Mechanistic Bioinorganic Chemistry - American Chemical Society

9 Structure and Function of Manganese in Photosystem II Gary W . Brudvig

Downloaded by SUNY STONY BROOK on October 31, 2014 | http://pubs.acs.org Publication Date: May 5, 1996 | doi: 10.1021/ba-1995-0246.ch009

Department of Chemistry, Yale University, New Haven, C T 06511

The tetranuclear Mn complex in photosystem II functions to accumulate oxidizing equivalents and to catalyze the four-electron oxidation of water to molecular oxygen. In the water-oxidation cycle, the Mn complex is advanced throughfiveintermediate oxidation states called S states (i = 0-4), where i denotes the number of stored oxidizing equivalents. Mechanistic studies of the photosynthetic water oxidation process have been aimed at characterizing the structure and properties of the Mn complex in each of the different S states. Electron paramagnetic resonance and X-ray absorption spectroscopies have been especially powerful methods to probe the Mn complex. However, to use these spectroscopic methods, it is necessary to prepare highly concentrated samples in a specific S state. The photochemical methods used to prepare the different S states are described and the results of studies of the S and S states are summarized. The structure of theMncomplex is considered in light of recent studies. i

1

2

ONE OF THE MOST IMPORTANT ROLES OF MANGANESE

i n b i o l o g y is i the photosynthetic oxidation of water to molecular oxygen. This reaction is c a t a l y z e d b y a m e m b r a n e - b o u n d p r o t e i n c o m p l e x c a l l e d p h o t o s y s t e m I I ( P S I I ) . P S I I uses l i g h t t o p r o d u c e a c h a r g e - s e p a r a t i o n r e a c t i o n t h a t results i n t h e r e d u c t i o n o f plastoquinone, t h e oxidation o f water, a n d t h e g e n e r a t i o n o f a p r o t o n g r a d i e n t across t h e c h l o r o p l a s t t h y l a k o i d membrane. T h e overall reaction, w h i c h requires four photochemical c h a r g e - s e p a r a t i o n r e a c t i o n s , is g i v e n i n e q u a t i o n 1: 2 H 0 + 2 P Q+ 4 H 2

o u t

+

^

0

2

+ 2PQH

2

+ 4H

i n

+

0065-2393/95/0246-0249/$08.00/0 © 1995 American Chemical Society

In Mechanistic Bioinorganic Chemistry; Thorp, H., et al.; Advances in Chemistry; American Chemical Society: Washington, DC, 1996.

(1)

250

M E C H A N I S T I C BIOINORGANIC CHEMISTRY

where P Q denotes plastoquinone, P Q H denotes plastoquinol, and in a n d out refer to the inside a n d outside o f the t h y l a k o i d vesicle, r e s p e c t i v e l y (for r e v i e w s , see r e f e r e n c e s 1 - 5 ) . T h e m e c h a n i s m o f 0 e v o l u t i o n i n p h o t o s y n t h e s i s has b e e n t h e f o c u s o f m u c h r e s e a r c h . I n a c l a s s i c e x p e r i m e n t , J o l i o t a n d c o - w o r k e r s (6) s h o w e d t h a t 0 is e v o l v e d i n a p e r i o d i c p a t t e r n w h e n a d a r k - a d a p t e d s a m p l e is g i v e n a series o f s h o r t , s a t u r a t i n g l i g h t flashes ( F i g u r e 1). T h i s p a t t e r n o f 0 e v o l u t i o n w a s e x p l a i n e d b y K o k a n d c o - w o r k e r s (7, 8) b y t h e S-state m o d e l s h o w n i n e q u a t i o n 2: 2

2

2


2

0

s

2

+ 4H*

hu

2

hu ^

Si

0

2H 0

s

hu

hu

w

s

2

3

w

^ s

4

(2)

Dark State

w h e r e the solid lines denote l i g h t - d r i v e n reactions and the dashed lines denote dark reactions. E a c h photochemical charge separation of PSII p r o d u c e s o n e o x i d i z i n g e q u i v a l e n t , w h i c h is s t o r e d i n t h e 0 - e v o l v i n g c e n t e r ( O E C ) o f P S I I . T h e i n t e r m e d i a t e o x i d a t i o n states o f t h e O E C a r e r e f e r r e d to as S ( " s t o r e " ) states w i t h a s u b s c r i p t t o d e n o t e t h e n u m b e r o f o x i d i z i n g equivalents that have b e e n stored. T o account for the m a x i m a l y i e l d o f 0 o n t h e t h i r d flash ( F i g u r e 1), it is r e q u i r e d t h a t t h e S state is t h e d a r k - s t a b l e state. I n s u b s e q u e n t flashes, t h e y i e l d o f 0 is m a x i m a l o n e v e r y f o u r t h flash d u e to t h e r e q u i r e m e n t o f f o u r o x i d i z i n g e q u i v a l e n t s t o p r o d u c e 0 f r o m w a t e r . B e c a u s e o f " m i s s e s " (in w h i c h t h e O E C d o e s n o t t u r n o v e r d u r i n g a flash) o r " d o u b l e h i t s " (in w h i c h a s i n g l e flash causes a t w o - s t e p a d v a n c e m e n t o f t h e O E C ) , t h e y i e l d o f 2

2

x

2

2

2.5,

Flash Number Figure 1. Normalized 0 yields from thylakoid membranes given a train of saturating flashes. Y„ denotes the yield of 0 on flash η and Y denotes the steady-state yield of 0 . Conditions are as described in reference 44. 2

2

ss

2


9.

BRUDVIG

Structure and Function of Manganese in Photosystem II

251

0 r e a c h e s a s t e a d y - s t a t e v a l u e a f t e r a b o u t 3 0 flashes. I n t h e s t e a d y state, t h e S - S states a r e a s s u m e d to b e p r e s e n t i n a p p r o x i m a t e l y e q u a l a m o u n t s . T h e S state d o e s n o t a c c u m u l a t e i n t h e s t e a d y state b e c a u s e it r a p i d l y d e c a y s t o t h e S state b y r e l e a s i n g 0 ; t h e S state is n o t , i n fact, e v e n o b s e r v e d as a k i n e t i c i n t e r m e d i a t e b e c a u s e f o r m a t i o n o f t h e S state is t h e r a t e - l i m i t i n g s t e p i n t h e S t o S c o n v e r s i o n . T h e S a n d S states a r e u n s t a b l e a n d d e c a y i n s e c o n d s t o t h e S state i n t h e d a r k . T h e S state also d e c a y s i n t h e d a r k to t h e S i state o n a m i n u t e s t i m e scale. H e n c e , a d a r k - a d a p t e d s a m p l e c o n t a i n s p r e d o m i n a n t l y t h e S i state. 2

0

3

4

0

2

4

3

4

0

2

3

x

0

T h e K o k m o d e l f o r 0 e v o l u t i o n is n o w g e n e r a l l y a c c e p t e d . H o w e v e r , t h i s m o d e l d o e s n o t a d d r e s s t h e m o l e c u l a r basis o f t h e i n t e r m e diates. T h u s , the K o k m o d e l o n l y provides a starting p o i n t f r o m w h i c h more detailed mechanistic questions can be posed.


