SPP 1601:  New Frontiers in Sensitivity for EPR Spectroscopy: from Biological Cells to Nano Materials

• Subject Area: Chemistry
• Term: from 2012 to 2020
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 198612328

• Final Report Year: 2021

Final Report Abstract

The priority program SPP 1601 brought together about 40 German principal investigators (PIs) working on very different areas of natural sciences, developing electron spin resonance (ESR/EPR) as a common spectroscopic tool. The technique allows for the detection of paramagnetic centers and their coupled magnetic nuclei on a time scale as short as nanoseconds and with a spatial resolution from the atomic up to the nanometer scale. Our strategy was to cross-fertilize several advances in specific areas of biological and material sciences taking advantage of recent progress in hardware, microwaves and digital technologies as well as leveraging synergy with the field of nuclear magnetic resonance (NMR). The priority program bundled all these research areas in a coordinated effort, with the shared goal to increase sensitivity of EPR in biology, chemistry, materials science, and physics and opening new application fields such as in-cell EPR or studies of molecular machines, thin-film solar cells and nano materials. In a synergistic fashion between chemistry, physics and theory, groups explored the capability of pulsed experiments based on arbitrary microwave pulses using recently available fast electronics. Other groups developed new approaches for spectroscopy in the THz range or micro resonators to access nanostructures. In a parallel track, groups working on single molecule detection took inspiration from recent developments in spectroscopy of biomolecules and labelling procedures to establish new atomic scale sensors. Also, on the biological and biophysical side tremendous progress was achieved in the field of spin labelling for biomolecules, which led to new studies on molecular machines and of biomolecules in cell. Major scientific results were presented to the reviewer’s panel in a final colloquium in Leipzig, September 2018. The priority program has substantially contributed in reshaping the research landscape in EPR spectroscopy in Germany and world-wide, but has also repositioned the importance of EPR with respect to other significant areas of spectroscopy, for instance NMR, or biophysics and physics. The concept of the SPP was so attractive, that the National Science Foundation (NSF) was immediately inspired (in 2012) to create a parallel network (called SharedEPR), which merged in a mutually sponsored German/US collaborative program. This unprecedented initiative led DFG to fund a large amount of international research exchanges as well as the attendance of international conferences and schools worldwide. In addition to the collaboration with the US, exchange with Israel was particularly in forefront. Several initiatives were adopted to support young investigators, for instance though research exchanges, schools and the organization of their own yearly young investigator’s workshops. Particular attention was dedicated to promote the career of young female students and researchers. All these measures fostered a new generation of successful scientists, with 38 PhD graduations, 4 habilitations and 11 professorships in Germany. New international activities were started, for instance the draft of the first Whitepaper on EPR contributed by 28 international experts including several SPP PIs.

Publications

• A cryogenic receiver for EPR. J. Mag. Res. 2013, 237, 79-84
  Narkowicz, R.; Ogata, H.; Reijerse, E.; Suter, D.
  
• A cryogenic receiver for EPR. J. Mag. Res. 2013, 237, 79-84
  Narkowicz, R.; Ogata, H.; Reijerse, E.; Suter, D., A cryogenic receiver for EPR
  
• Detecting and polarizing nuclear spins with double resonance on a single electron spin. Phys Rev. Lett. 2013, 111 (6), 067601
  London, P.; Scheuer, J.; Cai, J. M.; Schwarz, I.; Retzker, A.; Plenio, M. B.; Katagiri, M.; Teraji, T.; Koizumi, S.; Isoya, J.; Fischer, R.; McGuinness, L. P.; Naydenov, B.; Jelezko, F.
  
• Detection of a Few Metallo-Protein Molecules Using Color Centers in Nanodiamonds. Nano Lett. 2013, 13 (7), 3305-3309
  Ermakova, A.; Pramanik, G.; Cai, J. M.; Algara-Siller, G.; Kaiser, U.; Weil, T.; Tzeng, Y. K.; Chang, H. C.; McGuinness, L. P.; Plenio, M. B.; Naydenov, B.; Jelezko, F.
  
