Abstract
Mössbauer spectroscopy is very important for the characterization of iron sulfur clusters in biological and synthetic molecules. The electric and magnetic hyperfine parameters obtained for 57Fe provide valuable information about the electronic structure of the different iron sites occurring in Fe:S clusters. Although known since more than four decades, research in this field is very active, revealing unexpected functions, structures and redox states. In this overview, new aspects of double exchange and vibronic coupling in a structurally well-characterized two-iron model compound are discussed, the electronic structure of extremely reduced clusters with all iron in ferrous or even in iron(I) state is elucidated, and an exciting new type of cubane cluster occurring in oxygen-insensitive hydrogenases is presented. The latter cluster involves structural changes during function and it supports more than one redox transition, which may be essential for oxygen protection of the enzymes.
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Beinert, H., Holm, R.H., Münck, E.: Iron-sulfur clusters: nature’s modular, multipurpose structures. Science 277, 653–659 (1997)
Beinert, H.: Iron-sulfur proteins: ancient structures, still full of surprises. J. Biol. Inorg. Chem. 5(1), 2–15 (2000)
Rees, D.C.: Great metallclusters in enzymology. Ann. Rev. Biochem. 71, 221–246 (2002)
Rees, D.C., Howard, J.B.: The interface between the biological and inorganic worlds: iron-sulfur metalloclusters. Science 300(5621), 929–931 (2003). doi:10.1126/science.1083075
Huber, C., Wächtershäuser, G.: Activated acetic acid by carbon fixation on (Fe,Ni)S under primordial conditions. Science 276(5310), 245–247 (1997). doi:10.1126/science.276.5310.245
Rao, V.P., Holm, R.H.: Synthetic analogues of the active sites of iron-sulfur proteins. Chem. Rev. 104(2), 527–560 (2003). doi:10.1021/cr020615+
Johnson, D.C., Dean, D.R., Smith, A.D., Johnson, M.K.: Structure, function, and formation of biological iron-sulfur clusters. Ann. Rev. Biochem. 74(1), 247–281 (2005). doi:10.1146/annurev.biochem.74.082803.133518
Dos Santos, P.C., Dean, D.R.: Bioinorganic chemistry—electrons in Fe-S protein assembly. Nat. Chem. Biol. 6(10), 700–701 (2010). doi:10.1038/nchembio.438
Lill, R.: Function and biogenesis of iron-sulphur proteins. Nature 460(7257), 831–838 (2009)
Sheftel, A., Stehling, O., Lill, R.: Iron-sulfur proteins in health and disease. Trends Endocrinol. Metab. 21(5), 302–314 (2010)
Solomon, E.I., Xie, X., Dey, A.: Mixed valent sites in biological electron transfer. Chem. Soc. Rev. 37(4), 623–638 (2008)
Zener, C.: Interaction between the d-shells in the transition metals. 2. Ferromagnetic compounds of manganese with Perovskite structure. Phys. Rev. 82(3), 403–405 (1951)
Anderson, P.W., Hasegawa, H.: Considerations on double exchange. Phys. Rev. 100(2), 675–681 (1955)
Papaefthymiou, V., Girerd, J.-J., Moura, I., Moura, J.J.G., Münck, E.: Mössbauer study of D. gigas ferredoxin II and spin coupling model for the Fe3S4 cluster with valence delocalization. J. Am. Chem. Soc. 109(15), 4703–4710 (1987)
Noodleman, L., Case, D.A., Mouesca, J.M., Lamotte, B.: Valence electron delocalization in polynuclear iron-sulfur clusters. J. Biol. Inorg. Chem. 1(2), 177–182 (1996)
