X-ray structure of an asymmetrical trimeric ferredoxin-photosystem I complex

Photosystem I (PSI), a large protein complex located in the thylakoid membrane, mediates the final step in light-driven electron transfer to the stromal electron carrier protein ferredoxin (Fd). Here, we report the first structural description of the PSI-Fd complex from Thermosynechococcus elongatus. The trimeric PSI complex binds three Fds in a non-equivalent manner. While each is recognized by a PSI protomer in a similar orientation, the distances between Fds and the PSI redox centres differ. Fd binding thus entails loss of the exact three-fold symmetry of the PSI's soluble subunits, inducing structural perturbations which are transferred to the lumen through PsaF. Affinity chromatography and nuclear magnetic resonance analyses of PSI-Fd complexes support the existence of two different Fd-binding states, with one Fd being more tightly bound than the others. We propose a dynamic structural basis for productive complex formation, which supports fast electron transfer between PSI and Fd.

Kubota-Kawai H, Mutoh R, Shinmura K, Sétif P, Nowaczyk MM, Rögner M, Ikegami T, Tanaka H, Kurisu G (2018) Nature Plants doi:10.1038/s41477-018-0130-0 DOI

Press Release (German): http://news.rub.de/wissenschaft/2018-04-20-biologie-warum-ein-fotosyntheseprotein-am-liebsten-im-dreierpack-arbeitet



  • Zhao F, Hardt S, Hartmann V, Zhang H, Nowaczyk MM, Rögner M, Plumeré N, Schuhmann W, Conzuelo F (2018) Light-induced formation of partially reduced oxygen species limits the lifetime of photosystem 1-based biocathodes Nature Communications 9:1973 DOI
  • Kubota-Kawai H, Mutoh R, Shinmura K, Sétif P, Nowaczyk MM, Rögner M, Ikegami T, Tanaka H, Kurisu G (2018) X-ray structure of an asymmetrical trimeric ferredoxin-photosystem I complex Nature Plants doi:10.1038/s41477-018-0130-0 DOI
  • Hartmann V, Ruff A, Schuhmann W, Rögner, Nowaczyk MM (2018) Analysis of Photosystem II Electron Transfer with Natural PsbA-Variants by Redox Polymer/Protein Biophotoelectrochemistry Photosynthetica 56:229-235 DOI


  • Böhmer S, Köninger K, Gómez-Baraibar Á, Bojarra S, Mügge C, Schmidt S, Nowaczyk MM, Kourist R (2017) Enzymatic Oxyfunctionalization Driven by Photosynthetic Water-Splitting in the Cyanobacterium Synechocystis sp. PCC 6803 Catalysts 7:240 DOI
  • Zhao F, Plumeré N, Nowaczyk MM, Ruff A, Schuhmann W, Conzuelo F (2017) Interrogation of a PS1-based Photocathode by Means of Scanning Photoelectrochemical Microscopy Small 13:1604093 DOI
  • Essmann V, Zhao F, Hartmann V, Nowaczyk MM, Schuhmann W, Conzuelo F (2017) In operando investigation of electrically coupling of photosystem 1 and photosystem 2 by means of bipolar electrochemistry Analytical Chemistry 89:7160-7165 DOI
  • Zhao F, Conzuelo F, Hartmann V, Li H, Stapf S, Nowaczyk MM, Rögner M, Plumeré N, Lubitz W, Schuhmann W (2017) A novel versatile microbiosensor for local hydrogen detection by means of scanning photoelectrochemical microscopy Biosensors and Bioelectronics 94:433-437 DOI
  • Rexroth S, Nowaczyk MM, Rögner M (2017) Cyanobacterial Photosynthesis: The Light Reactions. In: Hallenbeck P. (eds) Modern Topics in the Phototrophic Prokaryotes. Springer, Cham, pp 163-191 DOI