2

A c o n s i d e r a b l e b o d y o f e v i d e n c e i n d i c a t e s t h a t t h e a c t i v e site f o r water oxidation contains a polynuclear M n complex. C a a n d C l ~ are also r e q u i r e d f o r w a t e r o x i d a t i o n a n d m a y b e a s s o c i a t e d w i t h t h e M n c o m p l e x . F o u r M n ions are r e q u i r e d for m a x i m a l 0 - e v o l u t i o n a c t i v i t y , b u t t h e o r g a n i z a t i o n o f t h e M n i o n s i n t h e O E C has b e e n d e b a t e d . It is c l e a r , h o w e v e r , t h a t o x i d a t i o n o f M n o c c u r s d u r i n g t h e S-state t r a n s i t i o n s . X - r a y absorption edge studies have b e e n r e p o r t e d on samples i n w h i c h t h e S states w e r e a d v a n c e d b y flashes o f l i g h t (9). T h e M n K - e d g e e n e r g y i n c r e a s e s f r o m t h e S t o t h e S state a n d s h o w s a p e r i o d - f o u r o s c i l l a t i o n . T h e s e r e s u l t s s u p p o r t t h e v i e w t h a t t h e S t o S states a r e i n c r e a s i n g l y h i g h e r o x i d a t i o n states o f t h e M n c o m p l e x . 2 +

2

0

3

0

3

T o u n d e r s t a n d t h e m e c h a n i s m o f w a t e r o x i d a t i o n , i t is n e c e s s a r y t o c h a r a c t e r i z e e a c h o f t h e S states. A v a r i e t y o f s p e c t r o s c o p i c m e t h o d s have b e e n b r o u g h t to b e a r o n this p r o b l e m . E l e c t r o n p a r a m a g n e t i c resonance (EPR) and X - r a y spectroscopies have been especially useful because these t e c h n i q u e s a l l o w the M n c o m p l e x to b e p r o b e d d i r e c t l y . E P R s p e c t r o s c o p y has t h e r e s t r i c t i o n t h a t t h e M n c o m p l e x m u s t b e p a r a m a g n e t i c to b e s t u d i e d . T h e S state is a n o d d - e l e c t r o n state, a n d E P R s p e c t r o s c o p y has b e e n u s e d e x t e n s i v e l y t o s t u d y t h e M n c o m p l e x i n t h e S state. X - r a y s p e c t r o s c o p y has t h e a d v a n t a g e t h a t a n y state o f t h e M n c o m p l e x is o b s e r v a b l e . H o w e v e r , t h e s u c c e s s f u l a p p l i c a t i o n o f E P R a n d X - r a y s p e c t r o s c o p i e s r e q u i r e s t h a t a s p e c i f i c S state b e p r e p a r e d i n h i g h y i e l d i n highly concentrated samples. 2

2

Methods for Preparation of Specific Oxidation States of the Mn Complex I n m o s t r e d o x e n z y m e s , t h e d i f f e r e n t o x i d a t i o n states o f a m e t a l c e n t e r can be p r o d u c e d by poising the ambient redox potential of the sample. H o w e v e r , t h e i n t e r m e d i a t e o x i d a t i o n states o f t h e M n c o m p l e x i n P S I I have v e r y h i g h r e d u c t i o n potentials (in the range o f 0 . 8 - 1 . 2 V vs. the


252


n o r m a l h y d r o g e n e l e c t r o d e ) . T o d a t e , it has n o t b e e n p o s s i b l e t o c a r r y out a redox titration of any of the species on the o x i d i z i n g side of PSII. T h e r e f o r e , o n e m u s t use p h o t o c h e m i c a l m e t h o d s t h a t a l l o w t h e c o n t r o l l e d t u r n o v e r o f P S I I t o p r e p a r e a s p e c i f i c o x i d a t i o n state o f t h e M n c o m p l e x . A k e y t o t h e s u c c e s s o f p h o t o c h e m i c a l m e t h o d s is t h e p r e p a r a t i o n o f a n i n i t i a l l y h o m o g e n e o u s S state. D a r k adaptation w i l l p r o d u c e a sample that contains p r i m a r i l y the S i state. T h e S a n d S states a r e u n s t a b l e a n d d e c a y b a c k t o t h e S state i n t h e d a r k ( e q u a t i o n 2). T h e S state also d e c a y s t o t h e S i state i n t h e dark via a redox reaction w i t h the oxidized tyrosine residue, Y " (equation 3): 2

3

x

0


D

S

0

+ Y

D

-^Sx + Y

(3)

D

H o w e v e r , t h e r e a c t i o n o f t h e S state w i t h Y ' is f a i r l y s l o w (tens o f m i n u t e s (JO)) a n d , d e p e n d i n g o n t h e p r i o r h i s t o r y o f i l l u m i n a t i o n o f t h e sample, Y * may not be present i n all of the PSII centers. T h e r e f o r e , the i n i t i a l y i e l d o f t h e S state c a n b e m a x i m i z e d b y g i v i n g a p r e v i o u s l y d a r k a d a p t e d s a m p l e o n e flash (or c o n t i n u o u s i l l u m i n a t i o n at 2 0 0 K ; see s u b sequent paragraphs) before further dark adaptation. These illuminations w i l l c a u s e t h e o x i d a t i o n o f S t o S o r Y t o Y °; a n y S state p r o d u c e d b y t h e i l l u m i n a t i o n w i l l d e c a y b a c k t o t h e S i state i n t h e d a r k . 0

D

D

x

0

x

D

D

2

O n c e a h o m o g e n e o u s i n i t i a l S-state p o p u l a t i o n is p r o d u c e d , it is p o s s i b l e t o a d v a n c e t h e S states s y n c h r o n o u s l y b y u s i n g s h o r t , s a t u r a t i n g flashes o f l i g h t (as s h o w n i n F i g u r e 1). F o r s a m p l e s t h a t a r e s u f f i c i e n t l y d i l u t e o r h a v e a v e r y s h o r t p a t h l e n g t h , flashes w o r k w e l l f o r p r e p a r i n g e a c h o f t h e S states. P r o v i d e d t h a t t h e s a m p l e is d a r k a d a p t e d t o e n s u r e t h a t t h e i n i t i a l S state is h o m o g e n e o u s , t h e S , S , o r S state c a n b e g e n e r a t e d b y u s i n g o n e , t w o , o r t h r e e flashes, r e s p e c t i v e l y . U n f o r t u n a t e l y , t u r n o v e r c o n t r o l o f P S I I is m o r e c o m p l i c a t e d t h a n t h e a b o v e d e s c r i p t i o n w o u l d i n d i c a t e . B e c a u s e t u r n o v e r o f t h e S states is a c h i e v e d v i a a p h o t o c h e m i c a l r e a c t i o n , t h e y i e l d o f t h e r e a c t i o n d e pends on both the electron donors and the electron acceptors. T h e overa l l p i c t u r e o f e l e c t r o n t r a n s f e r i n P S I I is s h o w n i n F i g u r e 2 (11). L i g h t i n d u c e s a series o f electron-transfer reactions that l e a d to the f o r m a t i o n o f p r o g r e s s i v e l y m o r e s t a b l e c h a r g e - s e p a r a t e d states. T h e d o m i n a n t r e action u n d e r p h y s i o l o g i c a l c o n d i t i o n s leads to a one-step a d v a n c e m e n t o f t h e S state a n d r e d u c t i o n o f t h e s e c o n d a r y q u i n o n e e l e c t r o n a c c e p t o r ( Q ) . I n p u r i f i e d P S I I p r e p a r a t i o n s , h o w e v e r , the q u i n o n e s are d e p l e t e d a n d t h e Q site w i l l m o s t l y b e u n o c c u p i e d u n l e s s e x o g e n o u s q u i n o n e s are a d d e d . I n flashing l i g h t , t h e r e are l i m i t a t i o n s o n t h e m i n i m u m a n d m a x i m u m t i m e s b e t w e e n flashes. T h e r a t e - l i m i t i n g s t e p i n t u r n o v e r o f P S I I is e x c h a n g e o f q u i n o n e f o r q u i n o l , w h i c h o c c u r s at t h e Q site. C o n s e q u e n t l y , the electron acceptors w i l l produce a bottleneck i f the time b e t w e e n x

2

3

0

B

B

B


9.


