Metal Clusters in Proteins - American Chemical Society

Chapter 11

Involvement of Manganese in Photosynthetic Water Oxidation Gary W. Brudvig

Downloaded by CORNELL UNIV on January 10, 2018 | http://pubs.acs.org Publication Date: June 21, 1988 | doi: 10.1021/bk-1988-0372.ch011

Department of Chemistry, Yale University, New Haven, CT 06511

A multinuclear Mn complex functions in photosystem II to accumulate oxidizing equivalents and also to bind water and catalyze its four-electron oxidation. The Mn complex can exist in five oxidation states called Si states ( i = 0-4). Electron paramagnetic resonance (EPR), Mn K-edge X-ray absorption, and ultraviolet -absorption spectroscopies have been applied to study the structure and function of the Mn complex. The application of these methods to probe the Mn complex in photosystem II is briefly reviewed. Considering the results of both the X-ray absorption and EPR studies, a distortion of an oxo-bridged "cubane"-like Mn tetramer seems to best account for the arrangement of Mn ions in the S state. Based on the known properties of the Mn complex in photosystem II and the coordination chemistry of Mn, structures were proposed for the five intermediate oxidation states of the Mn complex; these structures were incorporated into a molecular mechanism for the formation of an O-O bond and the displacement of O from the S state (Brudvig, G.W. and Crabtree, R.H. Proc. Natl. Acad. Sci. USA 1986, 83, 4586-88). This mechanism and the structure of the Mn complex are considered in light of recent studies of the Mn complex in photosystem II. 2

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A l t h o u g h Mn o c c u r s w i d e l y i n b i o l o g i c a l systems, o n l y a s m a l l number o f enzymes have been i d e n t i f i e d t h a t u t i l i z e oxidation s t a t e s o f Mn h i g h e r t h a n +2. These r e d o x - a c t i v e Mn enzymes i n c l u d e the Mn s u p e r o x i d e d i s m u t a s e , which i s t h e o n l y Mn enzyme i n t h i s group f o r w h i c h an X-ray c r y s t a l s t r u c t u r e i s a v a i l a b l e (1) , t h e M n - c o n t a i n i n g p s e u d o c a t a l a s e ( 2 ) , and photosystem I I ( f o r r e v i e w s see 3-6). Photosystem I I i s unique among t h i s group o f enzymes i n t h a t o t h e r t r a n s i t i o n m e t a l s have n o t been found t o f u n c t i o n i n p l a c e o f Mn, whereas a l t e r n a t e n a t u r a l l y - o c c u r r i n g forms o f supero x i d e dismutase and c a t a l a s e e x i s t w h i c h c o n t a i n Fe i n s t e a d o f Mn. The f u n c t i o n o f photosystem I I i s t o o x i d i z e water and reduce 0097-6156/88/0372-0221$06.00/0 « 1988 American Chemical Society

Que; Metal Clusters in Proteins ACS Symposium Series; American Chemical Society: Washington, DC, 1988.

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plastoquinone (PQ). I n a d d i t i o n , photosystem I I g e n e r a t e s a pH g r a d i e n t a c r o s s the t h y l a k o i d membrane by p r o d u c i n g and consuming p r o t o n s on o p p o s i t e s i d e s o f the membrane. The o v e r a l l r e a c t i o n , which r e q u i r e s four l i g h t - i n d u c e d charge s e p a r a t i o n s in the photosystem I I r e a c t i o n c e n t e r , i s : 2H 0 + 2PQ 2