  • Nowaczyk MM and Plumeré N (2016) Photosynthesis: Short Circuit at the Chlorophyll - News and Views in Nature Chemical Biology 12:990-991 DOI
  • Nowaczyk MM and Kourist R (2016) Lichtgetriebene Ganzzell-biotransformation mit rekombinanten Cyanobakterien Biospektrum 22:765 DOI
  • Ziehe D, Dünschede B, Zenker M, Funke S, Nowaczyk MM, Schünemann D (2016) The chloroplast SRP systems of charophytes and bryophytes as intermediates in the evolution of SRP-dependent protein transport in higher plants PLoS One PLoS One 11:e0166818 DOI
  • Calow J, Behrens AJ, Mader S, Bockau U, Struwe WB, Harvey DJ, Cormann KU, Nowaczyk MM, Loser K, Schinor D, Hartmann MWW, Crispin M (2016) Antibody production using a ciliate generates unusual antibody glycoforms displaying enhanced cell-killing activity MAbs 8:1498-1511 DOI
  • Heinz S, Rast A, Shao L, Gutu A, Gügel IL, Heyno E, Labs M, Rengstl B, Viola S, Nowaczyk MM, Leister D, Nickelsen J (2016) Thylakoid Membrane Architecture in Synechocystis Depends on CurT, a Homolog of the Granal CURVATURE THYLAKOID1 Proteins Plant Cell 28:2238-2260 DOI
  • Sokol KP, Mersch D, Hartmann V, Zhang JZ, Nowaczyk MM, Rögner M, Ruff A, Schuhmann W, Plumeré N, Reisner E (2016) Rational wiring of photosystem II to hierarchical indium tin oxide electrodes using redox polymers Energy Environ Sci 9:3698-3709 [cover] DOI
  • Köninger K, Gómez Baraibar Á, Mügge C, Paul CE, Hollmann F, Nowaczyk MM, Kourist R (2016) Recombinant Cyanobacteria for the Asymmetric Reduction of C=C Bonds Fueled by the Biocatalytic Oxidation of Water Angew Chem Int Ed 55:5582-5585 DOI
  • Cormann KU, Möller M, Nowaczyk MM (2016) Critical assessment of protein cross-linking and molecular docking: an updated model for the interaction between photosystem II and Psb27 Front Plant Sci 7:157 DOI
  • Vöpel T, Saw EN, Hartmann V, Williams R, Müller F, Schuhmann W, Plumeré N, Nowaczyk M, Ebbinghaus S, Rögner M (2016) Simultaneous measurements of photocurrents and H2O2 evolution from solvent exposed Photosystem 2 complexes Biointerphases 11:019001 DOI
  • Heinz S, Liauw P, Nickelsen J, Nowaczyk M (2016) Analysis of photosystem II biogenesis in cyanobacteria BBA Bioenergetics 1857:274-287 DOI
  • Korste A, Wulfhorst H, Ikegami T, Nowaczyk MM, Stoll R (2016) NOE distance and dihedral angle restraints to calculate the solution structure of the NDH-1 complex subunit CupS from Thermosynechococcus elongatus Data in brief 6:249-252 DOI
  • Plumeré N and Nowaczyk MM (2016) Biophotoelectrochemistry of Photosynthetic Proteins DOI


  • Mutoh R, Muraki N, Shinmura K, Kubota-Kawai H, Lee YH, Nowaczyk MM, Rögner M, Hase T, Ikegami T, Kurisu G (2015) X-ray Structure and Nuclear Magnetic Resonance Analysis of the Interaction Sites of the Ga-substituted Cyanobacterial Ferredoxin Biochemistry 54:6052-6061 DOI
  • Zhao F, Conzuelo F, Hartmann V, Li H, Nowaczyk MM, Plumeré N, Rögner M, Schuhmann W (2015) Light Induced H2 Evolution from a Biophotocathode Based on Photosystem 1 - Pt Nanoparticles Complexes Integrated in Solvated Redox Polymers Films J Phys Chem B 119:13726-31 DOI
  • Korste A, Wulfhorst H, Ikegami T, Nowaczyk MM, Stoll R (2015) Solution structure of the NDH-1 complex subunit CupS from Thermosynechococcus elongatus BBA Bioenergetics1847:1212-1221 DOI
  • Bartsch M, Gassmeyer SK, Köninger K, Igarashi K, Liauw P, Dyczmons-Nowaczyk N, Miyamoto K, Nowaczyk MM, Kourist R (2015) Photosynthetic production of enantioselective biocatalysts Microb Cell Fact 14:53 DOI
  • Liauw P, Kannchen D, Gasper R, Dyczmons-Nowaczyk N, Nowaczyk MM, Hofmann E (2015) Cloning, expression, crystallization and preliminary X-ray studies of a superfolder GFP fusion of cyanobacterial Psb32 Acta Cryst F 71:409-413 DOI
  • Walter B, Hristou A, Nowaczyk MM, Schünemann D (2015) In vitro reconstitution of cotranslational D1 insertion reveals a role of the cpSec/Alb3 translocase and Vipp1 in photosystem II biogenesis Biochem J 468: 315-324 DOI
  • Korste A, Wulfhorst H, Ikegami T, Nowaczyk MM, Stoll R (2015) 1H, 13C and 15N chemical shift assignments of the NDH-1 complex subunit CupS. Biomol NMR Assign 9:169-171 DOI
  • Nowaczyk MM, Rexroth S, Rögner M (2015) Biotechnological Potential of Cyanobacteria DOI