Schulz, C.E., Debrunner, P.G.: Rubredoxin. J. Phys. Coll. 37(C6), 153–158 (1976)
Münck, E., Debrunner, P.G., Tsibris, J.C.M., Gunsalus, I.C.: Mössbauer parameters of putidaredoxin and its selenium analog. Biochemistry 11(5), 855–863 (1972)
Kent, T.A., Huynh, B.h., Münck, E.: Iron-sulfur proteins: spin-coupling model for three-iron cluster. Proc. Natl. Acad. Sci. U. S. A. 77(11), 6574–6576 (1980)
Middleton, P., Dickson, D.P.E., Johnson, C.E., Rush, J.D.: Interpretation of the Mössbauer spectra of Four-Iron Ferredoxin from Bacillus stearothermophilis. Eur. J. Biochem. 88, 135–141 (1978)
Middleton, P., Dickson, D.P.E., Charles, E.J., Rush, J.D.: Interpretation of the Mössbauer spectra of the high-potential iron protein from chromatium. Eur. J. Biochem. 104(1), 289–296 (1980)
Gütlich, P., Bill, E., Trautwein, A.X.: Mössbauer spectroscopy and transition metal chemistry. Springer, Berlin Heidelberg (2011)
Cammack, R.: Iron-sulfur clusters in enzymes: themes and variations. In: Cammack, R. (ed.) Iron-Sulfur Proteins, vol. 38. Advances in Inorganic Chemistry, pp. 281–323. Academic Press, San Diego (1992)
Schünemann, V., Winkler, H.: Structure and dynamics of biomolecules studied by Mössbauer spectroscopy. Rep. Prog. Phys. 63(3), 263–353 (2000)
Mouesca, J.-M., Lamotte, B.: Iron-sulfur clusters and their electronic and magnetic properties. Coord. Chem. Rev. 178–180, 1573–1614 (1998)
Albers, A., Demeshko, S., Dechert, S., Bill, E., Bothe, E., Meyer, F.: The complete characterization of a reduced biomimetic [2Fe-2S] cluster. Angew. Chem. Int. Ed. 50(39), 9191–9194 (2011)
Ballmann, J., Albers, A., Demeshko, S., Dechert, S., Bill, E., Bothe, E., Ryde, U., Meyer, F.: A synthetic analogue of rieske-type [2Fe-2S] clusters. Angew. Chem. Int. Ed. 47(49), 9537–9541 (2008)
Mascharak, P.K., Papaefthymiou, G.C., Frankel, R.B., Holm, R.H.: Evidence for the localized iron(III)/iron(II) oxidation state configuration as an intrinsic property of [Fe2S2(SR)4]3- clusters. J. Am. Chem. Soc. 103(20), 6110–6116 (1981). doi:10.1021/ja00410a021
Beardwood, P., Gibson, J.F.: Iron-sulfur dimers with benzimidazolate-thiolate, -phenolate or bis(benzimidazolate) terminal chelating ligands. Models for Rieske-type proteins. J. Chem. Soc. Dalton Trans. 16, 2457–2466 (1992)
Ding, X.Q., Bill, E., Trautwein, A.X., Winkler, H., Kostikas, A., Papaefthymiou, V., Simpoulos, A., Beardwood, P., Gibson, J.F.: Exchange interactions, charge delocalization and spin relaxation in a mixed-valence diiron complex studied by Mössbauer-spectroscopy. J. Chem. Phys. 99(9), 6421–6428 (1993)
Hoggins, J.T., Steinfink, H.: Empirical bonding relationships in metal-iron-sulfide compounds. Inorg. Chem. 15(7), 1682–1685 (1976)
Piepho, S.B.: Vibronic coupling for calculations of Mixed-Valence Line-Shapes—the interdependence of vibronic and MO effects. J. Am. Chem. Soc. 110(19), 6319–6326 (1988)
Piepho, S.B., Krausz, E.R., Schatz, P.N.: Vibronic coupling for calculation of mixed-valence absorption profiles. J. Am. Chem. Soc. 100(10), 2996–3005 (1978)
Girerd, J.J.: Electron transfer between magnetic ions in mixed valence binuclear systems. J. Chem. Phys. 79, 1766–1775 (1983)
Blondin, G., Girerd, J.-J.: Interplay of electron exchange and electron transfer in metal polynuclear complexes in proteins or chemical models. Chem. Rev. 90, 1359 (1990)