+ 4H

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where i n and out r e f e r to the i n s i d e and o u t s i d e o f the t h y l a k o i d vesicle, respectively. Mn was f i r s t shown to p l a y an i m p o r t a n t r o l e i n p h o t o s y n t h e t i c 0 e v o l u t i o n by n u t r i t i o n a l s t u d i e s o f a l g a e ( 7 ) . The stoichiomet r y o f Mn i n photosystem I I was d e t e r m i n e d by q u a n t i t a t i n g Mn r e l e a s e d from t h y l a k o i d membranes by v a r i o u s t r e a t m e n t s ( 8 ) . These e x p e r i m e n t s e s t a b l i s h e d t h a t Mn i s s p e c i f i c a l l y r e q u i r e d f o r water o x i d a t i o n and t h a t f o u r Mn i o n s per photosystem I I are r e q u i r e d f o r optimal rates of 0 e v o l u t i o n ( 9 ) . More r e c e n t l y , photosystem I I preparations w i t h high rates of 0 e v o l u t i o n have been i s o l a t e d from a v a r i e t y o f s o u r c e s ( f o r a r e v i e w see 10). The i s o l a t i o n o f an 0 - e v o l v i n g photosystem I I has p r o v e d to be a major step f o r w a r d i n b o t h the b i o c h e m i c a l and s p e c t r o s c o p i c c h a r a c t e r i z a t i o n o f the 0 - e v o l v i n g system. These p r e p a r a t i o n s c o n t a i n f o u r Mn i o n s per p h o t o s y s t e m I I ( 1 1 ) , thus c o n f i r m i n g t h a t f o u r Mn ions are f u n c t i o n a l l y a s s o c i a t e d w i t h each 0 - e v o l v i n g c e n t e r .


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Photooxidation

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To a c c o u n t f o r the p e r i o d i c i t y o f f o u r i n the y i e l d o f 0 in a s e r i e s o f f l a s h e s (12-13), Kok and coworkers (14) p r o p o s e d t h a t photosystem I I c y c l e s through f i v e s t a t e s d u r i n g f l a s h i l l u m i n a tion. These i n t e r m e d i a t e o x i d a t i o n s t a t e s are r e f e r r e d to as S s t a t e s ( i = 0-4) w i t h the s u b s c r i p t d e n o t i n g the number o f o x i d i z i n g e q u i v a l e n t s accumulated. The s e q u e n t i a l advancement o f the S s t a t e s o c c u r s v i a the l i g h t - i n d u c e d charge s e p a r a t i o n i n photosystem I I . A l a r g e body o f e v i d e n c e now s u p p o r t s the b a s i c model put f o r w a r d by Kok and coworkers (3-6,15). The S state rapidly r e l e a s e s a m o l e c u l e o f 0 and r e g e n e r a t e s the S s t a t e . The S and S s t a t e s are u n s t a b l e and are reduced i n the dark to the state w i t h h a l f - t i m e s on the o r d e r o f one minute a t room temperature. F u r t h e r , the S s t a t e i s o x i d i z e d i n the d a r k to the S s t a t e w i t h a h a l f - t i m e on the o r d e r o f t e n minutes a t room temperature (1617). Hence, samples t h a t are i n c u b a t e d i n the dark f o r more t h a n t h i r t y minutes a t room temperature c o n t a i n o n l y the S state. In c o n t r a s t , c o n t i n u o u s l y i l l u m i n a t e d samples c o n t a i n e q u a l f r a c t i o n s of s t a t e s S t h r o u g h S w h i c h decay w i t h i n a few minutes i n the dark a t room temperature to a m i x t u r e o f S and S i n a 1:3 r a t i o . The q u e s t i o n o f the m o l e c u l a r b a s i s f o r the S s t a t e s has e x i s t e d s i n c e the o r i g i n a l p r o p o s a l by Kok and coworkers. As f i r s t f o r m u l a t e d , the S s t a t e d e s i g n a t i o n r e f e r r e d to the o x i d a t i o n s t a t e o f the 0 - e v o l v i n g c e n t e r w h i c h c o u l d , i n p r i n c i p l e , i n c l u d e a l l o f photosystem I I and i t s a s s o c i a t e d components. Indeed, t h e r e are a number o f r e d o x - a c t i v e components on the e l e c t r o n - d o n o r side of photosystem I I i n a d d i t i o n to the Mn complex, such as the t y r o s i n e r a d i c a l t h a t g i v e s r i s e to EPR s i g n a l I I , and cytochrome b . 2

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Manganese in Photosynthetic Water Oxidation

However, a change i n the o x i d a t i o n s t a t e o f these s p e c i e s does not a l t e r e i t h e r the p e r i o d - f o u r o s c i l l a t i o n o f 0 y i e l d s i n a s e r i e s o f f l a s h e s , p r o v i d e d t h a t the f l a s h e s are s u f f i c i e n t l y c l o s e l y spaced ( 1 6 ) , or the EPR s p e c t r a l p r o p e r t i e s o f the S s t a t e (18). Moreover, EPR (17-31) and X - r a y a b s o r p t i o n (32-38) s t u d i e s have shown t h a t Mn i s o x i d i z e d i n the S to S t r a n s i t i o n . Hence, i t appears t h a t the S s t a t e s s h o u l d be i n t e r p r e t e d i n terms o f d i s t i n c t i n t e r m e d i a t e o x i d a t i o n s t a t e s o f the Mn complex (see b e l o w ) . 2