  • Corman KU, Bartsch M, Rögner M, Nowaczyk MM (2014) Localization of the CyanoP binding site on photosystem II by surface plasmon resonance spectroscopy. Front Plant Sci 5:595 DOI
  • Wulfhorst H, Franken LE, Wessinghage T, Boekema EJ, Nowaczyk MM (2014) The 5 kDa Protein NdhP Is Essential for Stable NDH-1L Assembly in Thermosynechococcus elongatus. PLoS One 9:e103584 DOI
  • Rexroth S, Rexroth D, Veit S, Plohnke N, Cormann KU, Nowaczyk MM, Rögner M (2014) Functional Characterization of the Small Regulatory Subunit PetP from the Cytochrome b6f Complex in Thermosynechococcus elongatus. Plant Cell 26:3435-3448 DOI
  • Hartmann V, Kothe T, Pöller S, El-Mohsnawy E, Nowaczyk MM, Plumere N, Schuhmann W, Rögner M (2014) Redox hydrogels with adjusted redox potential for improved efficiency in Z-scheme inspired biophotovoltaic cells. Phys Chem Chem Phys 16:11936-11941 DOI
  • Lohmiller T, Krewald V, Pérez Navarro M, Retegan M, Rapatskiy L, Nowaczyk MM, Boussac A, Neese F, Lubitz W, Pantazis DA, Ames WM, Cox N (2014) Structure, ligands and substrate coordination of the oxygen-evolving complex of photosystem II in the S2 state: a combined EPR and DFT study. Phys Chem Chem Phys 16:11877-11892 DOI


  • Kothe T, Plumeré N, Badura A, Nowaczyk MM, Guschin DA, Rögner M, Schuhmann W (2013) Combination of a Photosystem 1-Based Photocathode and a Photosystem 2-Based Photoanode to a Z-Scheme Mimic for Biophotovoltaic Applications. Angew Chem Int Ed 52:14233-14236 DOI
  • Pérez Navarro M, Ames WM, Nilsson H, Lohmiller T, Pantazis DA, Rapatskiy L, Nowaczyk MM, Neese F, Boussac A, Messinger J, Lubitz W, Cox N (2013) Ammonia binding to the oxygen-evolving complex of photosystem II identifies the solvent-exchangeable oxygen bridge (µ-oxo) of the manganese tetramer. Proc Natl Acad Sci USA 110:15561-15567 DOI


  • Rapatskiy L, Cox N, Savitsky A, Ames WM, Sander J, Nowaczyk MM, Rögner M, Boussac A, Neese F, Messinger J, Lubitz W (2012) Detection of the Water Binding Sites of the Oxygen-evolving Complex of Photosystem II Using W-band (17)O ELDOR-detected NMR Spectroscopy. J Am Chem Soc 134:16619-16653 DOI
  • Nowaczyk MM, Krause K, Mieseler M, Sczibilanski A, Ikeuchi, M, Rögner M (2012) Deletion of psbJ leads to accumulation of Psb27–Psb28 photosystem II complexes in Thermosynechococcus elongatus. BBA Bioenergetics 1817:1339-1345 DOI


  • Grasse N, Mamedov F, Becker K, Styring S, Rögner M, Nowaczyk MM (2011) The role of a novel dimeric Photosystem II-Psb27 complex in PSII repair. J Biol Chem 286:29548-29555 DOI
  • Becker K, Cormann KU, Nowaczyk MM (2011) Assembly of the water-oxidizing complex in photosystem II. J Photochem Photobiol B 104:204-11 DOI
  • Nowaczyk MM, Wulfhorst H, Ryan CM, Souda P, Zhang H, Cramer WA, Whitelegge JP (2011) NdhP and NdhQ: two novel small subunits of the cyanobacterial NDH-1 complex. Biochemistry 50:1121-1125 DOI


  • El-Mohsnawy E, Kopczak MJ, Schlodder E, Nowaczyk M, Meyer HE, Warscheid B, Karapetyan NV, Rögner M (2010) Structure and Function of Intact Photosystem 1 Monomers from the Cyanobacterium Thermosynechococcus elongatus. Biochemistry 49:4740-4751 DOI
  • Sander J, Nowaczyk M, Buchta J, Dau H, Vass I, Deak Z, Dorogi M, Iwai M, Roegner M (2010) Functional characterization and quantification of the alternative PsbA copies in Thermosynechococcus elongatus and their role in photoprotection. J Biol Chem 285:29851-29856 DOI
  • Nowaczyk MM, Sander J, Grasse N, Cormann KU, Gomolla D, Bernat G, Rögner M (2010) Dynamics of the cyanobacterial photosynthetic network: Communication and modification of membrane protein complexes. Eur J Cell Biol 89:974-982 DOI


