. Yeagle GJ, Gilchrist ML, McCarrick RM, Britt RD (2008) Multifrequency pulsed electron paramagnetic resonance study of the S2 state of the photosystem II manganese cluster. Inorg Chem 47(6):1803–1814PubMedCrossRefGoogle Scholar
  87. Zheng M, Khangulov SV, Dismukes GC, Barynin VV (1994) Electronic structure of dimanganese(II, III) and dimanganese(III, IV) complexes and dimanganese catalase enzyme: a general EPR spectral simulation approach. Inorg Chem 33(2):382–387CrossRefGoogle Scholar
  88. Zouni A, Witt HT, Kern J, Fromme P, Krauss N, Saenger W, Orth P (2001) Crystal structure of photosystem II from Synechococcus elongatus at 3.8 angstrom resolution. Nature 409(6821):739–743PubMedCrossRefGoogle Scholar
  89. Zu YB, Fee JA, Hirst J (2001) Complete thermodynamic characterization of reduction and protonation of the bc(1)-type Rieske 2Fe–2S center of Thermus thermophilus. J Am Chem Soc 123(40):9906–9907PubMedCrossRefGoogle Scholar
  90. Zuris JA, Harir Y, Conlan AR, Shvartsman M, Michaeli D, Tamir S, Paddock ML, Onuchic JN, Mittler R, Cabantchik ZI, Jennings PA, Nechushtai R (2011) Facile transfer of 2Fe–2S clusters from the diabetes drug target mitoNEET to an apo-acceptor protein. Proc Natl Acad Sci USA 108(32):13047–13052PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Paul H. Oyala
    • 1
  • Troy A. Stich
    • 1
  • R. David Britt
    • 1
  1. 1.Department of ChemistryUniversity of California-DavisDavisUSA

Personalised recommendations