Research

Johannes Messinger sitting at a desk with different cables and other equipment in front of a window that is covered by a black blind.Photo: Mattias Pettersson

By harvesting and converting solar energy, photosynthesis supplies the chemical energy required for essentially all life on Earth. Thereby, photosynthesis is one of the most fundamental processes on our planet. Biological water oxidation to molecular oxygen (O2) and protons, performed by the enzyme Photosystem II, is the essential starting point in oxygenic photosynthesis, while the synthesis of carbohydrates (sugars) from carbon dioxide (CO2) by the enzyme Rubisco concludes it.

In my group, we aim to understand the design principles of biological redox catalysis by studying these two fundamental reactions in detail employing a range of structural and biophysical techniques. Of specific interest is how protein-water-cofactor interactions activate base metals, such as manganese (Mn), for complex conversion reactions of abundant small molecules and to derive design principles for scalable artificial catalysts for solar water splitting as well as to improve CO2 fixation by Rubisco.

We are also interested in the assembly and repair processes of photosystem II and the regulation of photosystem II via cellular processes, for example by CO2 and bicarbonate.

Despite the enormous progress towards a molecular understanding of the water-splitting and CO2 reduction reactions there is still a tremendous lack of knowledge. This can be exemplified by the fact that there are at present no stable and efficient synthetic catalysts for water oxidation made of abundant and inexpensive base metals and that there is at present no systematic approach for improving Rubisco, which is known to be a slow and inefficient enzyme.

The purpose of our research is to fill these knowledge gaps. The underlying hypothesis is that missing information regarding the function and basic design principles of protein-water-cofactor (p-w-c) interactions prevents full comprehension and mimicking of biological catalysis. Such interactions may include, for example, protein dynamics, temporary or permanent electric fields, control of water access, and H-bonding networks facilitating the efficient coupling of electron and proton transfer.

Employing an array of structural, biophysical and computational techniques we are aiming to prepare the ground for understanding the p-w-c interplay in Photosystem II (PSII) and Rubisco. For this, we utilize time-resolved membrane inlet mass spectrometry, cryo-EM, serial crystallography at free electron lasers, x-ray spectroscopy, neutron scattering and electron paramagnetic resonance. We perform these studies within a highly collaborative international network.

Key Publications

R Hussein, A Graça, J Forsman, AO Aydin, M Hall, J Gaetcke, P Chernev, P Wendler, H Dobbek, J Messinger, A Zouni, WP Schröder (2024) Cryo–electron microscopy reveals hydrogen positions and water networks in photosystem II, Science 348, 1349-1355. DOI: 10.1126/science.adn6541

C de Lichtenberg, L Rapatskiy, M Reus, E Heyno, A Schnegg, MM Nowaczyk, W Lubitz, J Messinger, N Cox (2024) Assignment of the slowly exchanging substrate water of nature’s water-splitting cofactor, P Natl Acad Sci USA 121, e2319374121 https://doi.org/10.1073/pnas.2319374121

A Bhowmick, R Hussein, I Bogaz, PS Simon, R Chatterjee, MD Doyle, MH Cheah, T Fransson, P Chernev, I-S Kim, H Makita, M Dasgupta, CJ Kaminsky, M Zhang, J Gätcke, S Haupt, II Nangca, SM Keable, AO Aydin, K Tono, S Owada, LB Gee, FD Fuller, A Batyuk, R Alonso-Mori, JM Holton, DW Paley, NW Moriaty, F Mamedov, PD Adams, AS Brewster, H Dobbek, NK Sauter, U Bergmann, A Zouni, J Messinger, J Kern, J Yano, VK Yachandra (2023) Structural evidence for intermediates during O2 formation in Photosystem II, Nature 617, 629-636. https://doi.org/10.1038/s41586-023-06038-z

D Shevela, JF Kern, G Govindjee, J Messinger (2023) Solar energy conversion by photosystem II: principles and structures. Photosynth Res 158, 279-307. https://doi.org/10.1007/s11120-022-00991-y

R Hussein, M Ibrahim, A Bhowmick, PS Simon, R Chatterjee, L Lassalle, M Doyle, I Bogacz, I-S Kim, MH Cheah, S Gul, C de Lichtenberg, P Chernev, CC Pham, ID Young, S Carbajo, FD Fuller, R Alonso-Mori, A Batyuk, KD Sutherlin, AS Brewster, R Bolotovsky, D Mendez, JM Holton, NW Moriarty, PD Adams, U Bergmann, NK Sauter, H Dobbek, J Messinger, A Zouni, J Kern, VK Yachandra, J Yano (2021) Structural dynamics in the water and proton channels of photosystem II during the S2 to S3 transition. Nat Commun 12, 6531. https://doi.org/10.1038/s41467-021-26781-z

