Introduction to Electron Transfer in Inorganic, Organic, and Biological

1 Introduction to Electron Transfer in Inorganic, Organic, and Downloaded by COLUMBIA UNIV on March 20, 2013 | http://pubs.acs.org Publication Date: May 5, 1991 | doi: 10.1021/ba-1991-0228.ch001

Biological Systems

James R. Bolton , Noboru Mataga , and George McLendon 1

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Photochemistry Unit, Department of Chemistry, University of Western Ontario, London, Ontario N6A 5B7, Canada Department of Chemistry, Faculty of Engineering Science, Osaka University, Toyonaka, Osaka 560 Japan Department of Chemistry, University of Rochester, Rochester, NY 14627

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This chapter provides an overview of the current developments in the field of electron transfer in theory and inorganic, organic, and biological systems. It shows how the various chapters of this volume contribute to the efforts to find common solutions to common problems.

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C U R R E N T I M P O R T A N C E O F E L E C T R O N - T R A N S F E R R E A C T I O N S is

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trated b y the fact that four of the symposia a n d 81 of the papers p r e s e n t e d at the C o n f e r e n c e of the Pacific B a s i n C h e m i c a l Societies i n H a w a i i i n D e c e m b e r 1989, h a d the words " e l e c t r o n transfer" i n the title. T h i s i n t e n s i t y of activity has b e e n b u i l d i n g since the mid-1950s, w h e n the basic e l e m e n t s o f electron-transfer t h e o r y w e r e i n t r o d u c e d b y M a r c u s ( 1 - 5 ) , w i t h later c o n t r i b u t i o n s from H u s h (6), L e v i c h a n d D o g o n a d z e (7, 8), a n d others. R e c e n t progress i n the e l u c i d a t i o n of its m e c h a n i s m s i n various fields of p h o t o c h e m i s t r y a n d photobiology is p a r t l y d u e to r e m a r k a b l e a d vances i n e x p e r i m e n t a l methods such as ultrafast laser spectroscopy (9, 10). T h e s e techniques have made possible m o r e d i r e c t a n d d e t a i l e d observations of electron-transfer processes. A b r i e f r e v i e w of basic electron-transfer theory is p r o v i d e d i n this v o l u m e (11). Interest i n electron-transfer processes can be d i v i d e d into four g e n e r a l 0065-2393/91/0228-0001$06.00/0 © 1991 American Chemical Society

In Electron Transfer in Inorganic, Organic, and Biological Systems; Bolton, J., et al.; Advances in Chemistry; American Chemical Society: Washington, DC, 1991.

Downloaded by COLUMBIA UNIV on March 20, 2013 | http://pubs.acs.org Publication Date: May 5, 1991 | doi: 10.1021/ba-1991-0228.ch001