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EPR

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I n g e n e r a l , one e x p e c t s t o observe an EPR s i g n a l from a t r a n s i t i o n m e t a l complex whenever the complex p o s s e s s e s an odd number o f unpaired electrons. I f the complex p o s s e s s e s an even number o f u n p a i r e d e l e c t r o n s , t h e n s p i n - s p i n i n t e r a c t i o n s may g i v e r i s e to l a r g e z e r o - f i e l d s p l i t t i n g s o f the s p i n l e v e l s w h i c h w i l l p r e v e n t the o b s e r v a t i o n o f EPR s i g n a l s w i t h c o n v e n t i o n a l EPR i n s t r u m e n t a tion. Because each S - s t a t e t r a n s i t i o n i n v o l v e s the removal o f one e l e c t r o n from the 0 - e v o l v i n g c e n t e r , one p r e d i c t s t h a t a l t e r n a t e S s t a t e s w i l l have an odd number o f u n p a i r e d e l e c t r o n s . These a l t e r n a t e S s t a t e s should, i n p r i n c i p l e , be d e t e c t a b l e by EPR s p e c t r o s c o p y . Indeed, the S s t a t e e x h i b i t s a m u l t i l i n e EPR s i g n a l ( F i g u r e 1) from a m u l t i n u c l e a r Mn complex ( 1 9 ) . The S -state m u l t i l i n e EPR s i g n a l was one o f the f i r s t d i r e c t probes o f the Mn complex i n photosystem I I and much o f the i n f o r m a t i o n on the s t r u c t u r e and f u n c t i o n o f the Mn complex has come from a n a l y s e s of the S - s t a t e EPR s i g n a l s (17-31). However, a major l i m i t a t i o n to the use of EPR s p e c t r o s c o p y to s t u d y the Mn complex i s t h a t measurements have been r e s t r i c t e d to the S state. Based on the argument t h a t EPR s i g n a l s are e x p e c t e d from a l t e r n a t e S s t a t e s , one p r e d i c t s t h a t the S s t a t e i s a good c a n d i d a t e f o r d e t e c t i o n by EPR s p e c t r o s c o p y . N o n e t h e l e s s , an EPR s i g n a l has not y e t been d e t e c t e d from the S s t a t e . Two d i s t i n c t EPR s i g n a l s have been o b s e r v e d from the S state ( F i g u r e 1) . The f i r s t i s the m u l t i l i n e EPR s i g n a l c e n t e r e d a t about g = 2.0. T h i s EPR s i g n a l a r i s e s from an S = 1/2 s t a t e o f a m i x e d - v a l e n c e m u l t i n u c l e a r Mn complex; the numerous h y p e r f i n e l i n e s a r i s e from the c o u p l i n g o f the u n p a i r e d e l e c t r o n to the n u c l e a r s p i n s o f s e v e r a l Mn i o n s (each Mn i o n has I = 5/2) . The second EPR s i g n a l from the S s t a t e e x h i b i t s a t u r n i n g p o i n t a t g = 4.1. The g = 4.1 EPR s i g n a l i s g e n e r a t e d by i l l u m i n a t i o n of photosystem I I membranes a t 130 K, but i s u n s t a b l e and i s c o n v e r t e d i n t o the m u l t i l i n e EPR s i g n a l upon warming to 200 Κ (18,22). However, the g = 4.1 EPR s i g n a l can be s t a b i l i z e d by the a d d i t i o n o f v a r i o u s exogenous m o l e c u l e s i n c l u d i n g amines ( 2 9 ) , f l u o r i d e ( 2 2 ) , and s u c r o s e (25). Two i n t e r p r e t a t i o n s o f the i d e n t i t y o f the s p e c i e s t h a t g i v e s r i s e to the S - s t a t e m u l t i l i n e and g = 4.1 EPR s i g n a l s have been p r o p o s e d (24-26). Both EPR s i g n a l s are p r o p o s e d to a r i s e from Mn centers. The d i f f e r e n c e i n i n t e r p r e t a t i o n s concerns the number of Mn i o n s i n v o l v e d i n each paramagnetic s p e c i e s . One v i e w i s t h a t t h r e e d i s t i n c t Mn c e n t e r s f u n c t i o n i n the water o x i d a t i o n p r o c e s s : two mononuclear Mn c e n t e r s and a b i n u c l e a r Mn c e n t e r (26). I t was proposed (26) t h a t the b i n u c l e a r c e n t e r g i v e s r i s e t o the m u l t i l i n e EPR s i g n a l , whereas, one of the 2

