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Structural insights into photosystem II assembly

Biogenesis of photosystem II (PSII), nature's water-splitting catalyst, is assisted by auxiliary proteins that form transient complexes with PSII components to facilitate stepwise assembly events. Using cryo-electron microscopy, we solved the structure of such a PSII assembly intermediate from Thermosynechococcus elongatus at 2.94 Ĺ resolution. It contains three assembly factors (Psb27, Psb28 and Psb34) and provides detailed insights into their molecular function. Binding of Psb28 induces large conformational changes at the PSII acceptor side, which distort the binding pocket of the mobile quinone (QB) and replace the bicarbonate ligand of non-haem iron with glutamate, a structural motif found in reaction centres of non-oxygenic photosynthetic bacteria. These results reveal mechanisms that protect PSII from damage during biogenesis until water splitting is activated. Our structure further demonstrates how the PSII active site is prepared for the incorporation of the Mn4CaO5 cluster, which performs the unique water-splitting reaction.

Zabret J, Bohn S, Schuller SK, Arnolds O, Möller M, Meier-Credo J, Liauw P, Chan A, Tajkhorshid E, Langer JD, Stoll R, Krieger-Liszkay A, Engel BD, Rudack T, Schuller JM, Nowaczyk MM (2021) Nature Plants 7, 524-538

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Press Release (English): 2021-04-22-biology-how-molecular-machine-assembled

Press Release (German): 2021-04-16-biologie-wie-eine-molekulare-maschine-zusammengebaut-wird

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Highlights

Cryo-EM structure of a functional monomeric Photosystem I from Thermosynechococcus elongatus reveals red chlorophyll cluster.

A high-resolution structure of trimeric cyanobacterial Photosystem I (PSI) from Thermosynechococcus elongatus was reported as the first atomic model of PSI almost 20 years ago. However, the monomeric PSI structure has not yet been reported despite long-standing interest in its structure and extensive spectroscopic characterization of the loss of red chlorophylls upon monomerization. Here, we describe the structure of monomeric PSI from Thermosynechococcus elongatus BP-. Comparison with the trimer structure gave detailed insights into monomerization-induced changes in both the central trimerization domain and the peripheral regions of the complex. Monomerization-induced loss of red chlorophylls is assigned to a cluster of chlorophylls adjacent to PsaX. Based on our findings, we propose a role of PsaX in the stabilization of red chlorophylls and that lipids of the surrounding membrane present a major source of thermal energy for uphill excitation energy transfer from red chlorophylls to P700.

Çoruh O, Frank A, Tanaka H, Kawamoto A, El-Mohsnawy E, Kato T, Namba K, Gerle C, Nowaczyk MM, Kurisu G (2021) Communications Biology 4:304

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Press Release (English): 2021-03-18-biology-hidden-machinery-photosynthetic-giant-revealed

Press Release (German): 2021-03-18-biologie-geheimnis-eines-fotosynthese-giganten-gelueftet

Improved quantum efficiency in an engineered light harvesting/photosystem II super-complex for high current density biophotoanodes.

Photosystem II (PSII) is the only enzyme that catalyzes light-induced water oxidation, the basis for its application as a biophotoanode in various bio-photovoltaics and photo-bioelectrochemical cells. However, the absorption spectrum of PSII limits the quantum efficiency in the range of visible light, due to a gap in the green absorption region of chlorophylls (500-600 nm). To overcome this limitation, we have stabilized the interaction between PSII and Phycobilisomes (PBSs) - the cyanobacterial light harvesting complex, in vitro. The PBS of three different cyanobacteria (Acaryochloris marina, Am, Mastigocladus laminosus, ML, and Synechocystis sp. PCC 6803, Syn) are analyzed for their ability to transfer energy to Thermosynechococcus elongatus (Te) PSII by fluorescence spill-over and photo-current action spectra. Integration of the PBS-PSII super-complexes within an Os-complex-modified hydrogel on macro-porous indium tin oxide electrodes (MP-ITO) resulted in notably improved, wavelength dependent, incident photon-to-electron conversion efficiencies (IPCE). IPCE values in the green gap were doubled from 3% to 6% compared to PSII electrodes without PBS and a maximum IPCE up to 10.9% at 670 nm was achieved.