BRUDVIG

253

P680*

-0.5 r-

Pheo

^ PQ

0.0

PQH


2

hv (680 nm)

0.5 2H 0 2

1.0 4H + o +

P680

2

1.2

E , 7 (V) m

Figure 2. Paths of electron transfer in PSII: P680, reaction-center chlorophyll that functions as the primary electron donor; P680*,firstexcited singlet state ofP680; Pheo, pheophytin; Q , primary quinone electron acceptor; Q , secondary quinone electron acceptor; cyt b , cytochrome b ; Chl , redoxactive chlorophyll that mediates electron transfer between cytochrome b and P680; Y , redox-active tyrosine that gives rise to the dark-stable tyrosine radical; Y , redox-active tyrosine that mediates electron transfer from the Mn complex to P680. A

B

559

559

z

559

D

z

flashes is s h o r t e r t h a n a b o u t 1 0 m s . O n t h e o t h e r h a n d , t h e t i m e b e t w e e n flashes c a n n o t b e t o o l o n g b e c a u s e t h e S a n d S states a r e u n s t a b l e a n d d e c a y o n a t i m e scale o f seconds, e i t h e r b y c h a r g e r e c o m b i n a t i o n o r b y oxidizing cytochrome b o r Y (11). T h e t i m e scales o f t h e s e r e a c t i o n s l e a v e o p e n a w i n d o w o f t i m e b e t w e e n flashes f o r w h i c h t h e t u r n o v e r o f t h e S states is o p t i m a l , a l t h o u g h " m i s s e s " o n t h e o r d e r o f 5 - 1 0 % p e r flash a r e u n a v o i d a b l e . 2

5 5 9

3

D


254


α

DCMU

Ο

,

HhO"

O-NDownloaded by SUNY STONY BROOK on October 31, 2014 | http://pubs.acs.org Publication Date: May 5, 1996 | doi: 10.1021/ba-1995-0246.ch009

>

Chloroxuron

ο

N

—'

ΝΗ

1

1 Figure 3.

Ν:

2

Structures of herbicides that bind to the Q site in PSII. B

O n e s i g n i f i c a n t d r a w b a c k o f u s i n g flashes t o a d v a n c e t h e S s t a t e s is t h a t t h e s a m p l e m u s t b e v e r y d i l u t e o r t h e p a t h l e n g t h m u s t b e v e r y short to a l l o w s a t u r a t i n g l i g h t to p e n e t r a t e t h r o u g h o u t the s a m p l e . (A t y p i c a l P S I I m e m b r a n e p r e p a r a t i o n has a b o u t 2 0 0 c h l o r o p h y l l s p e r P S I I (12), w h i c h m e a n s t h a t a s a m p l e c o n t a i n i n g 5 0 μ Μ P S I I h a s an o p t i c a l density of 5 0 - 1 0 0 0 t h r o u g h o u t the v i s i b l e spectrum.) E P R a n d e x t e n d e d X - r a y a b s o r p t i o n fine s t r u c t u r e ( E X A F S ) m e a s u r e m e n t s require a relatively large volume of concentrated sample. In such s a m p l e s , flashes a r e n o t e f f e c t i v e t o p r o d u c e a h i g h y i e l d o f t h e S , S , or S states. F o r t u n a t e l y , the e l e c t r o n - a c c e p t o r side o f P S I I can b e e x p l o i t e d to a l l o w t u r n o v e r c o n t r o l o f t h e S states i n h i g h l y c o n c e n t r a t e d s a m p l e s . A n u m b e r o f h e r b i c i d e s a r e k n o w n t h a t b i n d t i g h t l y t o t h e Q site a n d b l o c k e l e c t r o n t r a n s f e r past t h e p r i m a r y q u i n o n e e l e c t r o n a c c e p t o r ( Q ) (13). S o m e e x a m p l e s a r e s h o w n i n F i g u r e 3. E q u a t i o n s 4 a n d 5 s h o w the reactions of PSII i n the presence of 3 - ( 3 , 4 - d i c h l o r o p h e n y l ) - l , l - d i m e t h y l u r e a ( D C M U , F i g u r e 3). 2

3

0

B

A

SIQAQB + D C M U

τ± S j Q

A

D C M U

+

(4)

PQ

continuous illumination

SJQADCMU

S Q -DCMU 2

(5)

A

Q c a n o n l y a c c e p t a s i n g l e e l e c t r o n a n d , at l o w t e m p e r a t u r e , t h e S Q ~ c h a r g e s e p a r a t i o n is s t a b l e . B e c a u s e P S I I is r e s t r i c t e d t o o n l y o n e t u r n over b y D C M U , c o n t i n u o u s l i g h t can be u s e d to p r o d u c e a single charge s e p a r a t i o n (14). T h e s a m p l e c a n b e i l l u m i n a t e d f o r as l o n g as n e c e s s a r y to achieve a charge separation i n e v e r y P S I I c o m p l e x . E l e c t r o n transfer A

2


A

9.

BRUDVIG

255


f r o m Q ~ to Q is also b l o c k e d at t e m p e r a t u r e s at o r b e l o w 2 0 0 K . T h e r e f o r e , i l l u m i n a t i o n o f a d a r k - a d a p t e d s a m p l e at 2 0 0 Κ w i l l p r o d u c e t h e S state, e v e n w i t h o u t a d d i n g D C M U (15). T h e s e m e t h o d s h a v e b e e n e x t e n s i v e l y u s e d to p r o d u c e t h e S state f o r E P R o r E X A F S s t u d i e s . A

B

2

2

T h i s p r o t o c o l has b e e n e x t e n d e d t o p r o d u c e t h e S state b y u s i n g t h e r e d o x - a c t i v e h e r b i c i d e s 1 a n d 2 ( F i g u r e 3) (16). I n t h i s case, t w o s e q u e n t i a l c h a r g e - s e p a r a t i o n r e a c t i o n s o c c u r as s h o w n i n e q u a t i o n 6: 3


SiQJlR'NO + H

continuous

continuous

illumination

illumination

> S Q RR'NOH

+

2

A

,

> S Q ~RR'NOH 3

A

v

(6)

w h e r e R a n d R' are the groups b o u n d to the n i t r o x y l g r o u p of m o l e c u l e 1 o r 2 ( F i g u r e 3). T h e first c h a r g e s e p a r a t i o n r e s u l t s i n a o n e - e l e c t r o n r e d u c t i o n of the nitroxyl group of the h e r b i c i d e a n d the second results in the one-electron reduction of Q . B y using the redox-active herbicide, 2 , a n d c o n t i n u o u s i l l u m i n a t i o n at 2 5 0 K , a y i e l d o f t h e S state o f a b o u t 8 0 % w a s a c h i e v e d w h i c h is s i m i l a r t o w h a t is o b t a i n e d b y u s i n g flashes and more dilute samples. A