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Figure 1: S state EPR spectra: a) m u l t i l i n e EPR signal produced by i l l u m i n a t i o n at 200 K; b) g - 4.1 EPR signal produced by i l l u m i n a t i o n at 130 K. Experimental conditions are as i n (24). 2


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mononuclear Mn i o n s g i v e s r i s e t o t h e g — 4.1 EPR s i g n a l . I n o r d e r t o e x p l a i n t h e s t a b i l i z a t i o n o f t h e g = 4.1 EPR s i g n a l by exogenous m o l e c u l e s , Hansson e t a l . (26) proposed t h a t t h e g = 4.1 EPR s i g n a l a r i s e s from a mononuclear Mn(IV) i n redox e q u i l i b r i u m w i t h a b i n u c l e a r Mn s p e c i e s . Hence, i n t h e S s t a t e , i t was p r o p o s e d t h a t e i t h e r t h e mononuclear Mn i s o x i d i z e d t o Mn(IV) and g i v e s a g - 4.1 EPR s i g n a l o r t h e b i n u c l e a r Mn c e n t e r i s o x i d i z e d t o M n ( I I I ) - M n ( I V ) and g i v e s a m u l t i l i n e EPR s i g n a l . The r e d u c t i o n p o t e n t i a l s o f t h e s e two s p e c i e s must be comparable i n t h e cases when t h e g — 4.1 EPR s i g n a l i s s t a b i l i z e d . I n t h i s model, a f u r t h e r o x i d a t i o n o f the system t o t h e S s t a t e s h o u l d l e a v e b o t h t h e b i n u c l e a r and mononuclear c e n t e r s o x i d i z e d . However, no EPR s i g n a l i s o b s e r v e d from t h e Mn complex i n t h e S s t a t e w h i c h , i n t h i s model, r e q u i r e s t h a t t h e g » 4.1 and m u l t i l i n e EPR s i g n a l s p e c i e s a r e m a g n e t i c a l l y coupled i n the S state. Hence, t h e redox e q u i l i b r i u m model r e q u i r e s t h a t t h e s e two Mn s p e c i e s must be v e r y c l o s e t o g e t h e r . The a l t e r n a t e p r o p o s a l i s t h a t b o t h t h e m u l t i l i n e and g = 4.1 EPR s i g n a l s a r i s e from t h e same t e t r a n u c l e a r Mn complex (18,24-25). The c o n v e r s i o n o f t h e g = 4.1 EPR s i g n a l i n t o t h e m u l t i l i n e EPR s i g n a l upon i n c u b a t i o n a t 200 Κ i n t h e dark c a n t h e n be e x p l a i n e d by a temperature-dependent s t r u c t u r a l change i n t h e Mn s i t e upon formation o f the S s t a t e , w h i c h a l t e r s t h e exchange c o u p l i n g s between t h e Mn i o n s (24). G e n e r a t i o n o f t h e S s t a t e a t 130 Κ may not a l l o w such a rearrangement t o o c c u r r a p i d l y and, hence, t h e g - 4.1 EPR s i g n a l c o u l d be v i e w e d as an EPR s i g n a l a r i s i n g from an Sj^-state c o n f o r m a t i o n t h a t i s i n t