Bominaar, E.L., Borshch, S.A., Girerd, J.-J.: Double-exchange and vibronic coupling in mixed-valence systems. Electronic structure of [Fe4S4]3+ clusters in high-potential iron protein and related models. J. Am. Chem. Soc. 116, 5362–5372 (1994)
Bominaar, E.L., Hu, Z., Münck, E., Girerd, J.-J., Borshch, S.: Double exchange and vibronic coupling in mixed-valence systems. Elelctonic structure of exchange-coupled siroheme-[Fe4S4]2+ chromophore in oxidized E. Coli sulfite reductase. J. Am. Chem. Soc. 117(26), 6976–6989 (1995)
Münck, E., Papaefthymiou, V., Surerus, K.K., Girerd, J.J.: Double exchange in reduced Fe3S3 clusters and novel clusters with MFe3S4 cores. Acs Symposium Series 372, 302–325 (1988)
Orio, M., Mouesca, J.M.: Variation of average g values and effective exchange coupling constants among 2Fe-2S clusters: a density functional theory study of the impact of localization (trapping forces) versus delocalization (double-exchange) as competing factors. Inorg. Chem. 47(12), 5394–5416 (2008). doi:10.1021/ic701730h
Anxolabehere-Mallart, E., Glaser, T., Frank, P., Aliverti, A., Zanetti, G., Hedman, B., Hodgson, K.O., Solomon, E.I.: Sulfur K-edge X-ray absorption spectroscopy of 2Fe-2S ferredoxin: covalency of the oxidized and reduced 2Fe forms and comparison to model complexes. J. Am. Chem. Soc. 123(23), 5444–5452 (2001)
Glaser, T., Rose, K., Shadle, S.E., Hedman, B., Hodgson, K.O., Solomon, E.I.: S K-edge X-ray absorption studies of tetranuclear iron-sulfur clusters: μ-sulfide bonding and its contribution to electron delocalization. J. Am. Chem. Soc. 123(3), 442–454 (2000). doi:10.1021/ja002183v
Angove, H.C., Yoo, S.J., Burgess, B.K., Münck, E.: Mössbauer and EPR evidence for an all-ferrous Fe4S4 cluster with S = 4 in the Fe protein of nitrogenase. J. Am. Chem. Soc. 119(37), 8730–8731 (1997)
Musgrave, K.B., Angove, H.C., Burgess, B.K., Hedman, B., Hodgson, K.O.: All-ferrous titanium(III) citrate reduced Fe protein of nitrogenase: an XAS study of electronic and metrical structure. J. Am. Chem. Soc. 120(21), 5325–5326 (1998)
Angove, H.C., Yoo, S.J., Münck, E., Burgess, B.K.: An all-ferrous state of the Fe protein of nitrogenase—interaction with nucleotides and electron transfer to the MoFe protein. J. Biol. Chem. 273(41), 26330–26337 (1998)
Yoo, S.J., Angove, H.C., Burgess, B.K., Hendrich, M.P., Münck, E.: Mössbauer and integer-spin EPR studies and spin-coupling analysis of the 4Fe–4S (0) cluster of the Fe protein from Azotobacter vinelandii nitrogenase. J. Am. Chem. Soc. 121(11), 2534–2545 (1999)
Angove, H.C., Yoo, S.J., Munck, E., Burgess, B.K.: Role(s) of the P-clusters in nitrogenase catalysis. J. Inorg. Biochem. 74(1–4), 65–65 (1999)
Surerus, K.K., Hendrich, M.P., Christie, P.D., Rottgardt, D., Orme-Johnson, W.H., Münck, E.: Mössbauer and integer-spin EPR of the oxidized P-clusters of nitrogenase—Pox is a non-Kramers system with a nearly degenerate ground doublet. J. Am. Chem. Soc. 114(22), 8579–8590 (1992). doi:10.1021/ja00048a034
Hans, M., Buckel, W., Bill, E.: Spectroscopic evidence for an all-ferrous [4Fe–4S](0) cluster in the superreduced activator of 2-hydroxyglutaryl-CoA dehydratase from Acidaminococcus fermentans. J. Biol. Inorg. Chem. 13(4), 563–574 (2008)
