Studying the oxidation of water: The Photosystem II story

S.Roy-Chowdhury^1,2, K.Ayyer³, N.Stander^1,2, M.Vaughn^1,2, J.H.Yang^1,2, N.Vaughn^1,2, J.Coe^1,2, C.E.Conrad^1,2, I.Sarrou³, K.Dörner³, R.Fromme^1,2, H.N.Chapman^3,4, P.Fromme^1,2 * For complete author list see reference 3.

¹School of Molecular Sciences, Arizona State University, Tempe, AZ, USA

²Center for Applied Structural Discovery, Biodesign Institute, ASU, Tempe, AZ, USA

³Center for Free Electron Laser Science, DESY, Hamburg, Germany

⁴Department of Physics, University of Hamburg, Hamburg, Germany

Photosystem II (PSII) is a key enzyme in photosynthesis that drives the synthesis of oxygen by splitting water at the Mn₄O_xCa core of the oxygen-evolving cluster (OEC) in the protein complex. Using time-resolved femtosecond X-ray crystallography (TR-SFX) [1] at an X-ray free-electron laser, conformational changes have been reported both in the OEC and its protein environment [2]. Since 2014, we have optimized the crystallization procedures for improvement of the resolution obtained from nano-crystal diffraction. Combining innovative crystallization techniques with novel techniques for imaging macromolecules from ‘imperfect’ crystals [3] i.e. continuous diffraction, we have been successful at collecting data beyond the highest resolution of Bragg peaks. Additionally, since this method permits iterative phasing without a need for a structural model or experimental phase information [3], it is pioneering in the field of macromolecular structural studies.  

Photo-induced oxidation of water by PSII forms the basis for the development of synthetic water splitting devices [4]. Hence, an improved understanding of the natural process would enhance our efforts towards obtaining sustainable clean energy. Our work presents multi-disciplinary scientific collaboration because it encompasses various research fields of nano-crystallization, liquid sample delivery development, laser optics, along with, crystallographic data processing and evaluation. 

1. A. Aquila, M.S. Hunter, et.al., Opt Express, 20(3), (2012) 2706–16.

2. C. Kupitz, S. Basu, et.al., Nature, 513 (7517), (2014), 261-5.

3. Kartik Ayyer, Oleksandr M. Yefanov, Dominik Oberthür, Shatabdi Roy-Chowdhury, Lorenzo Galli, Valerio Mariani, Shibom Basu, Jesse Coe, Chelsie E. Conrad, Raimund Fromme, Alexander Schaffer, Katerina Dörner, Daniel James, Christopher Kupitz, Markus Metz, Garrett Nelson, Paulraj Lourfu Xavier, Kenneth R. Beyerlein, Marius Schmidt, Iosifina Sarrou, John C. H. Spence, Uwe Weirstall, Thomas A. White, Jay-How Yang, Yun Zhao, Mengning Liang, Andrew Aquila, Mark S. Hunter, Joseph S. Robinson, Jason E. Koglin, Sébastien Boutet, Petra Fromme, Anton Barty & Henry Chapman Nature, 530 (2016), 202-206

4. Y. Zhao, J. R. Swierk, et.al., PNAS, 109 (39), (2012), 15612-6.

The authors acknowledge financial support from NIH (award 1R01GM095583) & NSF’s BioXFEL Science Technology Center (award 1231306) and Arizona State University’s Center for Applied Structural Discovery.