h e S s t a t e . The s t r u c t u r a l d i f f e r e n c e between t h e "g = 4.1" and " m u l t i l i n e " c o n f o r m a t i o n s need not be l a r g e ; t h e c o n v e r s i o n o f t h e g = 4.1 EPR s i g n a l i n t o t h e m u l t i l i n e EPR s i g n a l c a n be u n d e r s t o o d as a s m a l l rearrangement o f the Mn complex i n t o i t s p r e f e r r e d c o n f o r m a t i o n i n t h e h i g h e r oxidation state. S t a b i l i z a t i o n o f t h e g - 4.1 EPR s i g n a l by exogenous m o l e c u l e s i s e x p l a i n e d i n t h i s model by s t a b i l i z a t i o n o f the "g — 4.1" c o n f o r m a t i o n . These two models may n o t be s i g n i f i c a n t l y d i f f e r e n t . The main d i f f e r e n c e between them i s t h e magnitude o f t h e magnetic c o u p l i n g p r o p o s e d t o e x i s t between t h e f o u r Mn i o n s i n t h e S s t a t e . How e v e r , t h e d i f f e r e n t Mn c e n t e r s must be v e r y c l o s e t o g e t h e r i n o r d e r to a c c o u n t f o r t h e absence o f an EPR s i g n a l from t h e S s t a t e . The S - s t a t e EPR s i g n a l s have a l s o been used t o probe t h e c o o r d i n a t i o n o f exogenous l i g a n d s t o t h e Mn complex (27-31). Ammonia, b u t n o t more b u l k y amines, d r a m a t i c a l l y a l t e r s t h e l i n e s h a p e o f t h e S - s t a t e m u l t i l i n e EPR s i g n a l , i n d i c a t i n g t h a t ammonia b i n d s d i r e c t l y t o Mn i n t h e S s t a t e ( 2 8 ) . The b i n d i n g o f ammonia t o t h e Mn complex has been p r o p o s e d t o be a n u c l e o p h i l i c a d d i t i o n r e a c t i o n and t o model t h e b i n d i n g o f s u b s t r a t e water (2729). Also, 0 - l a b e l e d w a t e r s l i g h t l y broadens t h e S - s t a t e m u l t i l i n e EPR s i g n a l ( 3 0 ) . The b r o a d e n i n g o f t h e S - s t a t e m u l t i l i n e EPR s i g n a l i n t h e presence o f 0 - l a b e l e d w a t e r under t h e c o n d i t i o n s o f t h e s e experiments i n d i c a t e s t h a t exchangeable w a t e r i s a l i g a n d t o Mn i n t h e S s t a t e . One c a n e n v i s i o n t h a t w a t e r c o o r d i n a t e s t o t h e Mn s i t e e i t h e r as t h e s u b s t r a t e o r i n t h e form of a s t r u c t u r a l oxo-bridge. (The mode o f b i n d i n g may be e q u i v a l e n t i n t h e s e two c a s e s ; t h e d i s t i n c t i o n c a n be made on t h e b a s i s o f the s p e c i e s t h a t g i v e s r i s e t o 0 ) . S e v e r a l s t u d i e s , however, i n d i c a t e t h a t t h e s u b s t r a t e water i s n o t bound t o t h e Mn s i t e i n 2