3

EPR Spectroscopic Studies of the Si and S States 2

T h e t w o S states that c a n b e p r o d u c e d m o s t r e a d i l y i n h i g h c o n c e n t r a t i o n a r e t h e Sx a n d S states. C o n s e q u e n t l y , t h e s e t w o states h a v e b e e n m o s t a c c e s s i b l e to s p e c t r o s c o p i c s t u d y . I n g e n e r a l , o n e e x p e c t s t o o b s e r v e a n E P R signal from a transition metal complex w h e n e v e r the complex pos sesses a n o d d n u m b e r o f u n p a i r e d e l e c t r o n s . I f t h e c o m p l e x possesses an e v e n n u m b e r o f u n p a i r e d e l e c t r o n s , E P R s i g n a l s a r e o f t e n u n d e t e c t a b l e w i t h c o n v e n t i o n a l i n s t r u m e n t a t i o n d u 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 . B e c a u s e e a c h S-state t r a n s i t i o n i n v o l v e s t h e r e m o v a l o f o n e e l e c t r o n f r o m t h e 0 - e v o l v i n g c e n t e r , a l t e r n a t e S states w i l l h a v e a n o d d n u m b e r o f e l e c t r o n s . T h e s e o d d - e l e c t r o n S states s h o u l d , i n p r i n c i p l e , b e d e t e c t a b l e b y E P R s p e c t r o s c o p y . T h e S state is a n o d d - e l e c t r o n state a n d e x h i b i t s a n u m b e r o f E P R s i g n a l s f r o m t h e M n c o m p l e x ( F i g u r e 4; f o r r e v i e w s , see r e f e r e n c e s 4 a n d 1 7 ) . A l t h o u g h t h e Si state is a n e v e n e l e c t r o n state, r e c e n t r e s u l t s i n d i c a t e t h a t it c a n exist i n a p a r a m a g n e t i c f o r m t h a t c a n b e s t u d i e d b y E P R s p e c t r o s c o p y (18, 19). 2

2

2

EPR Studies of the S 2 State. T w o t y p e s o f E P R s i g n a l s h a v e b e e n o b s e r v e d f r o m t h e S state ( F i g u r e 4). T h e first is a m u l t i l i n e E P R s i g n a l c e n t e r e d at a b o u t g = 2 ( F i g u r e 4a). T h i s E P R s i g n a l arises f r o m a n S = V2 state o f a m u l t i n u c l e a r M n c o m p l e x ; t h e h y p e r f i n e l i n e s a r i s e f r o m t h e c o u p l i n g o f t h e u n p a i r e d e l e c t r o n to t h e n u c l e a r s p i n s o f s e v e r a l M n i o n s ( e a c h M n i o n has I = % ) . T h e s e c o n d E P R s i g n a l f r o m t h e S state e x h i b i t s a t u r n i n g p o i n t at g = 4.1 ( F i g u r e 4 b ) . T h e g = 4.1 E P R s i g n a l c a n b e i n d u c e d b y i l l u m i n a t i o n at 1 3 0 Κ i n u n t r e a t e d s a m p l e s , 2

5 5

5 5

2


256



500 G

Figure 4. S state EPR spectra, (a) Multiline EPR signal produced by il lumination at 200 K. (b) g = 4.1 EPR signal produced by illumination at 130 K. (Reproduced from reference 45. Copyright 1988 American Chemical Society.) 2

b u t is u n s t a b l e a n d is c o n v e r t e d i n t o t h e m u l t i l i n e E P R s i g n a l u p o n w a r m i n g t o 2 0 0 K . A n u m b e r o f t r e a t m e n t s s u c h as t h e a d d i t i o n o f s u crose, ammonia, or fluoride; depletion of chloride; or replacement of Ca by S r c a u s e t h e g = 4.1 E P R s i g n a l t o b e s t a b i l i z e d at 2 0 0 Κ ( r e v i e w e d i n r e f e r e n c e 4). I n u n t r e a t e d s a m p l e s , t h e g = 4.1 E P R s i g n a l does not exhibit r e s o l v e d M n hyperfine structure. H o w e v e r , in am m o n i a - t r e a t e d samples that are o r i e n t e d b y d r y i n g onto M y l a r sheets, t h e g = 4.1 E P R s i g n a l e x h i b i t s r e s o l v e d M n h y p e r f i n e s t r u c t u r e (20), i n d i c a t i n g t h a t t h i s E P R s i g n a l also arises f r o m a m u l t i n u c l e a r M n c o m p l e x . A v a r i e t y o f m o d i f i e d f o r m s o f t h e m u l t i l i n e a n d g = 4.1 E P R signals h a v e b e e n o b s e r v e d a f t e r t h e a d d i t i o n o f v a r i o u s e x o g e n o u s m o l ecules i n c l u d i n g amines and fluoride or b y depletion of C a and re placement by S r . 2 +

2 +

5 5

5 5

2 +

2 +

T h e S - s t a t e m u l t i l i n e a n d g = 4.1 E P R signals 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 o n the structure a n d organization of the M n ions i n the O E C . H o w e v e r , t h e a s s i g n m e n t o f t h e s e signals is s t i l l n o t f u l l y r e s o l v e d , although recent results have significantly l i m i t e d the range of possibil ities. O r i g i n a l l y , t w o interpretations of the i d e n t i t y of the species that g i v e r i s e to t h e m u l t i l i n e a n d g = 4.1 E P R signals w e r e p r o p o s e d . 2

H a n s s o n et a l . (21) p r o p o s e d t h a t t h e t w o E P R s i g n a l s a r i s e f r o m distinct M n centers: an antiferromagnetically exchange-coupled m i x e d v a l e n c e b i n u c l e a r M n c e n t e r g i v i n g t h e m u l t i l i n e E P R s i g n a l f r o m its


9.

BRUDVIG

257


g r o u n d S = V2 state a n d a m o n o n u c l e a r h i g h - s p i n M n center giving the g = 4.1 E P R s i g n a l f r o m t h e S = % state w i t h a x i a l s y m m e t r y . T h i s p r o p o s a l f o l l o w e d f r o m t h e s i m i l a r i t y o f t h e m u l t i l i n e a n d g = 4.1 E P R signals to t h o s e o f b i n u c l e a r M n - M n and mononuclear M n model complexes, respectively. T h e interconversion of the S -state multiline a n d g = 4.1 E P R signals w a s e x p l a i n e d b y a r e d o x e q u i l i b r i u m b e t w e e n the binuclear and mononuclear centers. I V

m

I

V

I V


2

d e P a u l a et a l . (22, 23) p r o p o s e d t h a t b o t h t h e m u l t i l i n e a n d g = 4.1 E P R signals a r i s e f r o m t h e s a m e t e t r a n u c l e a r M n c o m p l e x . T h e m u l t i l i n e a n d g = 4.1 E P R signals w e r e a t t r i b u t e d t o t w o c o n f o r m a t i o n s o f t h e complex having different exchange couplings b e t w e e n the M n ions. T h i s p r o p o s a l w a s m a d e b y a n a l o g y t o t h e S = V2 a n d S = % f o r m s t h a t h a v e b e e n o b s e r v e d for F e S c u b a n e l i k e clusters. B a s e d o n this analogy a n d on studies of the t e m p e r a t u r e d e p e n d e n c e of the t w o E P R signals, the m u l t i l i n e a n d g = 4.1 E P R s i g n a l s w e r e p r o p o s e d t o a r i s e f r o m a n e x c i t e d S = V2 state a n d a g r o u n d S = % state o f a n e x c h a n g e - c o u p l e d M n tetramer, respectively. 4