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areas: t h e o r y , i n o r g a n i c systems, organic systems, a n d b i o l o g i c a l systems. A l t h o u g h there has b e e n considerable i n t e r a c t i o n b e t w e e n t h e o r y a n d a p plications, the t h r e e e x p e r i m e n t a l fields have t e n d e d to d e v e l o p separately, e v e n to the p o i n t o f u s i n g different n o m e n c l a t u r e . T h e k e y purposes o f this v o l u m e are to b r i n g these fields together, to increase interactions a m o n g t h e m , a n d to seek c o m m o n solutions to c o m m o n p r o b l e m s . M u c h of the c u r r e n t interest i n electron-transfer processes stems from the e x c i t i n g advances m a d e i n the past decade i n o u r u n d e r s t a n d i n g o f the p r i m a r y processes i n v o l v e d i n photosynthesis (12). T h e d e t e r m i n a t i o n of the crystal structure o f the reaction c e n t e r p r o t e i n i n p h o t o s y n t h e t i c b a c t e r i a (13, 14), together w i t h the results o f ultrafast laser photolysis a n d r e l a t e d investigations o n p h o t o i n d u c e d electron-transfer processes i n these systems, has p r o v i d e d not o n l y a v i v i d p i c t u r e of h o w p h o t o i n d u c e d e l e c t r o n transfer occurs i n photosynthesis, but also an insight i n t o h o w n a t u r e has o p t i m i z e d the efficiency o f the system. A t t e n t i o n is n o w shifting to the reaction centers of g r e e n - p l a n t systems, p a r t i c u l a r l y P h o t o s y s t e m I (15). E l e g a n t w o r k o n natural photosynthesis has s t i m u l a t e d studies o f m o d e l d o n o r - a c c e p t o r m o l e c u l e s , j o i n e d b y a spacer or d i r e c t l y b y a single b o n d ( 2 6 - 1 8 ) , as w e l l as o f m o d i f i e d p r o t e i n systems. T h e s e studies a t t e m p t e d to define the i m p o r t a n t factors that c o n t r o l e l e c t r o n transfer f r o m a d o n o r to an acceptor. O n the o t h e r h a n d , studies o f the electron-transfer m e c h a n i s m i n the fluorescence q u e n c h i n g reaction b e t w e e n u n c o m b i n e d d o n o r a n d acceptor systems, i n c l u d i n g various dyes a n d aromatic m o l e c u l e s as fluorescers a n d various organic a n d inorganic molecules as q u e n c h e r s i n s o l u t i o n , have a l o n g h i s t o r y d a t i n g from the 1930s (19). T h i s subject has b e e n one o f the most i m p o r t a n t aspects i n e l u c i d a t i o n of the mechanisms u n d e r l y i n g p h o t o i n d u c e d e l e c t r o n transfer i n solution. N e v e r t h e l e s s , t h e r e are still s o m e p r o b l e m s , such as the energy gap d e p e n d e n c e o f the electron-transfer rate constant i n the fluorescence q u e n c h i n g r e a c t i o n , that cannot b e i n t e r p r e t e d satisfactorily o n the basis of standard electron-transfer theories (10, 20). E l e c t r o n - t r a n s f e r theory has c o n t i n u e d to d e v e l o p since the p i o n e e r i n g w o r k m e n t i o n e d i n the foregoing discussion. C u r r e n t interest is focused o n e x p l a i n i n g the d e p e n d e n c e of f u n c t i o n a n d dynamics o n the structure o f the r e a c t i o n c e n t e r p r o t e i n a n d o n e x a m i n i n g the i n t e r p l a y b e t w e e n e l e c t r o n i c a n d n u c l e a r factors (21). T h i s i n f o r m a t i o n can p r o v i d e a b e t t e r u n d e r s t a n d i n g o f the role o f e l e c t r o n t u n n e l i n g a n d of solvation (20) a n d solvent d y n a m i c s (22, 23). T h e s e electron-transfer factors have b e e n e x a m i n e d i n m a n y systems, i n c l u d i n g solutions, m o l e c u l a r assemblies, a n d various m o d e l systems. M o s t o f the m o d e l systems, w i t h d o n o r a n d acceptor groups separated b y a spacer, are c o m p o s e d of organic or m e t a l i o n entities. It is a t r i b u t e to the synthetic c h e m i s t that w e have so m a n y m o d e l c o m p o u n d s today. T h e studies o n these m o l e c u l e s , m a n y o f w h i c h are discussed i n this v o l u m e , have p r o v i d e d a r i c h harvest o f i n f o r m a t i o n o n the various i m p o r t a n t factors


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that c o n t r o l i n t r a m o l e c u l a r e l e c t r o n transfer. A m o n g these factors are e n e r g y of the e x c i t e d state, exergonicity (-àG°), distance b e t w e e n the d o n o r (D) a n d acceptor (A), o r i e n t a t i o n of D w i t h respect to A , nature of the b r i d g e , nature of the solvent, a n d t e m p e r a t u r e . W o r k i n this area can b e b r o a d l y s u b d i v i d e d i n t o