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the S s t a t e ( f o r a d i s c u s s i o n see 2 7 ) . By measuring t h e e f f e c t o f 0 - l a b e l e d water on t h e S - s t a t e m u l t i l i n e EPR s i g n a l f o l l o w i n g i n c u b a t i o n w i t h a s p e c i f i c S s t a t e , one may be a b l e t o make a d i s t i n c t i o n between s u b s t r a t e w a t e r , w h i c h appears t o b i n d t o t h e Mn complex i n one o f t h e h i g h e r S s t a t e s , and s t r u c t u r a l oxob r i d g e s between t h e Mn i o n s , w h i c h may be exchangeable b u t remain bound t h r o u g h o u t t h e S - s t a t e cycle. 0-labeled water also broadens t h e a l t e r e d S - s t a t e m u l t i l i n e EPR s i g n a l formed i n t h e p r e s e n c e o f ammonia ( 3 1 ) . One i n t e r p r e t a t i o n o f t h i s r e s u l t i s t h a t t h e Mn complex i n t h e ammonia-bound d e r i v a t i v e o f photosystem I I c o n t a i n s exchangeable o x o - b r i d g e s between Mn i o n s t h a t a r e n o t d i s p l a c e d by ammonia i n the S s t a t e . 2

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X-ray Absorption

S t u d i e s o f the Manganese Complex

The o x i d a t i o n s t a t e s and l i g a t i o n o f Mn i n photosystem I I have been probed by X-ray a b s o r p t i o n edge and extended X-ray a b s o r p t i o n edge f i n e s t r u c t u r e (EXAFS) measurements (32-38). EXAFS a n a l y s e s have been done f o r Mn i n t h e S s t a t e p r e s e n t i n d a r k - a d a p t e d t h y l a k o i d membranes (33,37) and i n d a r k - a d a p t e d photosystem I I membranes (35) . These s t u d i e s i n d i c a t e t h a t each Mn i o n i s p r o b a b l y s i x c o o r d i n a t e and l i g a t e d t o oxygen and/or n i t r o g e n l i g a n d s . Each Mn i o n a l s o sees 0.77 (35) o r 2 - 3 (37) n e i g h b o r i n g Mn i o n s a t a distance o f 2.7 À. The EXAFS d a t a f o r t h e S state look e s s e n t i a l l y t h e same as f o r t h e S s t a t e (36) and, t h e r e f o r e , i t appears t h a t the Mn s i t e does n o t undergo a s u b s t a n t i a l s t r u c t u r a l r e o r g a n i z a t i o n d u r i n g the S.,^ t o S t r a n s i t i o n . The EXAFS o f Mn i n photosystem I I l o o k s v e r y much l i k e t h a t o f a m i x e d - v a l e n c e d i - / i - o x o - b r i d g e d Mn dimer model compound (33,35). I n p a r t i c u l a r , t h e Mn-Mn d i s t a n c e o f 2.7 À i n photosystem I I i s c h a r a c t e r i s t i c o f a di-μ-oxo-bridged s t r u c t u r e . Recent EXAFS d a t a have i n d i c a t e d t h a t a second Mn-Mn d i s t a n c e o f 3.3 À may a l s o be p r e s e n t (37-38). A l t h o u g h a c l e a r p i c t u r e o f a l l o f t h e Mn-Mn d i s t a n c e s i s n o t y e t a v a i l a b l e , t h e EXAFS r e s u l t s a r e c o n s i s t e n t w i t h a s t r u c t u r e i n which two di-μ-oxo b r i d g e d Mn dimers a r e present i n close proximity. Of note i s t h e apparent l a c k o f c h l o r i d e i n t h e f i r s t c o o r d i n a t i o n s h e l l o f Mn i n e i t h e r t h e S o r t h e S s t a t e as r e v e a l e d by EXAFS s t u d i e s o f Mn ( 3 5 ) . T h i s o b s e r v a t i o n i s o f p a r t i c u l a r i n t e r e s t because c h l o r i d e i s r e q u i r e d f o r o p t i m a l 0 e v o l u t i o n r a t e s (39) and has been proposed t o a c t as a b r i d g i n g l i g a n d i n a p o l y n u c l e a r Mn complex ( 4 0 ) . Recent EPR s t u d i e s , however, a l s o suggest t h a t c h l o r i d e i s n o t bound t o Mn i n the S o r S s t a t e (41) . The energy o f the X-ray a b s o r p t i o n edge r e f l e c t s t h e e l e c t r o n d e n s i t y about Mn w h i c h , i n t u r n , r e f l e c t s t h e o x i d a t i o n s t a t e and l i g a t i o n o f Mn. The energy o f the X-ray a b s o r p t i o n edge o f Mn i n the Sj^ s t a t e i s i n t h e range o b s e r v e d f o r M n ( I I I ) model compounds (32,34). The X-ray a b s o r p t i o n edge o f Mn s h i f t s t o h i g h e r energy i n the S s t a t e and i s i n the range o b s e r v e d f o r M n ( I I I ) and Mn(IV) model compounds (34) . I n l i g h t o f t h e c o n c l u s i o n from t h e EXAFS s t u d i e s t h a t t h e c o o r d i n a t i o n o f Mn does n o t change s u b s t a n t i a l l y i n t h e S^^ t o S t r a n s i t i o n (36) , t h i s r e s u l t i n d i c a t e s t h a t Mn i s o x i d i z e d i n the S to S t r a n s i t i o n . However, t h e s h i f t i n the Mn X - r a y a b s o r p t i o n edge i s v e r y s m a l l i n t h e S t o S transition, s u g g e s t i n g t h a t Mn i t s e l f i s n o t o x i d i z e d i n t h i s s t e p (34,38). 1

