Petrie Simon, Terrett Richard, Stranger Robert, Pace Ron J
Research School of Chemistry, College of Physical and Mathematical Sciences, The Australian National University, Acton, ACT 2601, Australia.
Chemphyschem. 2020 Apr 20;21(8):785-801. doi: 10.1002/cphc.201901106. Epub 2020 Mar 5.
Three atomic resolution crystal structures of Photosystem II, in the double flashed, nominal S intermediate state of its Mn Ca Water Oxidising Complex (WOC), have now been presented, at 2.25, 2.35 and 2.08 Å resolution. Although very similar overall, the S structures differ within the WOC catalytic site. The 2.25 Å structure contains only one oxy species (O5) in the WOC cavity, weakly associated with Mn centres, similar to that in the earlier 1.95 Å S structure. The 2.35 Å structure shows two such species (O5, O6), with the Mn centres and O5 positioned as in the 2.25 Å structure and O5-O6 separation of ∼1.5 Å. In the latest S variant, two oxy species are also seen (O5, Ox), with the Ox group appearing only in S , closely ligating one Mn, with O5-Ox separation <2.1 Å. The O5 and O6/Ox groups were proposed to be substrate water derived species. Recently, Petrie et al. (Chem. Phys. Chem., 2017) presented large scale Quantum Chemical modelling of the 2.25 Å structure, quantitatively explaining all significant features within the WOC region. This, as in our earlier studies, assumed a 'low' Mn oxidation paradigm (mean S Mn oxidation level of +3.0, Petrie et al., Angew. Chem. Int. Ed., 2015), rather than a 'high' oxidation model (mean S oxidation level of +3.5). In 2018 we showed (Chem. Phys. Chem., 2018) this oxidation state assumption predicted two energetically close S structural forms, one with the metal centres and O5 (as OH ) positioned as in the 2.25 Å structure, and the other with the metals similarly placed, but with O5 (as H O) located in the O6 position of the 2.35 Å structure. The 2.35 Å two flashed structure was likely a crystal superposition of two such forms. Here we show, by similar computational analysis, that the latest 2.08 Å S structure is also a likely superposition of forms, but with O5 (as OH ) occupying either the O5 or Ox positions in the WOC cavity. This highlights a remarkable structural 'lability' of the WOC centre in the S state, which is likely catalytically relevant to its water splitting function.
现已给出了光系统II的三个原子分辨率晶体结构，其处于锰钙水氧化复合物（WOC）的双闪光、标称S中间态，分辨率分别为2.25 Å、2.35 Å和2.08 Å。尽管整体非常相似，但这些S结构在WOC催化位点内存在差异。2.25 Å分辨率的结构在WOC腔中仅包含一种氧物种（O5），与锰中心弱结合，类似于早期1.95 Å分辨率的S结构中的情况。2.35 Å分辨率的结构显示有两种这样的物种（O5、O6），锰中心和O5的位置与2.25 Å分辨率结构中的相同，O5 - O6间距约为1.5 Å。在最新的S变体中，也观察到两种氧物种（O5、Ox），其中Ox基团仅在S态出现，紧密连接一个锰，O5 - Ox间距小于2.1 Å。O5和O6/Ox基团被认为是源自底物水的物种。最近，皮特里等人（《化学物理化学》，2017年）对2.25 Å分辨率的结构进行了大规模量子化学建模，定量解释了WOC区域内的所有重要特征。与我们早期的研究一样，这采用了“低”锰氧化范式（S态锰的平均氧化水平为 +3.0，皮特里等人，《德国应用化学》，2015年），而不是“高”氧化模型（S态的平均氧化水平为 +3.5）。2018年我们表明（《化学物理化学》，2018年），这种氧化态假设预测了两种能量相近的S结构形式，一种是金属中心和O5（作为OH）的位置与2.25 Å分辨率结构中的相同，另一种是金属位置类似，但O5（作为H₂O）位于2.35 Å分辨率结构的O6位置。2.35 Å分辨率的双闪光结构可能是这两种形式的晶体叠加。在此我们通过类似的计算分析表明，最新的2.08 Å分辨率的S结构也可能是多种形式的叠加，但O5（作为OH）占据WOC腔中的O5或Ox位置。这突出了WOC中心在S态时显著的结构“不稳定性”，这可能与其水分解功能在催化方面相关。