• A Genetically Encoded Spin Label for Electron Paramagnetic Resonance Distance Measurements. J. Am. Chem. Soc. 2014, 136 (17), 6510-6510
  Schmidt, M. J.; Borbas, J.; Drescher, M.; Summerer, D.
  
• Genetically Encoded Spin Label. WO2015107071A1 (2014)
  D. Summerer, M. J. Schmidt, M. Drescher
  
• Broadband electrically detected magnetic resonance using adiabatic pulses. J. Mag. Res. 2015, 254, 62-9
  Hrubesch, F. M.; Braunbeck, G.; Voss, A.; Stutzmann, M.; Brandt, M. S.
  
• Broadband spin echoes and broadband SIFTER in EPR. J. Mag. Res. 2015, 250, 55-62
  Schöps, P.; Spindler, P. E.; Marko, A.; Prisner, T. F.
  
• Carr–Purcell Pulsed Electron Double Resonance with Shaped Inversion Pulses. Phys. Chem. Lett., 2015, 6, 4331-4335
  Spindler, P.E.; Waclawska, I.; Endeward, B.; Plackmeyer, J.; Ziegler, C.; Prisner, T.F.
  
• Compact electrically detected magnetic resonance setup. AIP Adv. 2015, 5 (4), 047139
  Eckardt, M.; Behrends, J.; Münter, D.; Harneit, W.
  
• CW and pulsed electrically detected magnetic resonance spectroscopy at 263GHz/12T on operating amorphous silicon solar cells. J. Mag. Res. 2015, 257, 94-101
  Akhtar, W.; Schnegg, A.; Veber, S.; Meier, C.; Fehr, M.; Lips, K.
  
• High cooperativity coupling between a phosphorus donor spin ensemble and a superconducting microwave resonator. Appl. Phys. Lett. 2015, 107 (14), 142105
  Zollitsch, C. W.; Mueller, K.; Franke, D. P.; Goennenwein, S. T. B.; Brandt, M. S.; Gross, R.; Huebl, H.
  
• Hydrogen bond network between amino acid radical intermediates on the proton-coupled electron transfer pathway of E. coli α2 ribonucleotide reductase. J. Am. Chem. Soc. 2015, 137 (1), 289-98
  Nick, T. U.; Lee, W.; Kossmann, S.; Neese, F.; Stubbe, J.; Bennati, M.
  
• In vivo EPR on spin labeled colicin A reveals an oligomeric assembly of the pore-forming domain in E. coli membranes. Phys. Chem. Chem. Phys. 2015, 17 (7), 4875-4878
  Dunkel, S.; Pulagam, L. P.; Steinhoff, H. J.; Klare, J. P.
  
• Mechanism for nuclear and electron spin excitation by radio frequency current. Phys. Rev. B 2015, 92 (22), 220418
  Müllegger, S.; Rauls, E.; Gerstmann, U.; Tebi, S.; Serrano, G.; Wiespointner-Baumgarthuber, S.; Schmidt, W. G.; Koch, R.
  
• Sensor comprising a piezomagnetic or piezoelectric element on a diamond substrate with a colour center. EP3132278B1 (2017)
  J. Cai, F. Jelezko, M.B. Plenio
  
• Single Crystal Electron Paramagnetic Resonance with Dielectric Resonators of Mononuclear Cu2+ Ions in a Metal–Organic Framework Containing Cu2 Paddle Wheel Units. J. Org. Chem. C 2015, 119 (33), 19171-19179
  Friedländer, S.; Šimėnas, M.; Kobalz, M.; Eckold, P.; Ovchar, O.; Belous, A. G.; Banys, J. r.; Krautscheid, H.; Pöppl, A.
  
• Transient electrically detected magnetic resonance spectroscopy applied to organic solar cells. Appl. Phys. Lett. 2015, 107 (4), 043302
  Kraffert, F.; Steyrleuthner, R.; Meier, C.; Bittl, R.; Behrends, J.
  