1. p h o t o i n d u c e d electron-transfer reactions i n w h i c h b o t h forw a r d (charge separation) a n d reverse (charge recombination) i n t r a m o l e c u l a r electron-transfer rate constants have b e e n measured; 2. charge-shift reactions, i n w h i c h an e l e c t r o n is i n t r o d u c e d (e.g., b y p u l s e radiolysis) i n t o one e n t i t y i n the m o l e c u l e a n d t h e n undergoes i n t r a m o l e c u l a r e l e c t r o n transfer to another e n t i t y ; and 3. b i m o l e c u l a r studies u s i n g u n c o m b i n e d d o n o r a n d acceptor entities, i n w h i c h it has b e e n possible to infer the u n i m o l e c u l a r rate constants for charge r e c o m b i n a t i o n w i t h i n the geminate radical i o n pairs f o r m e d b y charge separation at e n c o u n t e r b e t w e e n an excited m o l e c u l e a n d a q u e n c h e r . Studies o n c o m b i n e d d o n o r - a c c e p t o r m o d e l systems have e x p a n d e d to i n c l u d e m u l t i p l e donors or acceptors, u p to four i n t e r a c t i n g entities. S o m e o f these m o l e c u l e s have also p r o v i d e d excellent m o d e l systems for the s t u d y of t r i p l e t excitation transfer. Studies o f organic d o n o r - a c c e p t o r adducts have b e e n c o m p l e m e n t e d a n d e x t e n d e d b y synthesis a n d d e t a i l e d investigation of i n o r g a n i c analogs. T h e v a r i a b i l i t y of oxidation states a n d reorganization energies afforded b y m e t a l complexes has b e e n u s e d to p a r t i c u l a r advantage i n studies r a n g i n g from the classic C r e u t z - T a u b e c o m p o u n d (24) to the elegant " i n t e r v a l e n e e " electron-transfer p e p t i d e spacer studies b y I s i e d (25, 26) a n d others [e.g., O h n o et a l . (27)]. T h e p h o t o c h e m i c a l p r o p e r t i e s of transition m e t a l complexes have b e e n strongly l i n k e d to t h e i r electron-transfer properties. M o s t r e c e n t l y , k e e n i n terest i n p h o t o c h e m i c a l " w a t e r s p l i t t i n g " catalyzed b y t r i s ( 4 , 4 ' - b i p y r i dyl)Ru(II) a n d its homologs has s p a w n e d a d e e p e r a p p r e c i a t i o n of the f u n d a m e n t a l r e l a t i o n b e t w e e n p h o t o c h e m i c a l radiationless transitions a n d e l e c t r o n transfer, as s u m m a r i z e d b y the energy gap l a w i n the i n v e r t e d r e g i o n (10). H e m e p r o t e i n s have also p r o v i d e d a v e r y useful system for the study of electron-transfer reactions across a fixed distance. I n these studies, i n o r g a n i c complexes (e.g., R u complexes) have b e e n attached to p e r i p h e r a l a m i n o acids, as e x e m p l i f i e d b y the w o r k of T h e r i e n et a l . (28), I s i e d (25, 26), a n d others. P h o t o i n d u c e d e l e c t r o n transfer is t h e n i n i t i a t e d b y excitation of e i t h e r


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the R u c o m p l e x o r the h e m e group. T h i s subject has b e e n h e l p e d c o n s i d e r a b l y b y theoretical w o r k such as that b y B e r a t a n a n d O n u c h i c (29).


A c o m p l e m e n t a r y approach has b e e n p u r s u e d b y N a t a n a n d H o f f m a n (30), M c L e n d o n et al. (31), a n d others, w h o s t u d i e d electron transfer b e t w e e n two proteins. I n general, these p r o t e i n pairs are p h y s i o l o g i c a l partners. I n such studies, some u n c e r t a i n t y m a y exist about the precise structure of the p r o t e i n - p r o t e i n complex. I n d e e d , recent w o r k has suggested that s u c h p r o t e i n - p r o t e i n complexes can b e h i g h l y d y n a m i c , w i t h relative m o t i o n a l o n g the i n t e r a c t i n g p r o t e i n surfaces. It is difficult i n such systems to discuss the "distance d e p e n d e n c e " or " p a t h w a y d e p e n d e n c e " of electron-transfer rates, because the system investigated describes not just one s t r u c t u r e , b u t a f a m i l y of structures. C o n v e r s e l y , such studies do p r o v i d e k e y i n f o r m a t i o n o n aspects of b i o l o g i c a l design. T h i s i n f o r m a t i o n leads not o n l y to adequate r e a c t i o n rates b u t also to excellent reaction specificities. It is h o p e d that such insights m a y u l t i m a t e l y l e a d to the study a n d u n d e r s t a n d i n g of i n v i v o e l e c t r o n transport systems. Researchers c o n t i n u e to study e l e c t r o n transfer i n p h o t o s y n t h e t i c systems. B y c a r r y i n g out specific modifications to the structure of the reaction center, e i t h e r b y extracting a n d r e p l a c i n g components or b y genetic m o d ifications, it is possible to obtain i n f o r m a t i o n o n the i m p o r t a n c e of c e r t a i n c o m p o n e n t s a n d structural features i n c o n t r o l l i n g the rate of e l e c t r o n transfer i n the reaction center. I n a d d i t i o n , m a n y sophisticated t e c h n i q u e s (e.g., Stark spectroscopy a n d quantitative femtosecond spectroscopy) are b e i n g u s e d to elucidate the nature of the electron-transfer process. S o m e of this w o r k is d e s c r i b e d i n this book (32). F i n a l l y , M i l l e r (33) has p r o v i d e d an excellent s u m m a r y of the p u z z l e s of electron-transfer processes, a n d M a r c u s (34) has s u m m a r i z e d the i m p o r tant points arising from the s y m p o s i u m u p o n w h i c h this v o l u m e was based. I n the future there is l i k e l y to be an expansion a n d b e t t e r u n d e r s t a n d i n g of the studies s u m m a r i z e d i n this i n t r o d u c t i o n , as w e l l as expansion i n t o o t h e r areas. T h e results w i l l b e a better u n d e r s t a n d i n g of the m e c h a n i s m s of e l e c t r o n transfer i n various m o l e c u l a r assemblies a n d of interfacial e l e c t r o n transfer. A p p l i c a t i o n s of this w o r k are l i k e l y to l e a d to the design of m o r e efficient photoconverters of solar energy, photosensing devices, i n f o r m a t i o n storage devices, a n d m a n y other d e v e l o p m e n t s . It is an e x c i t i n g field!

