Structural adaptations of photosynthetic complex I enable ferredoxin-dependent electron transfer (PDB 6HUM)

Photosynthetic complex I enables cyclic electron flow around photosystem I, a regulatory mechanism for photosynthetic energy conversion. We report a 3.3-angstrom-resolution cryo-electron microscopy structure of photosynthetic complex I from the cyanobacterium Thermosynechococcus elongatus. The model reveals structural adaptations that facilitate binding and electron transfer from the photosynthetic electron carrier ferredoxin. By mimicking cyclic electron flow with isolated components in vitro, we demonstrate that ferredoxin directly mediates electron transfer between photosystem I and complex I, instead of using intermediates such as NADPH (the reduced form of nicotinamide adenine dinucleotide phosphate). A large rate constant for association of ferredoxin to complex I indicates efficient recognition, with the protein subunit NdhS being the key component in this process.

Schuller JM, Birrell JA, Tanaka H, Konuma T, Wulfhorst H, Cox N, Schuller SK, Thiemann J, Lubitz W, Sétif P, Ikegami T, Engel BD, Kurisu G, Nowaczyk MM (2019) Science 363:257-260

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Perspective article in Science: Ulrich Brandt (2019) Adaptations of an ancient modular machine Science 363:230-231 DOI

Press releases

Press Release (English): 2018-12-21-biology-structure-and-function-photosynthesis-protein-explained-detail

Press Release (German): 2018-12-21-biologie-struktur-und-funktion-von-fotosyntheseprotein-im-detail-aufgeklaert


Bias-free photoelectrochemical water splitting with photosystem II on a dye-sensitized photoanode wired to hydrogenase

Natural photosynthesis stores sunlight in chemical energy carriers, but it has not evolved for the efficient synthesis of fuels, such as H2. Semi-artificial photosynthesis combines the strengths of natural photosynthesis with synthetic chemistry and materials science to develop model systems that overcome nature's limitations, such as low-yielding metabolic pathways and non-complementary light absorption by photosystems I and II. Here, we report a bias-free semi-artificial tandem platform that wires photosystem II to hydrogenase for overall water splitting. This photoelectrochemical cell integrated the red and blue light-absorber photosystem II with a green light-absorbing diketopyrrolopyrrole dye-sensitized TiO2 photoanode, and so enabled complementary panchromatic solar light absorption. Effective electronic communication at the enzyme-material interface was engineered using an osmium-complex-modified redox polymer on a hierarchically structured TiO2. This system provides a design protocol for bias-free semi-artificial Z schemes in vitro and provides an extended toolbox of biotic and abiotic components to re-engineer photosynthetic pathways.

Sokol KP, Robinson WE, Warnan J, Kornienko N, Nowaczyk MM, Ruff A, Zhang JZ, Reisner E (2018) Nature Energy 3:944-951 DOI

Press Release (English): http://news.rub.de/english/2018-09-26-biotechnology-bio-solar-cell-produces-hydrogen

Press Release (German): http://news.rub.de/wissenschaft/2018-09-26-biotechnologie-biosolarzelle-produziert-wasserstoff

Light-induced formation of partially reduced oxygen species limits the lifetime of photosystem 1-based biocathodes

Interfacing photosynthetic proteins specifically photosystem 1 (PS1) with electrodes enables light-induced charge separation processes for powering semiartificial photobiodevices with, however, limited long-term stability. Here, we present the in-depth evaluation of a PS1/Os-complex-modified redox polymer-based biocathode by means of scanning photoelectrochemical microscopy. Focalized local illumination of the bioelectrode and concomitant collection of H2O2 at the closely positioned microelectrode provide evidence for the formation of partially reduced oxygen species under light conditions. Long-term evaluation of the photocathode at different O2 concentrations as well as after incorporating catalase and superoxide dismutase reveals the particularly challenging issue of avoiding the generation of reactive species. Moreover, the evaluation of films prepared with inactivated PS1 and free chlorophyll points out additional possible pathways for the generation of oxygen radicals. To avoid degradation of PS1 during illumination and hence to enhance the long-term stability, the operation of biophotocathodes under anaerobic conditions is indispensable.

Zhao F, Hardt S, Hartmann V, Zhang H, Nowaczyk MM, Rögner M, Plumeré N, Schuhmann W, Conzuelo F (2018) Nature Communications 9:1973 DOI

Press Release (English): http://news.rub.de/english/2018-05-25-chemistry-why-bioelectrodes-energy-conversion-are-not-stable

Press Release (German): http://news.rub.de/wissenschaft/2018-05-25-chemie-warum-bioelektroden-fuer-die-energieumwandlung-nicht-stabil-sind

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 4:218-224 DOI

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



  • Schuller JM, Birrell JA, Tanaka H, Konuma T, Wulfhorst H, Cox N, Schuller SK, Thiemann J, Lubitz W, Sétif P, Ikegami T, Engel BD, Kurisu G, Nowaczyk MM (2019) Structural adaptations of photosynthetic complex I enable ferredoxin-dependent electron transfer Science 363:257-260 DOI


  • Sokol KP, Robinson WE, Oliveira A, Warnan J, Nowaczyk MM, Ruff A, Pereira I, Reisner E (2018) Photoreduction of CO2 with a formate dehydrogenase driven by photosystem II using a semi-artificial Z-scheme architecture J Am Chem Soc 140:16418-16422 DOI
  • Sokol KP, Robinson WE, Warnan J, Kornienko N, Nowaczyk MM, Ruff A, Zhang JZ, Reisner E (2018) Bias-free photoelectrochemical water splitting with photosystem II on a dye-sensitized photoanode wired to hydrogenase Nature Energy 3:944-951 DOI
  • Zhao F, Hartmann V, Ruff A, Nowaczyk MM, Rögner M, Schuhmann W, Conzuelo (2018) Unravelling electron transfer processes at photosystem 2 embedded in an Os-complex modified redox polymer Electrochimica Acta 290:451-456 DOI
  • 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 4:218-224 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