• Tuner and radiation shield for planar electron paramagnetic resonance microresonators. Rev. Sci. Instrum. 2015, 86 (2), 024701
  Narkowicz, R.; Suter, D.
  
• 28.2 A 14GHz battery-operated point-of-care ESR spectrometer based on a 0.13µm CMOS ASIC, 2016 IEEE International Solid-State Circuits Conference (ISSCC), 2016, 476-477
  Handwerker, J.; Schlecker, B.; Wachter, U.; Radermacher, P.; Ortmanns, M.; Anders, J.
  
• Continuous-Wave Single-Crystal Electron Paramagnetic Resonance of Adsorption of Gases to Cupric Ions in the Zn(II)-Doped Porous Coordination Polymer Cu2.965Zn0.035(btc)2. J. Org. Chem. C 2016, 120 (48), 27399-27411
  Friedländer, S.; Petkov, P. S.; Bolling, F.; Kultaeva, A.; Böhlmann, W.; Ovchar, O.; Belous, A. G.; Heine, T.; Pöppl, A.
  
• Multitechnique investigation of Dy3 – implications for coupled lanthanide clusters. Chem. Sci. 2016, 7 (7), 4347-4354
  Gysler, M.; El Hallak, F.; Ungur, L.; Marx, R.; Hakl, M.; Neugebauer, P.; Rechkemmer, Y.; Lan, Y.; Sheikin, I.; Orlita, M.; Anson, C. E.; Powell, A. K.; Sessoli, R.; Chibotaru, L. F.; van Slageren, J.
  
• Spacers for Geometrically Well-Defined Water-Soluble Molecular Rulers and Their Application. J. Org, Chem. 2016, 81 (6), 2549-2571
  Qi, M.; Hülsmann, M.; Godt, A.
  
• Spacers for Geometrically Well-Defined Water-Soluble Molecular Rulers and Their Application. J. Org, Chem. 2016, 81 (6), 2549-2571
  Qi, M.; Hülsmann, M.; Godt, A.
  
• SPIDYAN, a MATLAB library for simulating pulse EPR experiments with arbitrary waveform excitation. J. Mag. Res. 2016, 263, 45-54
  Pribitzer, S.; Doll, A.; Jeschke, G.
  
• A modified RF-transmission line concept for probe excitation in light-induced magnetic resonance force microscopy, 2017 IEEE Asia Pacific Microwave Conference (APMC), 13-16 Nov. 2017; 2017, 536-539
  Baer, C.; Orend, K.; Musch, T.; Deichmöller, J.; Havenith, M.
  
• A molecular quantum spin network controlled by a single qubit. Sci. Adv. 2017, 3 (8), e1701116
  Schlipf, L.; Oeckinghaus, T.; Xu, K.; Dasari, D. B. R.; Zappe, A.; de Oliveira, F. F.; Kern, B.; Azarkh, M.; Drescher, M.; Ternes, M.; Kern, K.; Wrachtrup, J.; Finkler, A.
  
• A new near-linear scaling, efficient and accurate, open-shell domain-based local pair natural orbital coupled cluster singles and doubles theory. J. Chem. Phys. 2017, 146 (16), 164105
  Saitow, M.; Becker, U.; Riplinger, C.; Valeev, E. F.; Neese, F.
  
• Efficient Electrical Spin Readout of NV− Centers in Diamond. Phys Rev. Lett. 2017, 118 (3), 037601
  Hrubesch, F. M.; Braunbeck, G.; Stutzmann, M.; Reinhard, F.; Brandt, M. S.
  
• Nanoscale nuclear magnetic resonance with chemical resolution. Science 2017, 357 (6346), 67-71
  Aslam, N.; Pfender, M.; Neumann, P.; Reuter, R.; Zappe, A.; Fávaro de Oliveira, F.; Denisenko, A.; Sumiya, H.; Onoda, S.; Isoya, J.; Wrachtrup, J.
  