References 1. 2. 3. 4. 5. 6.

Marcus, R. A. J. Chem. Phys. 1956, 24, Marcus, R. A. Faraday Discuss. Chem. Marcus, R. A. Annu. Rev. Phys. Chem. Marcus, R. A. J. Chem. Phys. 1965, 43, Marcus, R. A. Faraday Discuss. Chem. Hush, N. S. Trans. Faraday Soc. 1961,

966. Soc. 1960, 29, 21. 1964, 15, 1 5 5 . 679. Soc. 1982, 74, 7. 57, 5 5 7 .



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7. Levich, V. G.; Dogonadze, R. R. Dokl Akad. Nauk. SSSR 1959,124, 123; Dokl Phys. Chem. (Engl. Transi) 1959, 124, 9. 8. Levich, V. G. Adv. Electrochem. Electrochem. Eng. 1966, 4, 249. 9. Mataga, N.; Miyasaka, H.; Asahi, T.; Ojima, S.; Okada, T. In Ultrafast Phe nomena VI; Springer Verlag: Berlin, 1988; pp 511-516. 10. Mataga, N. In Electron Transfer in Inorganic, Organic, and Biological Systems; Bolton, J. R.; Mataga, N.; McLendon, G., Eds.; Advances in Chemistry Series 228; American Chemical Society: Washington, D C , 1991; Chapter 6 and ref erences cited therein. 11. Bolton, J. R.; Archer, M. D. In Electron Transfer in Inorganic, Organic, and Biological Systems; Bolton, J. R.; Mataga, N.; M c L e n d o n , G . , Eds.; Advances in Chemistry Series 228; American Chemical Society: Washington, D C , 1991; Chapter 2. 12. Deisenhofer, J.; Michel, H. Science (Washington, D.C.) 1989, 245, 1463. 13. Deisenhofer, J.; E p p , O.; M i k i , K . ; Huber, R.; Michel, H. J. Mol Biol 1984, 80, 385. 14. Chang, C. H.; Tiede, D.; Tang, J.; Smith, U.; Norris, J. R.; Schiffer, M . FEBS Lett. 1986, 205, 82. 15. Iwaki, M.; Itoh, S. In Electron Transfer in Inorganic, Organic, and Biological Systems; Bolton, J. R.; Mataga, N.; McLendon, G . , Eds. ; Advances in Chemistry Series 228; American Chemical Society: Washington, D C , 1991; Chapter 10. 16. Connolly, J. S.; Bolton, J. R. In Photoinduced Electron Transfer; Fox, Μ. Α.; Chanon, M., Eds.; Elsevier: New York, 1989; Vol 4, pp 303-393. 17. Wasielewski, M. R.; Johnson, D. G.; Niemczyk, M. P.; Gains, G. L.; O ' N e i l , R.; Svec, W. A. In Electron Transfer in Inorganic, Organic, and Biological Systems; Bolton, J. R.; Mataga, N.; McLendon, G . , Eds.; Advances in Chemistry Series 228; American Chemical Society: Washington, D C , 1991; Chapter 8. 18. Bolton, J. R.; Schmidt, J. Α.; H o , T . - F . ; L i u , J.-Y.; Roach, K. J.; Weedon, C.; Archer, M. D.; Wilford, J. H.; Gadzekpo, V. P. Y. In Electron Transfer in Inorganic, Organic, and Biological Systems; Bolton, J. R.; Mataga, N.; McLendon, G . , Eds.; Advances in Chemistry Series 228; American Chemical Society: Washington, D C , 1991; Chapter 7. 19. See for example Förster, T h . Fluoreszenz Organischer Verbindungen; Vandenhoeck & Ruprecht: Göttingen, 1951; p 219. 20. Kakitani, T.; Yoshimori, Α.; Mataga, N . In Electron Transfer in Inorganic, Or ganic, and Biological Systems; Bolton, J. R.; Mataga, N.; M c L e n d o n , G . , E d s . ; Advances in Chemistry Series 228; American Chemical Society: Washington, D C , 1991; Chapter 4. 21. Sutin, N . In Electron Transfer in Inorganic, Organic, and Biological Systems; Bolton, J. R.; Mataga, N.; McLendon, G . , Eds.; Advances in Chemistry Series 228; American Chemical Society: Washington, D C , 1991; Chapter 3. 22. Maroncelli, M.; Mclnnis, J.; Fleming, G. R. Science (Washington, D.C.) 1989, 243, 1674. 23. Zhang, X . ; Kozik, M.; Sutin, N.; Winkler, J. R. In Electron Transfer in Inor ganic, Organic, and Biological Systems; Bolton, J. R.; Mataga, N.; M c L e n d o n , G . , Eds.; Advances in Chemistry Series 228; American Chemical Society: Wash ington, D C , 1991; Chapter 16. 24. Creutz, C.; Taube, H . J. Am. Chem. Soc. 1969, 91, 3988. 25. Isied, S. S. Prog. Inorg. Chem. 1984, 32, 443. 26. Isied, S. S. In Electron Transfer in Inorganic, Organic, and Biological Systems; Bolton, J. R.; Mataga, N.; McLendon, G . , Eds.; Advances i n Chemistry Series 228; American Chemical Society: Washington, D C , 1991; Chapter 15. 27. Ohno, T.; Yoshimura, Α.; Ikeda, N.; Haga, M.-A. In Electron Transfer in In-


