Metal oxidation states in biological water splitting

• A central question in biological water splitting concerns the oxidation states of the manganese ions that comprise the oxygen-evolving complex of photosystem II. Understanding the nature and order of oxidation events that occur during the catalytic cycle of five Si states (i = 0-4) is of fundamental importance both for the natural system and for artificial water oxidation catalysts. Despite the widespread adoption of the so-called "high-valent scheme"-where, for example, the Mn oxidation states in the S-2 state are assigned as III, IV, IV, IV-the competing "low-valent scheme" that differs by a total of two metal unpaired electrons (i.e. III, III, III, IV in the S-2 state) is favored by several recent studies for the biological catalyst. The question of the correct oxidation state assignment is addressed here by a detailed computational comparison of the two schemes using a common structural platform and theoretical approach. Models based on crystallographic constraints were constructed for all conceivable oxidation state assignments in the four (semi) stable S states of the oxygen evolving complex, sampling various protonation levels and patterns to ensure comprehensive coverage. The models are evaluated with respect to their geometric, energetic, electronic, and spectroscopic properties against available experimental EXAFS, XFEL-XRD, EPR, ENDOR and Mn K pre-edge XANES data. New 2.5 K Mn-55 ENDOR data of the S-2 state are also reported. Our results conclusively show that the entire S state phenomenology can only be accommodated within the high-valent scheme by adopting a single motif and protonation pattern that progresses smoothly from S-0 (III, III, III, IV) to S-3 (IV, IV, IV, IV), satisfying all experimental constraints and reproducing all observables. By contrast, it was impossible to construct a consistent cycle based on the low-valent scheme for all S states. Instead, the low-valent models developed here may provide new insight into the over-reduced S states and the states involved in the assembly of the catalytically active water oxidizing cluster.

Ämnesord

NATURVETENSKAP  -- Kemi (hsv//swe)

NATURAL SCIENCES  -- Chemical Sciences (hsv//eng)

NATURVETENSKAP  -- Biologi -- Biokemi och molekylärbiologi (hsv//swe)

NATURAL SCIENCES  -- Biological Sciences -- Biochemistry and Molecular Biology (hsv//eng)

Nyckelord

PAULA JC

1986

JOURNAL OF THE AMERICAN CHEMICAL SOCIETY

V108

P4002 l Rhitankar

2013

BIOCHEMISTRY

V52

P7703 sunoki Masami

2011

JOURNAL OF PHOTOCHEMISTRY AND PHOTOBIOLOGY B-BIOLOGY

V104

P100 auss Andre

2012

PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF

PAULA JC

1987

JOURNAL OF THE CHEMICAL SOCIETY-FARADAY TRANSACTIONS I

V83

P3635 llier W

2000

BIOCHEMISTRY

V39

P4399 ussac Alain

2009

JOURNAL OF THE AMERICAN CHEMICAL SOCIETY

V131

P5050 pitz Christopher

2014

NATURE

V513

P261 harieva Ivelina

2011

ENERGY & ENVIRONMENTAL SCIENCE

V4

P2400 ena Yasufumi

2011

NATURE

V473

P55 trie Simon

2012

PHYSICAL CHEMISTRY CHEMICAL PHYSICS

V14

P11333

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