• Nanoscale x-ray investigation of magnetic metallofullerene peapods. Nanotechnology 2017, 28 (43), 435703
  Fritz, F.; Westerström, R.; Kostanyan, A.; Schlesier, C.; Dreiser, J.; Watts, B.; Houben, L.; Luysberg, M.; Avdoshenko, S. M.; Popov, A. A.; Schneider, C. M.; Meyer, C.
  
• Orthogonal spin labeling using click chemistry for in vitro and in vivo applications. J. Mag. Res. 2017, 275, 38-45
  Kucher, S.; Korneev, S.; Tyagi, S.; Apfelbaum, R.; Grohmann, D.; Lemke, E. A.; Klare, J. P.; Steinhoff, H. J.; Klose, D.
  
• Pulsed triple electron resonance (TRIER) for dipolar correlation spectroscopy. J. Mag. Res. 2017, 282, 119-128
  Pribitzer, S.; Sajid, M.; Hülsmann, M.; Godt, A.; Jeschke, G.
  
• Recent progress in synchrotron-based frequencydomain Fourier-transform THz-EPR. J. Mag. Res. 2017, 280, 10-19
  Nehrkorn, J.; Holldack, K.; Bittl, R.; Schnegg, A.
  
• Transport-related triplet states and hyperfine couplings in organic tandem solar cells probed by pulsed electrically detected magnetic resonance spectroscopy. J. Mag. Res. 2017, 282, 10-17
  Kraffert, F.; Bahro, D.; Meier, C.; Denne, M.; Colsmann, A.; Behrends, J.
  
• Triplet Excitons in Highly Efficient Solar Cells Based on the Soluble Small Molecule p- DTS(FBTTh2)2. Adv. Energ. Mater. 2017, 7 (7), 1602016
  Väth, S.; Tvingstedt, K.; Baumann, A.; Heiber, M. C.; Sperlich, A.; Love, J. A.; Nguyen, T.-Q.; Dyakonov, V.
  
• Versatile Trityl Spin Labels for Nanometer Distance Measurements on Biomolecules In Vitro and within Cells. Angew. Chem. Int. Edit. 2017, 56 (1), 177-181
  Jassoy, J. J.; Berndhäuser, A.; Duthie, F.; Kühn, S. P.; Hagelueken, G.; Schiemann, O.
  
• (2018) Topology of active, membrane-embedded Bax in the context of a toroidal pore. Cell Death Diff. 2018, 25, 1717–1731
  S. Bleicken, T. E. Assafa, C. Stegmueller, A. Wittig, A. J. Garcia-Saez, E. Bordignon
  
• Accurate spin-densities based on the domain-based local pair-natural orbital coupled-cluster theory. J. Chem. Phys. 2018, 149 (3), 034104
  Saitow, M.; Neese, F.
  
• Calculation of spin-spin zero-field splitting within periodic boundary conditions: Towards all-electron accuracy. Phys. Rev. B 2018, 97 (11), 115135
  Biktagirov, T.; Schmidt, W. G.; Gerstmann, U.
  
• Cooperative broadband spin echoes through optimal control. J. Mag. Res. 2018, 286, 115-137
  Kallies, W.; Glaser, S. J.
  
• Electron Paramagnetic Resonance Spectroscopy at Surfaces. In Encyclopedia of Interfacial Chemistry, Wandelt, K., Ed. Elsevier: Oxford, 2018; pp 129-142
  Clawin, P. M.; Richter, N. F.; Riedel, W.; Ronneburg, H.; Risse, T.
  
• Quantitative analysis of zero-field splitting parameter distributions in Gd(iii) complexes. Phys. Chem. Chem. Phys. 2018, 20 (15), 10470-10492
  Clayton, J. A.; Keller, K.; Qi, M.; Wegner, J.; Koch, V.; Hintz, H.; Godt, A.; Han, S.; Jeschke, G.; Sherwin, M. S.; Yulikov, M.
  