Hartmann V, Harris D, Bobrowsk T, Ruff A, Rögner M, Frank A, Günther Pomorski T, Rögner M, Schuhmann W, Adir N, Nowaczyk MM (2020) Journal of Materials Chemistry A 8:14463-14471

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Press Release (English): 2020-06-02-biotechnology-more-efficient-biosolar-cells-modelled-nature

Press Release (German): 2020-06-02-biotechnologie-effizientere-biosolarzellen-nach-dem-vorbild-der-natur

Redox-coupled proton pumping drives carbon concentration in the photosynthetic complex I (PDB 6TJV)

Photosynthetic organisms capture light energy to drive their energy metabolism, and employ the chemical reducing power to convert carbon dioxide (CO2) into organic molecules. Photorespiration, however, significantly reduces the photosynthetic yields. To survive under low CO2 concentrations, cyanobacteria evolved unique carbon-concentration mechanisms that enhance the efficiency of photosynthetic CO2 fixation, for which the molecular principles have remained unknown. We show here how modular adaptations enabled the cyanobacterial photosynthetic complex I to concentrate CO2 using a redox-driven proton-pumping machinery. Our cryo-electron microscopy structure at 3.2?Ĺ resolution shows a catalytic carbonic anhydrase module that harbours a Zn2+ active site, with connectivity to proton-pumping subunits that are activated by electron transfer from photosystem I. Our findings illustrate molecular principles in the photosynthetic complex I machinery that enabled cyanobacteria to survive in drastically changing CO2 conditions.

Schuller JM, Saura P, Thiemann J, Schuller SK, Gamiz-Hernandez AP, Kurisu G, Nowaczyk MM, Kaila VRI (2020) Nature Communications 11, 494

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Press Release (English): protein-machine-by-which-cyanobacteria-concentrate-carbon-dioxide-from-the-atmosphere-revealed

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

Publications

2021

  • Zabret J, Bohn S, Schuller SK, Arnolds O, Möller M, Meier-Credo J, Liauw P, Chan A, Tajkhorshid E, Langer JD, Stoll R, Krieger-Liszkay A, Engel BD, Rudack T, Schuller JM, Nowaczyk MM (2021) Structural insights into photosystem II assembly. Nature Plants 7, 524-538 DOI DOI
  • Nowaczyk MM, Grimm HC, Assil-Companioni, Kourist R (2021) Cyanobakterien als Biokatalysatoren BIOspektrum 27:208-210 DOI
  • Çoruh O, Frank A, Tanaka H, Kawamoto A, El-Mohsnawy E, Kato T, Namba K, Gerle C, Nowaczyk MM, Kurisu G (2021) Cryo-EM structure of a functional monomeric Photosystem I from Thermosynechococcus elongatus reveals red chlorophyll cluster. Communications Biology 4:304 DOI DOI