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These r e s u l t s seem t o i n d i c a t e t h a t o x i d a t i o n o f Mn o c c u r s i n some, b u t n o t a l l , o f the S - s t a t e t r a n s i t i o n s . T h i s has l e d to p r o p o s a l s t h a t r e d o x - a c t i v e c e n t e r s o t h e r t h a n Mn are i n v o l v e d i n the s t o r a g e o f o x i d i z i n g e q u i v a l e n t s d u r i n g some o f the S - s t a t e t r a n s i t i o n s . However, the energy o f the Mn X - r a y a b s o r p t i o n edge r e f l e c t s e l e c t r o n d e n s i t y about Mn and n o t d i r e c t l y the o x i d a t i o n s t a t e . I t i s p o s s i b l e t h a t the changes i n the energy o f the Mn X-ray a b s o r p t i o n edge c o u l d be a c c o u n t e d f o r by a s i n g l e o x i d a t i o n o f a Mn i o n i n b o t h the S t o S and S t o S t r a n s i t i o n s i f t h e r e i s a change i n l i g a t i o n o f the Mn i o n s i n the S to S transition. Indeed, t h e r e i s e v i d e n c e t h a t the s u b s t r a t e w a t e r c o o r d i n a t e s to the Mn complex i n the S s t a t e ( f o r a d i s c u s s i o n see 27) . The c o o r d i n a t i o n o f a Lewis base, such as w a t e r , t o the Mn complex i n the S s t a t e would be e x p e c t e d t o cause the s h i f t o f the Mn X - r a y a b s o r p t i o n edge i n the S t o S t r a n s i t i o n t o be s m a l l even though the Mn complex i s o x i d i z e d by one e l e c t r o n . x

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U l t r a v i o l e t A b s o r p t i o n S t u d i e s o f the Manganese Complex Flash-induced UV-difference spectral data indicate that a chromophore a s s o c i a t e d w i t h the S s t a t e s can be m o n i t o r e d i n the 300-350 nm range (42-46). The d i f f i c u l t y w i t h these measurements i s t h a t s e v e r a l o t h e r components i n photosystem I I a l s o e x h i b i t s p e c t r a l changes i n t h i s r e g i o n o f the spectrum. A f t e r c o r r e c t i n g f o r the absorbance changes due to redox changes o f Q , Q ( o r an exogenous e l e c t r o n a c c e p t o r ) , and Ζ i n p h o t o s y s t e m I I , Dekker e t a l . (42) found t h a t the absorbance changes a s s o c i a t e d w i t h the S to S , S t o S , and S t o S t r a n s i t i o n s were a l l e q u i v a l e n t and r e s e m b l e d the d i f f e r e n c e i n absorbance between a M n ( I I I ) and a M n ( I V ) - g l u c o n a t e model complex. Dekker e t a l . (42) c o n c l u d e d t h a t one M n ( I I I ) i s o x i d i z e d t o Mn(IV) i n each o f the f i r s t t h r e e Sstate transitions. More r e c e n t work has c o n s i d e r a b l y c o m p l i c a t e d t h i s i n t e r p r e t a t i o n (43-46). I t now seems p r o b a b l e t h a t the absorbance changes are n o t a l l the same f o r the d i f f e r e n t S - s t a t e transitions. The most r e c e n t U V - s p e c t r a l d a t a are c o n s i s t e n t w i t h a s i n g l e o x i d a t i o n o f Mn i n each o f the S - s t a t e t r a n s i t i o n s (454 6 ) , a l t h o u g h the assignment o f the U V - d i f f e r e n c e s p e c t r a t o the o x i d a t i o n o f M n ( I I I ) t o Mn(IV) i s n o t c l e a r because the s p e c t r a l changes f o r the o x i d a t i o n o f M n ( I I ) t o M n ( I I I ) may be s i m i l a r ( 4 7 ) . A