• Ultra-broadband EPR spectroscopy in field and frequency domains. Phys. Chem. Chem. Phys. 2018, 20 (22), 15528-15534
  Neugebauer, P.; Bloos, D.; Marx, R.; Lutz, P.; Kern, M.; Aguilà, D.; Vaverka, J.; Laguta, O.; Dietrich, C.; Clérac, R.; van Slageren, J.
  
• A new perspective on membrane-embedded Bax oligomers using DEER and bioresistant orthogonal spin labels. Sci. Rep. 2019, 9 (1), 13013
  Teucher, M.; Zhang, H.; Bader, V.; Winklhofer, K. F.; García-Sáez, A. J.; Rajca, A.; Bleicken, S.; Bordignon, E.
  
• Application of commercially available fluorophores as triplet spin probes in EPR spectroscopy. Mol. Phys. 2019, 117 (19), 2688-2699
  Serrer, K.; Matt, C.; Sokolov, M.; Kacprzak, S.; Schleicher, E.; Weber, S.
  
• Device and method for generating and detecting a transient magnetization of a sample. US Patent App. 15/779,104 (2019), Deutsches Patent Nr. DE102015120644B3 (03.09.2017)
  J. Anders, K. Lips
  
• Examination of the Magneto-Structural Effects of Hangman Groups on Ferric Porphyrins by EPR. Inorg. Chem. 2019, 58 (20), 14228-14237
  Nehrkorn, J.; Bonke, S. A.; Aliabadi, A.; Schwalbe, M.; Schnegg, A.
  
• Extending electron paramagnetic resonance to nanoliter volume protein single crystals using a self-resonant microhelix. Sci. Adv. 2019, 5 (10), eaay1394
  Sidabras, J. W.; Duan, J.; Winkler, M.; Happe, T.; Hussein, R.; Zouni, A.; Suter, D.; Schnegg, A.; Lubitz, W.; Reijerse, E. J.
  
• Quantitative Modeling of Superconducting Planar Resonators for Electron Spin Resonance. Phys. Rev. Appl. 2019, 12 (2), 024021
  Weichselbaumer, S.; Natzkin, P.; Zollitsch, C. W.; Weiler, M.; Gross, R.; Huebl, H.
  
• Studying Conformational Changes of the Yersinia Type-III-Secretion Effector YopO in Solution by Integrative Structural Biology. Structure 2019, 27 (9), 1416-1426.e3
  Peter, M. F.; Tuukkanen, A. T.; Heubach, C. A.; Selsam, A.; Duthie, F. G.; Svergun, D. I.; Schiemann, O.; Hagelueken, G.
  
• Towards Low-Cost, High-Sensitivity Point-of-Care Diagnostics Using VCO-Based ESR-on-a-Chip Detectors. IEEE Sens. J. 2019, 19 (20), 8995-9003
  Schlecker, B.; Hoffmann, A.; Chu, A.; Ortmanns, M.; Lips, K.; Anders, J.
  
• Towards Low-Cost, High-Sensitivity Point-of-Care Diagnostics Using VCO-Based ESR-on-a-Chip Detectors. IEEE Sens. J. 2019, 19 (20), 8995-9003
  Schlecker, B.; Hoffmann, A.; Chu, A.; Ortmanns, M.; Lips, K.; Anders, J.
  
• Cross-polarisation ENDOR for spin-1 deuterium nuclei. Mol. Phys. 2020, 118 (18), e1763490
  Bejenke, I.; Zeier, R.; Rizzato, R.; Glaser, S. J.; Bennati, M.
  
• Cross-polarisation ENDOR for spin-1 deuterium nuclei. Mol. Phys. 2020, 118 (18), e1763490
  Bejenke, I.; Zeier, R.; Rizzato, R.; Glaser, S. J.; Bennati, M.
  
• Optically and electrically excited intermediate electronic states in donor:acceptor based OLEDs. Mater. Horiz. 2020, 7 (4), 1126-1137
  Bunzmann, N.; Weissenseel, S.; Kudriashova, L.; Gruene, J.; Krugmann, B.; Grazulevicius, J. V.; Sperlich, A.; Dyakonov, V.