Synthesizing Mechanism of the Mn₄Ca Cluster Mimicking the Oxygen‐Evolving Center in Photosynthesis

Abstract

The photosynthetic oxygen-evolving center (OEC) is a unique Mn 4 CaO 5 cluster that serves as a blueprint to develop superior water-splitting catalysts for the generation of solar fuels in artificial photosynthesis. It is a great challenge and longstanding issue to reveal the synthesizing mechanism of this Mn 4 CaO 5 cluster in both natural and artificial photosynthesis. Herein, efforts were made to reveal the synthesizing mechanism of an artificial Mn 4 CaO 4 cluster, a close mimic of the OEC. Four key intermediates were successfully isolated and structurally characterized for the first time. It was demonstrated that the Mn 4 CaO 4 cluster could be formed through a reaction between a thermodynamically stable Mn 3 CaO 4 cluster and an unusual fourcoordinated Mn III ion, followed by stabilization process through binding an organic base (e.g., pyridine) on the "dangling" Mn ion. These findings shed new light on the synthesizing mechanism of the OEC and rational design of new artificial water-splitting catalysts. Figure 4. Synthesizing mechanism of the Mn 4 CaO 4 cluster.

Mimicking the Oxygen-Evolving Center in Photosynthesis

“…In 2012, Christou group reported a Mn IV 3 Ca 2 O 4 -complex ( 2 ) with one Ca 2+ attached to the Mn 3 CaO 4 cubane ( Mukherjee et al, 2012 ) ( Figures 4C , D ). A similar Mn 3 Ca 2 O 4 -complex was also isolated as a by-product during the synthesis of Mn 4 CaO 4 -cluster ( Chen et al, 2022 ). Here, the peripheral ligands of the Mn 3 Ca 2 O 4 -cluster are provided by pivalic anions or neutral pivalic acid, which resembles to that of the OEC in PSII ( Umena et al, 2011 ).…”

“…The mechanism of the synthesis of the artificial Mn 4 CaO 4 -cluster has been recently studied by characterizing the intermediate species during the synthesis of the Mn 4 CaO 4 -complex ( 4 ) ( Chen et al, 2022 ). By using the high-resolution electrospray ionization (HR-ESI) mass spectroscopy, we have characterized the precursor of the Mn 4 CaO 4 -cluster and observed five key fragments with m/z − values at 1233.235, 1218.259, 875.118, 358.120, and 343.143 assigned to the [Mn 4 CaO 4 ( t BuCO 2 ) 9 ] − , [Mn 3 Ca 2 O 4 ( t BuCO 2 ) 9 ] − , [Mn 3 CaO 4 ( t BuCO 2 ) 6 ] − , [Mn( t BuCO 2 ) 3 ] − , and [Ca( t BuCO 2 ) 3 ] − , respectively ( Chen et al, 2022 ). More importantly, after extensive experimentation, three key intermediates, [Mn 3 CaO 4 ( t BuCO 2 ) 6 ( t BuCO 2 H) 3 ] ( 5 ), [ n Bu 4 NMn( t BuCO 2 ) 4 ] ( 6 ), and [Mn 4 CaO 4 ( t BuCO 2 ) 8 ( t BuCO 2 H) 3 ] ( 7 ), were successfully crystallized.…”

“… Structures of three intermediates for the synthesis of the artificial Mn 4 CaO 4 -cluster ( Chen et al, 2022 ). (A) Core of [Mn 3 CaO 4 (tBuCO 2 ) 6 (tBuCO 2 H) 3 ] ( 5 ); (B) structure of 5 ; (C) Mn center in [ n Bu 4 NMn( t BuCO 2 ) 4 ] ( 6 ); (D) structure of the [Mn( t BuCO 2 ) 4 ] − anion in 6 ; (E) core structure of [Mn 4 CaO 4 ( t BuCO 2 ) 8 ( t BuCO 2 H) 3 ] ( 7 ); (F) structure of 7 .…”

“…The mechanism of the synthesis of the artificial Mn 4 CaO 4 -cluster has been recently studied by characterizing the intermediate species during the synthesis of the Mn 4 CaO 4 -complex (4) (Chen et al, 2022). By using the high-resolution electrospray ionization (HR-ESI) mass spectroscopy, we have characterized the precursor of the Mn 4 CaO 4cluster and observed five key fragments with m/z − values at 1233.…”

“…In PSII, the early steps of the assembly of the OEC involving two Mn and one Ca ions have been studied for more than 50 years (Cheniae and Martin, 1971;Dasgupta et al, 2008;Bao and Burnap, 2016;Murray et al, 2020); on the other hand, the assembly of the third and the fourth Mn ions in OEC is fully unknown (Bao and Burnap, 2016;Avramov et al, 2020). Considering the observed thermodynamical stability of the fully carboxylic ligand coordinated Mn 3 CaO 4 -cluster (5) observed (Chen et al, 2022), we propose that a similar Mn 3 CaO 4cluster could be present during the synthesis of the OEC in PSII. If it was the case, a mono-nuclear Mn ion (similar to that in 6) would be necessary to be incorporated into the Mn 3 CaO 4 -cluster, followed by structural rearrangements to form the intact OEC, as has been suggested recently (Gisriel et al, 2020;Sato et al, 2021).…”