4

M o r e recent studies have clarified the assignments of the S -state m u l t i l i n e a n d g = 4.1 E P R s i g n a l s . S t u d i e s o f t h e t e m p e r a t u r e d e p e n d e n c e of the m u l t i l i n e E P R signal have s h o w n that the signal follows C u r i e - l a w t e m p e r a t u r e d e p e n d e n c e f r o m 1.4 t o 2 0 Κ (24, 2 5 ) . T h e s e results, w h i c h w e r e p r o d u c e d i n our lab, are best e x p l a i n e d i f the m u l t i l i n e E P R s i g n a l arises f r o m a n S = V2 g r o u n d state. T h e e a r l i e r r e s u l t s o f d e P a u l a et a l . (23, 26), i n d i c a t i n g t h a t t h e m u l t i l i n e E P R s i g n a l c a m e f r o m a n e x c i t e d state, w e r e a r t i f a c t u a l b e c a u s e o f m i c r o w a v e p o w e r s a t u r a t i o n . A n S = V2 g r o u n d state c o u l d a r i s e f r o m a n e x c h a n g e - c o u p l e d mixed-valence M n d i m e r , t r i m e r , or tetramer. These possibilities have b e e n c o m p a r e d b y E P R s p e c t r a l s i m u l a t i o n s (27). T h e b r e a d t h o f t h e m u l t i l i n e E P R s i g n a l is o n l y a c c o u n t e d f o r b y a M n t e t r a m e r , i f o n e assumes t h a t t h e S state c o n t a i n s o n l y M n a n d M n ions w i t h o u t large magnetic anisotropy. 2

2

m

I V

T h e S - s t a t e g = 4.1 E P R s i g n a l w a s o r i g i n a l l y a s s u m e d (21-23) to arise f r o m the p e r p e n d i c u l a r c o m p o n e n t o f an axially s y m m e t r i c S = % state b a s e d o n t h e p o s i t i o n o f t h e E P R r e s o n a n c e . H o w e v e r , m e a s u r e m e n t s o f t h e g = 4.1 E P R s i g n a l at s e v e r a l m i c r o w a v e f r e q u e n c i e s (28) s u p p o r t s a n a s s i g n m e n t o f t h e g = 4.1 s i g n a l t o t h e m i d d l e K r a m e r s d o u b l e t o f a n S = % state w i t h n e a r - r h o m b i c s y m m e t r y . T h e o r i e n t a t i o n 2

d e p e n d e n c e o f t h e g = 4.1 E P R s i g n a l has also b e e n m e a s u r e d i n P S I I m e m b r a n e s a m p l e s t h a t h a v e b e e n o r i e n t e d b y d r y i n g o n t o m y l a r sheets (20, 29). T h e o b s e r v a t i o n o f a least 1 6 h y p e r f i n e l i n e s o n t h e g = 4.1 E P R signal from oriented, ammonia-treated PSII membranes requires, w i t h r e a s o n a b l e a s s u m p t i o n s , t h a t t h e g = 4.1 s i g n a l o r i g i n a t e s f r o m a c l u s t e r o f at least t h r e e M n i o n s . T h i s r e s u l t , t o g e t h e r w i t h t h e r e q u i r e m e n t t h a t t h e S - s t a t e m u l t i l i n e E P R s i g n a l m u s t also a r i s e f r o m a c l u s t e r 2


258


o f at least t w o M n i o n s , p r o v i d e s s t r o n g s u p p o r t f o r t h e p r o p o s a l t h a t b o t h t h e g = 4.1 a n d m u l t i l i n e E P R s i g n a l s a r i s e f r o m t h e s a m e M n cluster. T h e r e m a i n i n g q u e s t i o n is w h e t h e r t h e r e d o x - a c t i v e c e n t e r o b s e r v e d b y E P R i n t h e S state is a t r i n u c l e a r o r t e t r a n u c l e a r M n c l u s t e r . I f t h e g = 4.1 a n d m u l t i l i n e E P R s i g n a l s b o t h a r i s e f r o m a t r i n u c l e a r c l u s t e r , t h e n the r e m a i n i n g M n i o n w o u l d have to b e M n i n b o t h the S a n d S states to e s c a p e E P R d e t e c t i o n . H o w e v e r , r e c e n t E P R s p i n r e l a x a t i o n s t u d i e s h a v e s h o w n t h a t t h e M n c l u s t e r is d i a m a g n e t i c i n t h e S r e s t i n g state [(19), see S t r u c t u r e o f t h e M a n g a n e s e C o m p l e x . ] . B e c a u s e a n i s o lated M n i o n w o u l d be paramagnetic, this result rules out the possibility t h a t t h e f o u r M n i o n s i n P S I I a r e a r r a n g e d as a t r i m e r p l u s a m o n o m e r . O n e is left w i t h t h e c o n c l u s i o n f r o m t h e E P R s t u d i e s t h a t t h e M n i o n s i n PSII are o r g a n i z e d into an e x c h a n g e - c o u p l e d tetranuclear c o m p l e x . 2

m

x

2


x

m

EPR Studies of the S x State. T h e S i state is a n e v e n - e l e c t r o n state. I n s u c h a n i n t e g e r - s p i n s y s t e m , it is o f t e n t h e case t h a t l a r g e z e r o field s p l i t t i n g s p r e v e n t t h e o b s e r v a t i o n o f c o n v e n t i o n a l E P R s i g n a l s . A l t h o u g h no c o n v e n t i o n a l E P R signals have b e e n o b s e r v e d f r o m the S state, t w o a p p r o a c h e s h a v e b e e n u s e d t o s t u d y t h e S state b y E P R s p e c troscopy. A n u m b e r of papers have b e e n p u b l i s h e d on the spin relaxation e n h a n c e m e n t o f t h e s t a b l e t y r o s i n e r a d i c a l , Y * , b y t h e M n c l u s t e r (19, 30-33). These studies p r o v i d e information on the magnetic properties o f t h e M n c l u s t e r . A n o t h e r a p p r o a c h is t o u s e p a r a l l e l - m o d e E P R s p e c t r o s c o p y , w h i c h selects f o r s o - c a l l e d " A m = 2 " a n d " A m = 4 " t r a n s i t i o n s o f i n t e g e r - s p i n s y s t e m s (34). A n i n t e g e r - s p i n E P R s i g n a l at g = 4 . 8 has b e e n r e p o r t e d a n d a s s i g n e d t o M n i n t h e Si state (18). Y

Y

D

s

s

T h e M n c o m p l e x has b e e n f o u n d t o e n h a n c e m a r k e d l y t h e s p i n lattice relaxation rate of the stable tyrosine radical, Y \ C o n s e q u e n t l y , t h e s p i n - l a t t i c e r e l a x a t i o n r a t e o f Y * c a n s e r v e as a p r o b e o f t h e m a g n e t i c p r o p e r t i e s o f t h e M n c o m p l e x i n e a c h o f t h e S states. A d e t a i l e d s t u d y o f t h e Si state w a s r e p o r t e d (19). It w a s f o u n d t h a t t h e S state c a n exist i n t w o f o r m s w i t h v e r y d i f f e r e n t m a g n e t i c p r o p e r t i e s : a r e s t i n g state o r a n a c t i v e state, d e p e n d i n g o n w h e t h e r t h e s a m p l e w a s s u b j e c t e d to l o n g (4 h) o r s h o r t (6 m i n ) p e r i o d s o f d a r k a d a p t a t i o n at 0 ° C , r e s p e c t i v e l y . T h e Si r e s t i n g state has a d i a m a g n e t i c g r o u n d state. I n a d d i t i o n , f r o m the temperature d e p e n d e n c e of the spin-lattice relaxation rate enhancem e n t , it w a s f o u n d t h a t a p a r a m a g n e t i c e x c i t e d state is p o p u l a t e d at higher temperatures. H o w e v e r , the splitting between the ground and e x c i t e d state is v e r y l a r g e (at least 1 0 0 c m " ) , i n d i c a t i n g t h a t t h e M n ions are strongly 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 i n the S resti n g state. T h e S a c t i v e state has a p a r a m a g n e t i c g r o u n d o r l o w - l y i n g e x c i t e d state b e c a u s e its s p i n - l a t t i c e r e l a x a t i o n r a t e e n h a n c e m e n t o f Y w a s s i g n i f i c a n t e v e n at 4 K . T h e d i f f e r e n t m a g n e t i c p r o p e r t i e s o f t h e Si D

D

2

1

x

x

D


e

9.