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organic, Organic, and Biological Systems; Bolton, J. R.; Mataga, N.; M c L e n d o n , G., E d s . ; Advances in Chemistry Series 228; American Chemical Society: Wash ington, D C , 1991; Chapter 14. Therien, M. J.; Bowler, Β. E.; Selman, Μ. Α.; Gray, Η. B.; Chang, I-J.; Winkler, In Electron Transfer in Inorganic, Organic, and Biological Systems; Bolton, Mataga, N.; McLendon, G . , Eds.; Advances in Chemistry Series 228; American Chemical Society: Washington, D C , 1991; Chapter 12. Beratan, D. N.; Onuchic, J. N. In Electron Transfer in Inorganic, Organic, and Biological Systems; Bolton, J. R.; Mataga, N.; McLendon, G . , Eds.; Advances in Chemistry Series 228; American Chemical Society: Washington, D C , 1991; Chapter 5. Natan, M. J.; Hoffman, Β. M. In Electron Transfer in Inorganic, Organic, and Biological Systems; Bolton, J. R.; Mataga, N.; McLendon, G . , E d s . ; Advances in Chemistry Series 228; American Chemical Society: Washington, D C , 1991; Chapter 13. McLendon, G. L.; Hickey, D . ; Sherman, F.; Brayer, G . In Electron Transfer in Inorganic, Organic, and Biological Systems; Bolton, J. R.; Mataga, N.; M c L e n d o n , G . , E d s . ; Advances in Chemistry Series 228; American Chemical Society: Washington, D C , 1991; Chapter 11. Franzen, S.; Boxer, S. G. In Electron Transfer in Inorganic, Organic, and Biological Systems; Bolton, J. R.; Mataga, N . ; McLendon, G . , Eds.; Advances in Chemistry Series 228; American Chemical Society: Washington, D C , 1991; Chapter 9. M i l l e r , J. R. In Electron Transfer in Inorganic, Organic, and Biological Systems; Bolton, J. R.; Mataga, N.; McLendon, G . , Eds.; Advances in Chemistry Series 228; American Chemical Society: Washington, D C , 1991; Chapter 17. Marcus, R. A . In Electron Transfer in Inorganic, Organic, and Biological Sys tems; Bolton, J. R.; Mataga, N.; McLendon, G . , Eds.; Advances in Chemistry Series 228; American Chemical Society: Washington, D C , 1991; Epilogue.

R E C E I V E D for review A p r i l 27, 1990. A C C E P T E D revised manuscript July 19, 1990.


Introduction to Electron Transfer in Inorganic, Organic, and Biological

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