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S t r u c t u r e o f the Manganese Complex The Mn-Mn d i s t a n c e o f 2.7 Â d e t e r m i n e d by EXAFS i s d i a g n o s t i c o f a d i - ) L i - o x o - b r i d g e d Mn dimer i n photosystem I I (33,35). However, one c o u l d imagine a number o f arrangements o f the f o u r Mn i o n s i n photosystem I I w h i c h c o n t a i n a di-/z-oxo-bridged s t r u c t u r e . Moreo v e r , the o b s e r v a t i o n o f two d i f f e r e n t Mn-Mn d i s t a n c e s by EXAFS, c o u l d o n l y be a c c o u n t e d f o r by one o f the f o l l o w i n g t h r e e arrangements o f Mn: a Mn t r i m e r p l u s one i s o l a t e d (more t h a n 3.3 A away) Mn mononuclear c e n t e r , two i s o l a t e d i n e q u i v a l e n t Mn d i m e r s , or a Mn tetramer. I n o r d e r t o d i s t i n g u i s h between these p o s s i b i l i t i e s , one must c o n s i d e r the EPR p r o p e r t i e s o f the S and S s t a t e s . Measurements have been made o f the temperature dependence o f the S -state m u l t i l i n e (24,48-49) and g = 4.1 (24) EPR s i g n a l s i n o r d e r t o 2

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determine whether the EPR s i g n a l s a r i s e from the ground s t a t e o r from a t h e r m a l l y - p o p u l a t e d s t a t e . The S - s t a t e g » 4.1 EPR s i g n a l e x h i b i t s C u r i e - l a w b e h a v i o r c h a r a c t e r i s t i c o f an EPR t r a n s i t i o n from a ground s t a t e o r from a system i n the h i g h - t e m p e r a t u r e l i m i t (24). I t seems p r o b a b l e t h a t the g — 4.1 EPR s i g n a l a r i s e s from a ground S = 3/2 s t a t e o f a Mn s p e c i e s . The S - s t a t e m u l t i l i n e EPR s i g n a l has been a s s i g n e d t o e i t h e r a ground o r l o w - l y i n g S - 1/2 s t a t e o f a m u l t i n u c l e a r m i x e d - v a l e n c e Mn s p e c i e s (24,48-49); and the S s t a t e does n o t e x h i b i t an EPR s i g n a l . These assignments s e v e r e l y r e s t r i c t the p o s s i b l e arrangements o f Mn i n photosystem I I and a l s o p r o v i d e i m p o r t a n t i n f o r m a t i o n on the s t r u c t u r e o f the Mn complex. On the b a s i s o f a s i m i l a r i t y o f the M n n u c l e a r hyper f i n e c o u p l i n g s i n the S - s t a t e m u l t i l i n e EPR s i g n a l w i t h those o f EPR s i g n a l s from Mn dimer model complexes, i t has been s u g g e s t e d t h a t the S - s t a t e m u l t i l i n e EPR s i g n a l a r i s e s from the S = 1/2 s t a t e o f an a n t i f e r r o m a g n e t i c a l l y exchange c o u p l e d m i x e d - v a l e n c e Mn dimer (20,26). T h i s assignment has l e d t o p r o p o s a l s o f a v a r i e t y o f models i n w h i c h a Mn dimer i s the c a t a l y t i c s i t e f o r water oxidation. T h e r e f o r e , c o n s i d e r the magnetic p r o p e r t i e s o f a b i n u c l e a r m i x e d - v a l e n c e Mn complex. A number o f i n o r g a n i c mixedv a l e n c e Mn dimers have been s y n t h e s i z e d and t h e i r s t r u c t u r e s and magnetic p r o p e r t i e s have been d e t e r m i n e d (50-52) . The u n p a i r e d e l e c t r o n s on each Mn i o n a r e c o r r e l a t e d t h r o u g h exchange i n t e r a c t i o n s t h a t a r i s e from e i t h e r d i r e c t o r b i t a l o v e r l a p o r o r b i t a l o v e r l a p t h a t i s mediated by the b r i d g i n g l i g a n d s ( 5 3 ) . For a binuclear Mn complex, a single isotropic exchange coupling c o n s t a n t , J , u s u a l l y i s s u f f i c i e n t t o account f o r the magnetic p r o p e r t i e s . U s i n g the H e i s e n b e r g exchange H a m i l t o n i a n ( E q u a t i o n 2) one o b t a i n s the energy l e v e l s ( E q u a t i o n 3) f o r a p a i r o f Mn i o n s w i t h e l e c t r o n s p i n s o f S and S , r e s p e c t i v e l y . 2

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Metal Clusters in Proteins - American Chemical Society

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