Room temperature XFEL crystallography reveals asymmetry in the vicinity of the two phylloquinones in photosystem I

  • Stephen M. Keable
  • , Adrian Kölsch
  • , Philipp S. Simon
  • , Medhanjali Dasgupta
  • , Ruchira Chatterjee
  • , Senthil Kumar Subramanian
  • , Rana Hussein
  • , Mohamed Ibrahim
  • , In Sik Kim
  • , Isabel Bogacz
  • , Hiroki Makita
  • , Cindy C. Pham
  • , Franklin D. Fuller
  • , Sheraz Gul
  • , Daniel Paley
  • , Louise Lassalle
  • , Kyle D. Sutherlin
  • , Asmit Bhowmick
  • , Nigel W. Moriarty
  • , Iris D. Young
  • Johannes P. Blaschke, Casper de Lichtenberg, Petko Chernev, Mun Hon Cheah, Sehan Park, Gisu Park, Jangwoo Kim, Sang Jae Lee, Jaehyun Park, Kensuke Tono, Shigeki Owada, Mark S. Hunter, Alexander Batyuk, Roland Oggenfuss, Mathias Sander, Serhane Zerdane, Dmitry Ozerov, Karol Nass, Henrik Lemke, Roman Mankowsky, Aaron S. Brewster, Johannes Messinger, Nicholas K. Sauter, Vittal K. Yachandra, Junko Yano, Athina Zouni, Jan Kern

Research output: Contribution to journalArticlepeer-review

17 Scopus citations

Abstract

Photosystem I (PS I) has a symmetric structure with two highly similar branches of pigments at the center that are involved in electron transfer, but shows very different efficiency along the two branches. We have determined the structure of cyanobacterial PS I at room temperature (RT) using femtosecond X-ray pulses from an X-ray free electron laser (XFEL) that shows a clear expansion of the entire protein complex in the direction of the membrane plane, when compared to previous cryogenic structures. This trend was observed by complementary datasets taken at multiple XFEL beamlines. In the RT structure of PS I, we also observe conformational differences between the two branches in the reaction center around the secondary electron acceptors A1A and A1B. The π-stacked Phe residues are rotated with a more parallel orientation in the A-branch and an almost perpendicular confirmation in the B-branch, and the symmetry breaking PsaB-Trp673 is tilted and further away from A1A. These changes increase the asymmetry between the branches and may provide insights into the preferential directionality of electron transfer.

Original languageEnglish
Article number21787
JournalScientific Reports
Volume11
Issue number1
DOIs
StatePublished - Dec 2021
Externally publishedYes

Funding

This work was supported by the Director, Office of Science, Office of Basic Energy Sciences (OBES), Division of Chemical Sciences, Geosciences, and Biosciences (CSGB) of the Department of Energy (DOE) for Ultrafast XFEL crystallography studies of charge separation in photosynthetic reaction centers (J.K.), and for X-ray spectroscopy and crystallography methodology and instrumentation (J.Y., V.K.Y.). National Institutes of Health (NIH) provides funding through Grants GM126289 (J.K.) and GM110501 (J.Y.) for instrumentation development for XFEL experiments, GM055302 (V.K.Y.) for biochemistry support, and GM117126 (N.K.S.) for development of computational protocols for analyzing XFEL data. Funding from Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) under Germany´s Excellence Strategy—EXC 2008/1—390540038 (A.Z.), Sfb1078 (Humboldt Universität Berlin) TP A5 (A.Z., M.I., R.H.) is acknowledged. A.K., A.Z. and S.S. gratefully acknowledge the support of this research by the Bundesministerium für Bildung und Forschung (BMBF), Germany, 2020+, projects 031B0557 A+B, and Vetenskapsrådet 2016-05183 (J.M.) is also gratefully acknowledged. XFEL data was collected under proposal PO58 at LCLS/SLAC, Stanford, under proposal 2018B8089 at SACLA, Japan, under proposal 20190996 at SwissFEL, Switzerland, and under proposal 2019-1st-NCI-033 at PAL-XFEL, Korea. This work was supported by the Global Science Experimental Data Hub Center (GSDC) for data computing and the Korea Research Environment Open NETwork (KREONET) for network service provided by the Korea Institute of Science and Technology Information (KISTI). Use of the LCLS, SLAC National Accelerator Laboratory, is supported by the U.S. DOE, Office of Science, OBES under Contract No. DE-AC02-76SF00515. We thank the support staff at LCLS/SLAC, SACLA, SwissFEL and PAL-XFEL.

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