  • Szczepaniak M, Sander J, Nowaczyk M, Müller MG, Rögner M, Holzwarth AR (2009) Charge separation, stabilization, and protein relaxation in photosystem II core particles with closed reaction center. Biophys J 96:621-31 DOI
  • Cormann KU, Bangert JA, Ikeuchi M, Rögner M, Stoll R, Nowaczyk MM (2009) Structure of Psb27 in solution: implications for transient binding to Photosystem II during biogenesis and repair. Biochemistry 48:8768-70 DOI
  • Cormann KU, Ikeuchi M, Rögner M, Nowaczyk MM, Stoll R (2009) Sequence-specific 1H, 13C, and 15N backbone assignment of Psb27 from Synechocystis PCC 6803. Biomol NMR Assign 3:247-9 DOI
  • Schottkowski M, Ratke J, Oster U, Nowaczyk M, Nickelsen J (2009) Pitt, a Novel Tetratricopeptide Repeat Protein Involved in Light-Dependent Chlorophyll Biosynthesis and Thylakoid Membrane Biogenesis in Synechocystis sp PCC 6803. Mol Plant 2:1289-1297 DOI


  • Folea IM, Zhang P, Nowaczyk MM, Ogawa T, Aro EM, Boekema EJ (2008) Single particle analysis of thylakoid proteins from Thermosynechococcus elongatus and Synechocystis 6803: localization of the CupA subunit of NDH-1. FEBS Lett 582:249-54 DOI
  • Martinez-Junza V, Szczepaniak M, Braslavsky SE, Sander J, Nowaczyk M, Rögner M, Holzwarth AR (2008) A photoprotection mechanism involving the D(2) branch in photosystem II cores with closed reaction centers. Photochem Photobiol Sci 7:1337-43 DOI


  • Mamedov F, Nowaczyk MM, Thapper A, Rögner M, Styring S (2007) Functional Characterization of Monomeric Photosystem II Core Preparations from Thermosynechococcus elongatus with or without the Psb27 Protein. Biochemistry 46:5542-5551 DOI
  • Klinkert B, Nowaczyk MM, Nickelsen J (2007) Function of Genetic Material: Assembly Factors of the Photosynthetic Machinery in Cyanobacteria. Progress in Botany (Esser K, Lüttge U, Beyschlag W, Murata J, eds) 68: 57-79 DOI


  • Milaslavina Y, Szczepaniak M, Müller MG, Sander J, Nowaczyk M, Rögner M, Holzwarth, AR (2006) Charge separation kinetics in intact photosystem II core particles is traplimited. A picosecond fluorescence study. Biochemistry 45:2436-2442 DOI
  • Holzwarth AR, Müller MG, Reus M, Nowaczyk M, Sander J, Rögner M (2006) Mechanism of electron transfer in intact photosystem II and in isolated reaction centers. Pheophytin is the primary electron acceptor. Proc Natl Acad Sci USA 103:6895-6900 DOI
  • Nowaczyk MM, Hebeler R, Schlodder E, Meyer HE, Warscheid B, Rögner M (2006) Psb27, a Cyanobacterial Lipoprotein, Is Involved in the Repair Cycle of Photosystem II. Plant Cell 18:3121-3131 DOI
  • Nowaczyk M, Berghaus C, Steinhoff,H-J, Stoll R, Rögner M (2006) Preliminary NMR and EPR studies of the 33 kDa protein (PsbO) in solution. Essays on Science (Rashid S, ed), Hamdard Foundation, Pakistan, 184-196


  • Arteni AA, Nowaczyk M, Lax J, Kouril R, Rögner M, Boekema EJ (2005) Single particle electron microscopy in combination with mass spectrometry to investigate novel complexes of membrane proteins. J Struct Biol 149:325-331 DOI
  • Nowaczyk M, Steinhoff H-J, Rögner M (2005) EPR-spectroscopy of spin-labeled PsbO from Thermosynechococcus elongatus. Photosynthesis: Fundamental Aspects to Global Perspectives" (van der Est A and Bruce D, eds) 246-248


  • Nowaczyk M, Berghaus C, Stoll R, Rögner M (2004) Preliminary structural characterisation of the 33 kDa protein (PsbO) in solution studied by site-directed mutagenesis and NMR spectroscopy. Phys Chem Chem Phys 6:4878-4881 DOI
  • Nowaczyk M, Ambill M, Lax J, Prodöhl A, Oworah-Nkruma R, Rögner M (2004) Biochemical Analysis of a new 'His-Tag' PS2-Preparation from Thermosynechococcus elongatus. Cell Mol Biol Lett 9:79
  • Nowaczyk M, Oworah-Nkruma R, Rögner M, Popot JL (2004) Amphipols: Strategies For an Improved PS2 Environment in Aqueous Solution. Biohydrogen III (Miyake J, Igarashi Y, Rögner M, eds) 151-159 DOI