2020

  • Zabret J, Bohn S, Schuller SK, Arnolds O, Möller M, Meier-Credo J, Liauw P, Chan A, Tajkhorshid E, Langer JD, Stoll R, Krieger-Liszkay A, Engel BD, Rudack T, Schuller JM, Nowaczyk MM (2020) How to build a water-splitting machine: structural insights into photosystem II assembly bioRxiv DOI
  • Assil-Companioni L, Büchsenschütz HC, Solymosi D, Dyczmons-Nowaczyk NG, Bauer KKF, Wallner S, Macheroux P, Allahverdiyeva Y, Nowaczyk MM, Kourist R (2020) Engineering of NADPH Supply Boosts Photosynthesis-Driven Biotransformations ACS catalysis 10, 11864-11877 DOI DOI
  • Wang P, Frank A, Zhao F, Szczesny J, Junqueira JRC, Zacarias S, Ruff A, Nowaczyk MM, Pereira IAC, Rögner M, Conzuelo F, Schuhmann W (2020) Closing the Gap for Electronic Short-Circuiting: Photosystem I Mixed Monolayers Enable Improved Anisotropic Electron Flow in Biophotovoltaic Devices. Angew Chem Int Ed DOI DOI
  • Hartmann V, Harris D, Bobrowsk T, Ruff A, Rögner M, Frank A, Günther Pomorski T, Rögner M, Schuhmann W, Adir N, Nowaczyk MM (2020) Improved quantum efficiency in an engineered light harvesting/photosystem II super-complex for high current density biophotoanodes. Journal of Materials Chemistry A 8:14463-14471 DOI DOI
  • Böhmer S, Marx C, Gómez-Baraibar A, Nowaczyk MM, Tischler D, Hemschemeier A, Happe T (2020) Evolutionary diverse Chlamydomonas reinhardtii Old Yellow Enzymes reveal distinctive catalytic properties and potential for whole-cell biotransformations. Algal Research 50:101970 DOI DOI
  • Kraus A, Weskamp M, Zierles J, Balzer M, Busch R, Eisfeld J, Lambertz J, Nowaczyk MM, Narberhaus F (2020) Arginine-rich small proteins with a domain of unknown function DUF1127 play a role in phosphate and carbon metabolism of Agrobacterium tumefaciens. Journal of Bacteriology 202, e00309-20 DOI
  • Bobrowski T, Conzuelo F, Ruff A, Hartmann V, Frank A, Erichsen T, Nowaczyk MM, Schuhmann W (2020) Scalable Fabrication of Biophotoelectrodes by Means of Automated Airbrush Spray-Coating ChemPlusChem 85:1396-1400 DOI
  • Wang P, Zhao F, Hartmann V, Nowaczyk MM, Ruff A, Schuhmann W, Conzuelo F (2020) Reassessing the rationale behind herbicide biosensors: the case of a photosystem II/redox polymer-based bioelectrode. Bioelectrochemistry 136, 107597 DOI
  • Kannchen D, Zabret J, Oworah-Nkruma R, Dyczmons-Nowaczyk N, Wiegand K, Löbbert P, Frank A, Nowaczyk MM, Rexroth S, Rögner M (2020) Remodeling of photosynthetic electron transport in Synechocystis sp. PCC 6803 for future hydrogen production from water.BBA Bioenergetics 1861, 148208 DOI
  • Cimiotti D, Fujita-Becker S, Möhner D, Smolina N, Budde H, Wies A, Morgenstern L, Gudkova A, Sejersen T, Sjöberg G, Mügge A, Nowaczyk MM, Reusch P, Pfitzer G, Stehle R, Schröder RR, Mannherz HG, Kostareva A, Jaquet K (2020) Infantile restrictive cardiomyopathy: cTnI-R170G/W impair the interplay of sarcomeric proteins and the integrity of thin filaments. PLoS one e0229227 DOI
  • Aras M, Hartmann V, Hartmann J, Nowaczyk MM, Frankenberg-Dinkel N (2020) Proximity channeling during cyanobacterial phycoerythrobilin synthesis FEBS J 287:284-294 DOI
  • Schuller JM, Saura P, Thiemann J, Schuller SK, Gamiz-Hernandez AP, Kurisu G, Nowaczyk MM, Kaila VRI (2020) Redox-coupled proton pumping drives carbon concentration in the photosynthetic complex I Nature Communications 11:494 DOI DOI

2019

  • Zhao F, Wang P, Ruff A, Hartmann V, Zacarias S, Pereira IC, Nowaczyk MM, Rögner M, Conzuelo F, Schuhmann W (2019) A photosystem I monolayer with anisotropic electron flow enables Z-scheme like photosynthetic water splitting Energy Environ Sci 12:3133-3143 DOI
  • Hristou A, Gerlach I, Stolle DS, Neumann J, Bischoff A, Dünschede B, Nowaczyk MM, Zoschke R, Schünemann D (2019) Ribosome-associated chloroplast SRP54 enables efficient co-translational membrane insertion of key photosynthetic proteins Plant Cell 31:2734-2750 DOI
  • Chrysina M, Heyno E, Kutin Y, Reus M, Nilsson H, Nowaczyk MM, DeBeer S, Neese F, Messinger J, Lubitz W, Cox N (2019) Five-coordinate MnIV intermediate in the activation of nature's water splitting cofactor Proc Natl Acad Sci USA 116:16841-16846 DOI
  • 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 DOI

2018

  • 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 DOI
  • Zhao F, Hartmann V, Ruff A, Nowaczyk MM, Rögner M, Schuhmann W, Conzuelo F (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 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

2017

  • 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

2016

  • 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 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

2015

  • 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

2014

  • 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

2013

  • 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

2012

  • 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

2011

  • 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

2010

  • 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

2009

  • 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

2008

  • 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

2007

  • 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

2006

  • 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

2005

  • 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

2004

  • 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

 

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