BRUDVIG


259

a c t i v e a n d r e s t i n g states c a n b e e x p l a i n e d b y t w o c o n f o r m a t i o n s o f t h e M n c o m p l e x that have different exchange c o u p l i n g s b e t w e e n the M n i o n s , as has also b e e n i n v o k e d t o e x p l a i n t h e d i f f e r e n t f o r m s o f t h e S state. D e x h e i m e r a n d K l e i n (18) h a v e r e p o r t e d a n i n t e g e r - s p i n E P R s i g n a l at g = 4.8 f r o m t h e S i state i n l o n g d a r k - a d a p t e d P S I I m e m b r a n e s . T h e s e d a r k - a d a p t e d s a m p l e s w o u l d b e e x p e c t e d to b e i n t h e S r e s t i n g state, w h i c h w a s f o u n d to b e d i a m a g n e t i c (19) a n d s h o u l d n o t e x h i b i t a n y E P R signals. H o w e v e r , the p a r a l l e l - m o d e E P R signal was v e r y w e a k ; this w e a k n e s s c o u l d b e e x p l a i n e d i f t h e s i g n a l arises f r o m a s m a l l a m o u n t o f t h e S i a c t i v e state i n t h e l o n g d a r k - a d a p t e d s a m p l e s . T o a d d r e s s t h e question of the origin of the parallel-mode E P R signal r e p o r t e d b y D e x h e i m e r a n d K l e i n (18), w e a t t e m p t e d t o m e a s u r e t h i s s i g n a l i n b o t h S active-state a n d S i resting-state PSII m e m b r a n e samples. M e a s u r e m e n t s w e r e m a d e b y u s i n g c o n v e n t i o n a l p e r p e n d i c u l a r - m o d e E P R (19) a n d also b y u s i n g p a r a l l e l - m o d e E P R ( D . K o u l o u g l i o t i s a n d G . B r u d v i g , Y a l e University; M . H e n d r i c k , U n i v e r s i t y of M i n n e s o t a , u n p u b l i s h e d results). W e d i d n o t o b s e r v e a n y E P R s i g n a l at g = 4 . 8 , o r o t h e r s i g n a l s i n t h e scans f r o m 0 t o 5 0 0 0 G t h a t c o u l d b e a t t r i b u t e d t o t h e S i state. 2


x

x

Structure of the Manganese Complex O n t h e basis o f t h e E P R s t u d i e s d e s c r i b e d i n t h e p r e v i o u s p a r a g r a p h s , t h e M n ions i n t h e O E C a r e d e t e r m i n e d to b e o r g a n i z e d i n t o a n e x c h a n g e c o u p l e d tetranuclear cluster. T h e exchange interactions b e t w e e n the M n ions m u s t b e v a r i a b l e to a c c o u n t f o r t h e d i f f e r e n t t y p e s o f E P R signals t h a t h a v e b e e n o b s e r v e d f r o m t h e S state a n d t h e d i f f e r e n t m a g n e t i c p r o p e r t i e s o f t h e S a c t i v e a n d r e s t i n g states. A l t h o u g h t h e m a g n i t u d e s of the exchange interactions b e t w e e n the M n ions are not w e l l - d e f i n e d b y the E P R studies, these c o u p l i n g s must b e large e n o u g h to p r o d u c e a s p l i t t i n g b e t w e e n t h e g r o u n d a n d first e x c i t e d s p i n states o f o v e r 1 0 0 cm i n t h e S r e s t i n g state (19) a n d a p p r o x i m a t e l y 3 0 c m " i n t h e m u l t i l i n e f o r m o f t h e S state (21). T h e s t r u c t u r e s f o r t h e M n c l u s t e r t h a t are c o n s i d e r e d must account for such large exchange interactions b e t w e e n the M n ions. 2

x

- 1

1

x

2

T h e m a g n e t i c p r o p e r t i e s o f t h e S r e s t i n g state p l a c e a s i g n i f i c a n t restriction on the possible structures of the M n complex. A mononuclear M n i o n is r u l e d o u t b y t h e o b s e r v a t i o n t h a t t h e S i r e s t i n g state has a d i a m a g n e t i c g r o u n d state; a m o n o n u c l e a r M n i o n is e x p e c t e d t o b e p a r a m a g n e t i c i n a n y o f its p o s s i b l e o x i d a t i o n states. T h i s l e a v e s o n l y t w o possible models for the o r g a n i z a t i o n of the M n ions i n the S i resting state. E i t h e r t h e M n i o n s a r e a r r a n g e d as a d i m e r - o f - d i m e r s i n w h i c h t h e M n i o n s i n e a c h d i m e r h a v e t h e s a m e o x i d a t i o n state a n d a r e s t r o n g l y antiferromagnetically e x c h a n g e - c o u p l e d , or the M n ions are a r r a n g e d x


260


as a t e t r a m e r i n w h i c h s t r o n g e x c h a n g e i n t e r a c t i o n s b e t w e e n t h e M n i o n s p r o d u c e a n e t s p i n o f z e r o i n t h e g r o u n d state. F u r t h e r i n f o r m a t i o n is a v a i l a b l e f r o m X - r a y a b s o r p t i o n structure

(XANES)

and

extended

X - r a y absorption

near-edge

fine

structure

( E X A F S ) s t u d i e s . F r o m analyses o f t h e M n X A N E S , it is p o s s i b l e to o b t a i n i n f o r m a t i o n o n t h e o x i d a t i o n states o f t h e M n i o n s . T h e M n X A N E S

of

t h e Si state h a v e b e e n a n a l y z e d b y s e v e r a l g r o u p s ( 3 5 - 3 9 ) . T h e r e s u l t s i n d i c a t e t h a t t h e Si state d o e s n o t c o n t a i n M n tains t w o M n

m

and two M n

I v

1 1

and most p r o b a b l y c o n

. A n alternate a p p r o a c h for assigning o x i


d a t i o n states i n v o l v e s a n a n a l y s i s o f m e t a l - l i g a n d b o n d l e n g t h s . A v e r a g e m e t a l - l i g a n d b o n d lengths for the M n ions i n P S I I have b e e n

obtained

f r o m E X A F S studies. T h e s e results have b e e n u s e d to calculate that the Si state has t w o M n

m

and two M n

I V

b y using the b o n d valence

sum

m e t h o d (40). T h u s , it s e e m s p r o b a b l e t h a t t h e o x i d a t i o n states o f t h e M n i o n s i n t h e Si state a r e Μ η

Π Ι

2

Μη

ι ν

2

. H o w e v e r , the analysis of the

X A N E S data and the b o n d valence sum m e t h o d both require a compar i s o n t o m o d e l c o m p l e x e s . B e c a u s e t h e l i g a t i o n o f t h e M n i o n s i n P S I I is n o t k n o w n , i t is also p o s s i b l e t h a t t h e S i state has f o u r M n

m

.

