Photosystem II and the Oxygen Evolving Site

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Photosystem II Movies PART II

The Structure of the OEC

With the increasing structural refinements to the PSII crystals and new spectroscopic approaches the mechanism of the Oxygen Evolving Complex (OEC) is becoming more and more clear. The proximity to solving one of natures greatest mechanistic secrets has fuelled a tremendous amount of new activity and research in PSII. A review of this spectroscopy [1] can be found <pdf>. The figure on the right is a recent summary of the final events of the catalysis of water oxidation. Only the last (S4) state is presented.

OEC mechanism 1977
 
Hillier & Messinger (2006)

A Pressing Question

The fundamental chemistry of photosynthetic water oxidation is a important question in its own scientific right. Clearly molecular oxygen is critical for most of the life on the planet. However, the chemistry of water oxidation is also important from a catalytic sense. The earth faces certain climatic consequences associated with looming increases of CO2 into the atmosphere. These increases are arising from the burning fossil fuels. They are clearly documented and a renewable carbon neutral solution is urgently needed derived from a renewable fuels. The long term solution is a hydrogen economy. The generation of hydrogen from renewable sources (water) will need a catalytic counterpart in the form of a catalyst for water oxidation: An electrochemical cell that generated hydrogen on one side of the electrode and molecular oxygen on the other half.

In this regard PSII provides a remarkable paradigm. The reaction is thermodynamically efficient (spectacularly so) and the reaction operating with low driving force and low overpotential. The reaction is also catalysed using a transition metal (Manganese) that is not particularly hard to come by. In contrast redox chemistry can be performed with Platinum electrodes. However, these are expensive due to the commodity price of platinum. (Platinum Commodity Prices) (10+ Price Trends). An platinum electrodes are not tremendously efficient in the redox chemistry. In this regard nature has many useful secrets to learn, and these secrets provide extremely useful paradigms to build on. Nature after all has had 2.7 billion years to work on water oxidation chemistry..

 
Returning to the work engaged in solving the mechanism of water splitting in the natural system.

Summary beyond PAGE 1

  • In Dec 2005 the Berlin group published a 3.0Å structure (pdb 2AXT) [7].
  • In November 2006 X-ray absorption spectroscopy EXAFS [8] was used on the PSII crystals to map the Mn-Mn distances as a function of the angle of the crystal. This approach was the first attempt to use this approach to solve a metal structure in a crystal.

Note: the following movies require Flash plug-in from Macromedia and will possibly take a moment to stream (patience please) and the movies can be downloaded below (WMV best quality).

 

Photosystem II OEC Movies

As discussed in the previous page <back here> the structure of the Oxygen Evolving complex of Photosystem II has undergone iterations of improvement in resolution over the past decade. The work published at the end of 2006 [8] presented a new approach with the combination of EXAFS (Extended X-ray Absorption Fine Structure) and X-ray diffraction of PSII crystals to generate a model of the catalytic site. This was the first attempt at using EXAFS on single crystals of a protein. The EXAFS approach generates Mn-Mn and Mn-Ca vectors that provide precise distances between metal centres and can be used to fit experimental data to model Mn system. The figure below presents the analysis of these vectors and generates 4 (!) solutions for the Mn4Ca complex that could accommodate the experimental results. The authors of [8] make a number of interesting statements and commented that the differences between their findings and earlier findings "highlight the difficulties of deriving high-resolution structures from low resolution x-ray diffraction data". It is likely soon that one of these models will be put forward as a preferred scenario when the next round of research is completed and published.

 

 

Open Questions

  • Resolution of X-ray diffraction will improve as crystallisation is optimised and crystals are made larger
  • None of these structures have yet identified a substrate water molecule (due to limited resolution) so there remains considerable speculation as to where the chemistry of water oxidation is precisely occurring on the Mn4Ca ions of the OEC.
  • Future studies of X-ray diffraction or possibly more likely from EXAFS of crystals will reveal the structural changes of the OEC as a function of the catalytic intermediate states of the reaction (i.e. changes as a function of S-state).
  • Radiation damage and reduction of the Mn ions will be controlled and the analysis will be performed in precisely defined oxidation states of the catalyst.
  • Channels for substrate water and product oxygen will be revealed.
 

To be Continued...

 

 

References

  [1] Hillier and Messinger (2005) Mechanism of Photosynthetic Oxygen Production. In Wydrzynski and Satoh (eds) Photosystem II: The Light-Driven Water:Plastoquinone Oxidoreductase, pp 567-608. Springer, Dordrecht. <pdf>
  [2] Wydrzynski TJ (1977) The role of manganese in photosynthetic oxygen evolution. PhD thesis. University of Illinois at Urbana- Champaign, Illinois.
  [2a] Govindjee, Wydrzynski T and Marks SB (1978) Manganese and chloride: their roles in photosynthesis. In: Metzner H (ed) Photosynthetic Oxygen Evolution, pp 321–344. Academic Press, New York
  [3] Rhee, Morris, Barber and Kühlbrandt (1998) Nature 396, 283-286.
  [4] Zouni, Witt, Kern, Fromme , Krauß, Saenger and Orth (2001) Nature 409, 739-743.
  [5] Kamiya and Shen (2003) Proc Natl Acad Sci 100, 98-103.
  [6] Ferreira, Iverson, Maghlaoui, Barber and Iwata (2004) Science 303, 1831-1838.
  [7] Loll, Kern, Saenger, Zouni and Biesiadka (2005) Nature 438, 1040-1044.
  [8] Yano, Kern, Sauer, Latimer, Pushkar, Biesiadka, Loll, Saenger, Messinger, Zouni, Yachandra (2006) Science 314, 821-825.
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1S5L pdb Full structure (ie. dimer) from London group. <Download>

1S5L overlay with 2AXT Backbone chain overlay pdb. <Download>

2AXT pdb Full structure (ie dimer) from Berlin group. <Download>.

2AXT overlay with 1S5L Backbone chain overlay pdb. <Download>

WMV Movies PC platform (right click to save) <1S5L>, <2AXT>, <Overlay>, <MnCat>

Quicktime Movies (Large file sizes) Quicktime (right click to save) <1S5L>, <2AXT>, <Overlay>, <MnCat>

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