Leggate, E.J., Bill, E., Essigke, T., Ullmann, G.M., Hirst, J.: Formation and characterization of an all-ferrous Rieske cluster and stabilization of the [2Fe–2S]0 core by protonation. Proc. Natl. Acad. Sci. U. S. A. 101(30), 10913–10918 (2004)
Clark, M.M., Stubbert, B.D., Brennessel, W.W., Bill, E., Holland, P.L.: Synthesis, structure, and spectroscopy of an iron(I)-sulfide complex. Inorg. Chem (2011, accepted)
Stoian, S.A., Yu, Y., Smith, J.M., Holland, P.L., Bominaar, E.L., Münck, E.: Mössbauer, electron paramagnetic resonance, and crystallographic characterization of a high-spin Fe(I) diketiminate complex with orbital degeneracy. Inorg. Chem. 44(14), 4915–4922 (2005)
Brugna-Guiral, M., Tron, P., Nitschke, W., Stetter, K.O., Burlat, B., Guigliarelli, B., Bruschi, M., Giudici-Orticoni, M.T.: NiFe hydrogenases from the hyperthermophilic bacterium Aquifex aeolicus: properties, function, and phylogenetics. Extremophiles 7(2), 145–157 (2003). doi:10.1007/s00792-002-0306-3
Pandelia, M.-E., Fourmond, V., Tron-Infossi, P., Lojou, E., Bertrand, P., Leger, C., Giudici-Orticoni, M.-T., Lubitz, W.: Membrane-bound hydrogenase I from the hyperthermophilic bacterium aquifex aeolicus: enzyme activation, redox intermediates and oxygen tolerance. J. Am. Chem. Soc. 132(20), 6991–7004 (2010). doi:10.1021/ja910838d
Fontecilla-Camps, J.C., Volbeda, A., Cavazza, C., Nicolet, Y.: Structure/function relationships of NiFe- and FeFe-hydrogenases. Chem. Rev. 107(10), 4273–4303 (2007). doi:10.1021/cr050195z
Surerus, K.K., Chen, M., Vanderzwaan, J.W., Rusnak, F.M., Kolk, M., Duin, E.C., Albracht, S.P.J., Münck, E.: Further characterization of the spin coupling observed in oxidized hydrogenase from chromatium-vinosum—a Mössbauer and multifrequency EPR study. Biochemistry 33(16), 4980–4993 (1994)
Pandelia, M.-E., Nitschke, W., Infossi, P., Giudici-Orticoni, M.-T., Bill, E., Lubitz, W.: Characterization of a unique FeS cluster in the electron transfer chain of the oxygen tolerant NiFe hydrogenase from Aquifex aeolicus. Proc. Natl. Acad. Sci. 108(15), 6097–6102 (2011). doi:10.1073/pnas.1100610108
Pandelia, M.-E., Nitschke, W., Infossi, P., Giudici-Orticoni, M.-T., Bill, E., Lubitz, W. (2012, to be published)
Shomura, Y., Yoon, K.-S., Nishihara, H., Higuchi, Y.: Structural basis for a [4Fe-3S] cluster in the oxygen-tolerant membrane-bound [NiFe]-hydrogenase. Nature advance online publication (2011). doi:http://www.nature.com/nature/journal/vaop/ncurrent/abs/nature10504.html#supplementary-information
Fritsch, J., Scheerer, P., Frielingsdorf, S., Kroschinsky, S., Friedrich, B., Lenz, O., Spahn, C.M.T.: The crystal structure of an oxygen-tolerant hydrogenase uncovers a novel iron-sulphur centre. Nature advance online publication (2011). doi:http://www.nature.com/nature/journal/vaop/ncurrent/abs/nature10505.html#supplementary-information
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Bill, E. (2013). Iron-sulfur clusters—new features in enzymes and synthetic models. In: Yoshida, Y. (eds) ICAME 2011. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-4762-3_48
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DOI: https://doi.org/10.1007/978-94-007-4762-3_48
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