M n E X A F S data provide more detailed structural information. Sev eral groups have collected and analyzed M n E X A F S data from the S

x

state (35, 36, 38, 39). A l t h o u g h s o m e d i s a g r e e m e n t s r e m a i n , a c o n s e n s u s s e e m s t o b e e m e r g i n g o n s e v e r a l p o i n t s . P e r h a p s m o s t s i g n i f i c a n t is t h e o b s e r v a t i o n o f a M n b a c k s c a t t e r e r at a b o u t 2.7 À . S i m u l a t i o n s o f t h e E X A F S d a t a i n d i c a t e that e a c h M n a t o m has 1 - 1 . 5 n e i g h b o r i n g M n a t o m s at t h i s d i s t a n c e . T h i s d i s t a n c e is s i g n i f i c a n t b e c a u s e , t o d a t e , i t has o n l y b e e n o b s e r v e d i n m o d e l c o m p l e x e s h a v i n g άί-μ -οχο 2

o r άί-μ -οχο 3

bridges

b e t w e e n t w o M n i o n s (41). It s e e m s p r o b a b l e t h a t t w o o r t h r e e d i - μ - ο χ ο b r i d g e d M n u n i t s exist i n P S I I . A n o t h e r h e a v y - a t o m b a c k s c a t t e r e r has 2

b e e n i d e n t i f i e d at 3 . 3 À . It r e m a i n s u n c l e a r , h o w e v e r , b a c k s c a t t e r e r is a M n i o n , C a

2 +

w h e t h e r this

, or b o t h . B a s e d on these E X A F S data, a

d i m e r - o f - d i m e r s m o d e l f o r t h e M n c l u s t e r i n t h e Si state has b e e n p r o p o s e d (39) i n w h i c h t w o d i - μ - ο χ ο b r i d g e d M n d i m e r s ( e a c h h a v i n g a 2.7 À M n - M n separation) are c o n n e c t e d v i a a single μ-οχο b r i d g e (giving a 3.3 À separation b e t w e e n t w o of the M n ions). A l t e r n a t i v e l y , the E X A F S data could be explained b y a distorted cubane-like tetranuclear M n complex. T o c o m p a r e these t w o possibilities, one can consider the results of studies of M n m o d e l

complexes.

O n e i m p o r t a n t c o n s i d e r a t i o n is t h e t y p e o f s t r u c t u r e t h a t c o u l d p r o d u c e the strong antiferromagnetic exchange interactions n e e d e d to account for the magnetic p r o p e r t i e s o f the S i a n d S

2

states. T h e r e is a

substantial b o d y of data on the magnetic properties of binuclear M n c o m p l e x e s . It has b e e n o b s e r v e d t h a t d i - μ - ο χ ο b r i d g e d M n d i m e r s h a v e antiferromagnetic exchange couplings that decrease e x p o n e n t i a l l y w i t h the distance b e t w e e n the t w o M n ions; this c o u l d be e x p l a i n e d i f direct


9.

261


BRUDVIG

e x c h a n g e m a k e s a n i m p o r t a n t c o n t r i b u t i o n f o r t h e s e s t r u c t u r e s (41). A l l examples of di-μ-οχο b r i d g e d M n dimers have large antiferromagnetic e x c h a n g e i n t e r a c t i o n s . H o w e v e r , t h e r e a r e v e r y f e w e x a m p l e s o f di-μο χ ο b r i d g e d M n d i m e r s b e c a u s e t h e a b i l i t y o f M n t o s u p p o r t a di-μοχο l i g a t i o n r e q u i r e s that the ancillary ligands be p o o r donors. M a g n e t i c data are available o n l y for the [ M n 2 ( 0 ) 2 ( 6 - M e 2 b i s p i c e n ) 2 ] complex (42), w h i c h s h o w s f a i r l y s t r o n g a n t i f e r r o m a g n e t i c e x c h a n g e c o u p l i n g (J = 1 7 2 . 8 c m " , H = JSi · S ) . H o w e v e r , o t h e r di-μ-οχο b r i d g e d M n d i m e r s a r e also f o u n d as u n i t s i n h i g h e r n u c l e a r i t y M n c o m p l e x e s . I n s u c h sys tems for w h i c h magnetic studies have b e e n d o n e , the exchange c o u p l i n g between the M n i o n s is w e a k ( r e v i e w e d i n r e f e r e n c e 4 1 ) . T h e e x c h a n g e i n t e r a c t i o n s a r e also i n v a r i a b l y w e a k b e t w e e n M n i o n s t h a t a r e b r i d g e d b y groups other than the di-μ-οχο ligands. I V

m

m

n i


1

2 +

m

2

1 1 1

These results place some constraints on the d i m e r - o f - d i m e r s m o d e l . T o p r o d u c e t h e m a g n e t i c p r o p e r t i e s o f t h e S i r e s t i n g state w i t h a M n M n 2 system, one d i m e r should be M n and the other M n . If b o t h d i m e r s h a v e a d i - μ - ο χ ο b r i d g e d s t r u c t u r e , as i n d i c a t e d f r o m t h e E X A F S data, then the r e q u i r e d magnetic properties s h o u l d be present. H o w e v e r , the r e m a i n i n g ligands to the M n p a i r w o u l d have to b e p o o r donors to account for the stabilization o f the di-μ-οχο b r i d g e d structure at t h e M n o x i d a t i o n l e v e l . A c o m b i n a t i o n o f p o o r d o n o r l i g a n d s t o o n e p a i r of M n a n d stronger d o n o r ligands to the o t h e r p a i r c o u l d e x p l a i n t h e n e c e s s a r y a s y m m e t r i c a r r a n g e m e n t o f t h e o x i d a t i o n states a m o n g t w o M n d i m e r s . It is u n c l e a r , h o w e v e r , w h e t h e r a d i - μ - ο χ ο b r i d g e d M n d i m e r c o u l d be b r i d g e d to a M n d i m e r v i a a n o x o g r o u p as p r o p o s e d b y Y a c h a n d r a et a l . (39). T h i s w o u l d p l a c e t h r e e o x o l i g a n d s o n o n e M n , w h i c h w o u l d be unfavorable unless this M n w e r e less t h a n s i x c o o r d i n a t e o r w e r e c o o r d i n a t e d t o e s p e c i a l l y p o o r d o n o r l i g a n d s . It is also p o s s i b l e to e x p l a i n t h e d i f f e r e n t m a g n e t i c p r o p e r t i e s o f t h e S r e s t i n g a n d a c t i v e states w i t h a d i m e r - o f - d i m e r s m o d e l . A s m a l l c o n f o r m a t i o n a l change o f the O E C c o u l d cause the ligands to the M n p a i r to b e c o m e b e t t e r d o n o r ligands. T h i s c o u l d l e a d to p r o t o n a t i o n o f one o f the oxo bridges b e t w e e n the M n ions, w h i c h w o u l d greatly w e a k e n t h e i r ex c h a n g e c o u p l i n g a n d c o u l d g i v e r i s e t o a p a r a m a g n e t i c state. n i

2

m

I V

I V

2

2

m

m

m

I V

m

1 1 1

x

m

m

M u c h less i n f o r m a t i o n is a v a i l a b l e o n t h e m a g n e t i c p r o p e r t i e s o f o t h e r t e t r a n u c l e a r s t r u c t u r e s , s u c h as a d i s t o r t e d c u b a n e - l i k e s t r u c t u r e , that c o u l d account for the spectroscopic data of the O E C . A series o f d i s t o r t e d c u b a n e - l i k e h i g h - v a l e n t M n c o m p l e x e s h a v i n g a M n M n 3 0 C l core have been characterized (reviewed i n reference 41). T h e magnetic properties of the M n 0 3 C l 4 ( 0 C C H 3 ) ( p y ) 3 complex, w h i c h has C s y m m e t r y , h a v e b e e n a n a l y z e d i n d e t a i l (43). A l t h o u g h s u c h a c o m p l e x w i t h C s y m m e t r y c a n , i n p r i n c i p l e , h a v e a g r o u n d state w i t h a n y s p i n f r o m S = V2 t o S = / , d e p e n d i n g o n t h e v a l u e s o f t h e e x c h a n g e i n t e r a c t i o n s , t h e M n ^ C U ^ C C H s X p y ^ c o m p l e x has a I V

n i

3

4

2

3

3

15

2


262

MECHANISTIC BIOINORGANIC CHEMISTRY

ground state with S = %. This complex has an oxidation state that is equal to the probable oxidation state of the S state. Unfortunately, the magnetic properties of the S state are not well-characterized. Therefore, it is not possible to make a very definitive comparison between the model complex data and possible tetranuclear structures of the Mn complex in PSII. Further work to prepare and characterize new model complexes and to better characterize the magnetic properties of the S state is needed. 0

