Mutual Control of Axial and Equatorial Ligands: Model Studies with [Ni]-Bacteriochlorophyll-a Roie Yerushalmi, ²,‡ Dror Noy, ²,§ Kim K. Baldridge, | and Avigdor Scherz* ,‡ Contribution from the Department of Plant Sciences, The Weizmann Institute of Science, 76100 RehoVot, Israel, and Department of Chemistry, UniVersity of California, San Diego, California Received September 4, 2001 Abstract: Modification of the metal’s electronic environment by ligand association and dissociation in metalloenzymes is considered cardinal to their catalytic activity. We have recently presented a novel system that utilizes the bacteriochlorophyll (BChl) macrocycle as a ligand and reporter. This system allows for charge mobilization in the equatorial plane and experimental estimate of changes in the electronic charge density around the metal with no modification of the metal’s chemical environment. The unique spectroscopy, electrochemistry and coordination chemistry of [Ni]-bacteriochlorophyll ([Ni]-BChl) enable us to follow directly fine details and steps involved in the function of the metal redox center. This approach is utilized here whereby electro-chemical reduction of [Ni]-BChl to the monoanion [Ni]-BChl - results in reversible dissociation of biologically relevant axial ligands. Similar ligand dissociation was previously detected upon photoexcitation of [Ni]-BChl (Musewald, C.; Hartwich, G.; Lossau, H.; Gilch, P.; Pollinger-Dammer, F.; Scheer, H.; Michel- Beyerle, M. E. J. Phys. Chem. B 1999, 103, 7055-7060 and Noy, D.; Yerushalmi, R.; Brumfeld, V.; Ashur, I.; Baldridge, K. K.; Scheer, H.; Scherz, A. J. Am. Chem. Soc. 2000, 122, 3937-3944). The electrochemical measurements and quantum mechanical (QM) calculations performed here for the neutral, singly reduced, monoligated, and singly reduced, monoligated [Ni]-BChl suggest the following: (a) Electroreduction, although resulting in a π anion [Ni]-BChl - radical, causes electron density migration to the [Ni]-BChl core. (b) Reduction of nonligated [Ni]-BChl does not change the macrocycle conformation, whereas axial ligation results in a dramatic expansion of the metal core and a flattening of the highly ruffled macrocycle conformation. (c) In both the monoanion and singly excited [Ni]-BChl ([Ni]-BChl*), the frontier singly occupied molecular orbital (SOMO) has a small but nonnegligible metal character. Finally, (d) computationally, we found that a reduction of [Ni]-BChl . imidazole results in a weaker metal-axial ligand bond. Yet, it remains weakly bound in the gas phase. The experimentally observed ligand dissociation is accounted for computationally when solvation is considered. On the basis of the experimental observations and QM calculations, we propose a mechanism whereby alterations in the equatorial π system and modulation of σ bonding between the axial ligands and the metal core are mutually correlated. Such a mechanism highlights the dynamic role of axial ligands in regulating the activity of metal centers such as factor F430 (F430), a nickel-based coenzyme that is essential in methanogenic archea. Introduction The catalytic action of biological metal centers frequently involves changing the coordination sphere of the metal, by breaking and forming coordinative bonds with protein residues, substrates, or other small molecules (e.g., CO, O 2 , NO, or water). Presumably, the dynamical effect of this process modulates the electronic properties and coordination chemistry of the metal and thereby its activity throughout the catalytic cycle. 3-6 The coordination properties of a particular metal in different electronic states may be utilized for triggering substrate binding and release as well as to mediate protein conformational changes. 6-12 * To whom correspondence should be addressed. E-mail: avigdor. scherz@weizmann.ac.il. ² In partial fulfillment of Ph.D. Thesis. ‡ Weizmann Institute of Science. § Present address: Biochemistry and Biophysics Dept., University of Pennsylvania. | University of California. (1) Musewald, C.; Hartwich, G.; Lossau, H.; Gilch, P.; Pollinger-Dammer, F.; Scheer, H.; Michel-Beyerle, M. E. J. Phys. Chem. B 1999, 103, 7055- 7060. (2) Noy, D.; Yerushalmi, R.; Brumfeld, V.; Ashur, I.; Baldridge, K. K.; Scheer, H.; Scherz, A. J. Am. Chem. Soc. 2000, 122, 3937-3944. (3) Hall, J. F.; Kanbi, L. D.; Harvey, I.; Murphy, L. M.; Hasnain, S. S. Biochemistry 1998, 37, 11451-11458. (4) Hall, J. F.; Kanbi, L. D.; Strange, R. W.; Hasnain, S. S. Biochemistry 1999, 38, 12675-12680. (5) Malmstrom, B. G.; Wittung-Stafshede, P. Coord. Chem. ReV. 1999, 186, 127-140. (6) Sharp, R. E.; Chapman, S. K. Biochim. Biophys. Acta 1999, 1432, 143- 158. (7) Poulos, T. L. Nat. Struct. Biol. 1996, 3, 401-403. (8) Williams, P. A.; Fulop, V.; Garman, E. F.; Saunders, N. F. W.; Ferguson, S. J.; Hajdu, J. Nature 1997, 389, 406-412. (9) Pascher, T.; Chesick, J. P.; Winkler, J. R.; Gray, H. B. Science 1996, 271, 1558-1560. (10) Wittung-Stafshede, P.; Lee, J. C.; Winkler, J. R.; Gray, H. B. Proc. Natl. Acad. Sci. U.S.A. 1999, 96, 6587-6590. (11) Wittung, P.; Malmstrom, B. G. Febs Lett. 1996, 388, 47-49. Published on Web 06/19/2002 8406 9 J. AM. CHEM. SOC. 2002, 124, 8406-8415 10.1021/ja0121078 CCC: $22.00 © 2002 American Chemical Society