Ekspong J, C Larsen, J Stenberg, WL Kwong, J Wang, J Zhang, EMJ Johansson, J Messinger, L Edman, T Wågberg (2021) Solar-Driven Water Splitting at 13.8% Solar-to-Hydrogen Efficiency by an Earth-Abundant Electrolyzer. Acs Sustain Chem Eng 9, 14070-14078. DOI: 10.1021/acssuschemeng.1c03565

C de Lichtenberg, CJ Kim, P Chernev, RJ Debus J Messinger (2021) The exchange of the fast substrate water in the S2 state of photosystem II is limited by diffusion of bulk water through channels - implications for the water oxidation mechanism. Chem Sci 12, 12763-12775. https://doi.org/10.1039/D1SC02265B

D Shevela, HN Do, A Fantuzzi, AW Rutherford, J Messinger (2020) Bicarbonate-mediated CO2 formation on both sides of photosystem II, Biochemistry 59, 2442-2449. https://doi.org/10.1021/acs.biochem.0c00208

S Kosourov, V Nagy, D Shevela, M Jokel, J Messinger, Y Allahverdiyeva (2020) Water oxidation by photosystem II is the primary source of electrons for sustained H2 photoproduction in nutrient-replete green algae, P Natl Acad Sci USA 117, 29629-29636. https://doi.org/10.1073/pnas.2009210117

MH Cheah, M Zhang, D Shevela, F Mamedov, A Zouni, J Messinger (2020) Assessment of the manganese cluster's oxidation state via photoactivation of photosystem II microcrystals, P Natl Acad Sci USA 117, 141-145. https://doi.org/10.1073/pnas.1915879117

J. Kern, R. Chatterjee, I.D. Young, F.D. Fuller, L. Lassalle, M. Ibrahim, S. Gul, T. Fransson, A.S. Brewster, R. Alonso-Mori, R. Hussein, M. Zhang, L. Douthit, C. de Lichtenberg, M.H. Cheah, D. Shevela, J. Wersig, I. Seuffert, D. Sokaras, E. Pastor, C. Weninger, T. Kroll, R.G. Sierra, P. Aller, A. Butryn, A.M. Orville, M.N. Liang, A. Batyuk, J.E. Koglin, S. Carbajo, S. Boutet, N.W. Moriarty, J.M. Holton, H. Dobbek, P.D. Adams, U. Bergmann, N.K. Sauter, A. Zouni, J. Messinger, J. Yano, V.K. Yachandra, Structures of the intermediates of Kok's photosynthetic water oxidation clock, Nature, 563 (2018) 421-425. https://doi.org/10.1038/s41586-018-0681-2

W.L. Kwong, E. Gracia-Espino, C. Choo, R. Sandström, T. Wågberg, J. Messinger, Cationic vacancy defects in iron phosphide: A promising route toward efficient and stable hydrogen evolution by electrochemical water splitting, ChemSusChem, 10 (2017) 4544-4551. https://doi.org/10.1002/cssc.201701565

H. Nilsson, F. Rappaport, A. Boussac, J. Messinger, Substrate-water exchange in photosystem II is arrested before dioxygen formation, Nat Commun, 5 (2014). https://doi.org/10.1038/ncomms5305

N. Cox, J. Messinger, Reflections on substrate water and dioxygen formation, BBA-Bioenergetics, 1827 (2013) 1020-1030. https://doi.org/10.1016/j.bbabio.2013.01.013

L.V. Kulik, B. Epel, W. Lubitz, J. Messinger, Electronic structure of the Mn4OxCa cluster in the S0 and S2 states of the oxygen-evolving complex of photosystem II based on pulse 55Mn-ENDOR and EPR Spectroscopy, J Am Chem Soc, 129 (2007) 13421-13435. https://doi.org/10.1021/ja071487f

J. Messinger, M. Badger, T. Wydrzynski, Detection of one slowly exchanging substrate water molecule in the S3 state of photosystem II, P Natl Acad Sci USA, 92 (1995) 3209-3213. https://doi.org/10.1073/pnas.92.8.3209