0

0


Acknowledgments I thank Dionysios Koulougliotis and Michael Hendrick for making the parallel-mode EPR measurements on PSII and Chao Lin for help with preparation of the figures. This work was supported by the National Institutes of Health (GM32715 and GM36442). References

1. Babcock, G. T. In New Comprehensive Biochemistry: Photosynthesis; Ame J., Ed.; Elsevier: Amsterdam, 1987; pp 125-158. 2. Andréasson, L.-E.; Vänngård, T. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1988, 39, 379-411. 3. Brudvig, G. W.; Beck, W. F.; de Paula, J. C. Annu. Rev. Biophys. Biophys. Chem. 1989, 18, 25-46. 4. Debus, R. J. Biochim. Biophys. Acta 1992, 1102, 269-352. 5. Rutherford, A. W.; Zimmermann, J.-L.; Boussac, A. In The Photosystems: Structure, Function and Molecular Biology; Barber, J., Ed.; Elsevier Science Publishers Β. V.: Cedex, France, 1992; pp 179-229. 6. Joliot, P.; Barbieri, G.; Chabaud, R. Photochem. Photobiol. 1969, 10, 309329. 7. Kok, B.; Forbush, B.; McGloin, M. Photochem. Photobiol. 1970, 11, 457475. 8. Forbush, B.; Kok, B.; McGloin, M. P. Photochem. Photobiol. 1971, 14, 307321. 9. Ono, T.-a.; Noguchi, T.; Inoue, Y.; Kusunoki, M.; Matsushita, T.; Oyanagi, H. Science (Washington, D.C.)1992, 258, 1335-1337. 10. Styring, S.; Rutherford, A. W. Biochemistry 1987, 26, 2401-2405. 11. Buser, C. Α.; Diner, Β. Α.; Brudvig, G. W. Biochemistry 1992, 31, 1144911459. 12. Berthold, D. Α.; Babcock, G. T.; Yocum, C. F. FEBS Lett. 1981, 134, 231234. 13. Draber, W.; Tietjen, K.; Kluth, J. F.; Trebst, A. Angew. Chem., Int. Ed. Engl. 1991, 30, 1621-1633. 14. Beck, W. F.; de Paula, J. C.; Brudvig, G. W. Biochemistry 1985, 24, 30353043. 15. Brudvig, G. W.; Casey, J. L.; Sauer, K. Biochim. Biophys. Acta 1983, 723, 366-371. 16. Bocarsly, J. R.; Brudvig, G. W. J. Am. Chem. Soc. 1992, 114, 9762-9767. 17. Miller, A.-F.; Brudvig, G. W. Biochim. Biophys. Acta 1991, 1056, 1-18. 18. Dexheimer, S. L.; Klein, M. P. J. Am. Chem. Soc. 1992, 114, 2821-2826.



9.

BRUDVIG


19. Koulougliotis, D.; Hirsh, D. J.; Brudvig, G. W. J. Am. Chem. Soc. 1992, 114, 8322-8323. 20. Kim, D. H.; Britt, R. D.; Klein, M. P.; Sauer, K. J. Am. Chem. Soc. 1990, 112, 9389-9391. 21. Hansson, Ö;. Aasa, R.; Vänngård, T. Biophys. J. 1987, 51, 825-832. 22. de Paula, J. C.; Innes, J. B.; Brudvig, G. W. Biochemistry 1985, 24, 81148120. 23. de Paula, J. C.; Beck, W. F.; Brudvig, G. W. J. Am. Chem. Soc. 1986, 108, 4002-4009. 24. Aasa, R.; Andréasson, L.-E.; Lagenfelt, G.;Vänngård,T. FEBSLett.1987, 221, 245-248. 25. Britt, R. D.; Lorigan, G. Α.; Sauer, Κ.; Klein, M. P.; Zimmermann, J.-L. Biochim. Biophys. Acta 1992, 1040, 95-101. 26. de Paula, J. C.; Brudvig, G. W. J. Am. Chem. Soc. 1985, 107, 2643-2648. 27. Bonvoisin, J.; Blondin, G.; Girerd, J.-J.; Zimmermann, J.-L. Biophys. J. 1992, 61, 1076-1086. 28. Vänngård, T.; Hansson, Ö.; Haddy, A. In Manganese Redox Enzymes; Pecoraro, V. L., Ed.; VCH Publishers: New York, 1992; pp 105-118. 29. Rutherford, A. W. Biochim. Biophys. Acta 1985, 807, 189-201. 30. Styring, S.; Rutherford, A. W. Biochemistry 1988, 27, 4915-4923. 31. Innes, J. B.; Brudvig, G. W. Biochemistry 1989, 28, 1116-1125. 32. Evelo, R. G.; Styring, S.; Rutherford, A. W.; Hoff, A. J. Biochim. Biophys. Acta 1989, 973, 428-442. 33. Beck, W. F.; Innes, J. B.; Brudvig, G. W. In Current Research in Photosynthesis; Baltscheffsky, M., Ed.; Kluwer Academic Publishers: Dordrecht, 1990; pp 817-820. 34. Hendrick, M. P.; Debrunner, P. G. J. Magn. Reson. 1988, 78, 133-141. 35. George, G. Ν.; Prince, R. C.; Cramer, S. P. Science (Washington, D.C.) 1989, 243, 789-791. 36. Penner-Hahn, J. E.; Fronko, R. M.; Pecoraro, V. L.; Yocum, C. F.; Betts, S. D.; Bowlby, N. R. J. Am. Chem. Soc. 1990, 112, 2549-2557. 37. Kusunoki, M.; Ono, T.; Matsushita, T.; Oyanagi, H.; Inoue, Y.J.Biochem. 1990, 108, 560-567. 38. MacLachlan, D. J.; Hallahan, B. J.; Ruffle, S. V.; Nugent, J. H. Α.; Evans, M. C. W.; Strange, R. W.; Hasnain, S. S. J. Biochem. 1992, 285, 569-576. 39. Yachandra, V. K.; DeRose, V. J.; Latimer, M. J.; Mukerji, I.; Sauer, K.; Klein, M. P. Science (Washington, D.C.)1993, 260, 675-679. 40. Thorp, H. H. Inorg. Chem. 1992, 31, 1585-1588. 41. Thorp, H. H.; Brudvig, G. W. New J. Chem. 1991, 15, 479-490. 42. Goodson, P. Α.; Oki, A. R.; Glerup, J.; Hodgson, D. J. J. Am. Chem. Soc. 1990, 112, 6248-6254. 43. Schmitt, Ε. Α.; Noodleman, L.; Baerends, E. J.; Hendrickson, D. N.J.Am. Chem. Soc. 1992, 114, 6109-6119. 44. Lin, C.; Brudvig, G. W. Photosynth. Res. 1993, 38, 441-448. 45. Brudvig, G. W. In Metal Clusters in Proteins; Que, L., Jr., Ed.; ACS Sym posium Series 372; American Chemical Society: Washington, DC, 1988; pp 221-237. RECEIVED

for review August 11, 1993. ACCEPTED revised manuscript December

27, 1993.


26

Mechanistic Bioinorganic Chemistry - American Chemical Society

Recommend Documents