Spin-Polarized Radicals with Extremely Long Spin-Lattice Relaxation Time at Room Temperature in a Metal-Organic Framework.

The generation of spin polarization is key in quantum information science and dynamic nuclear polarization. Polarized electron spins with long spin-lattice relaxation times (T1) at room temperature are important for these applications but have been difficult to achieve. We report the realization of spin-polarized radicals with extremely long T1 at room temperature in a metal-organic framework (MOF) in which azaacene chromophores are densely integrated. Persistent radicals are generated in the MOF by charge separation after photoexcitation. Spin polarization of a triplet generated by photoexcitation is successfully transferred to the persistent radicals. Pulse electron spin resonance measurements reveal that the T1 of the polarized radical in the MOF is as long as 214 µs with a relatively long spin-spin relaxation time T2 of the radicals of up to 0.98 µs at room temperature. The achievement of extremely long spin polarization in MOFs with nanopores accessible to guest molecules will be an important cornerstone for future highly sensitive quantum sensing and efficient dynamic nuclear polarization.

Location of two Mn2+ affinity sites in photosystem II detected by pulsed electron-electron double resonance.

In this study, we identified two Mn2+ sites in apo-Photosystem II (PSII) using the pulsed electron-electron double resonance (PELDOR). A Mn2+ ion was bound to apo-PSII on the deactivation of the oxygen-evolving complex. The electron-electron magnetic dipole interaction of the Mn2+ to YD· was estimated to be 2.4 MHz. The site was assigned at the position between His332 and Glu189 in the D1 polypeptide, which is close to the Mn1 site in mature PS II. Using recent structures observed under electron microscopes (EM), the location of the Mn2+ site on photoactivation was reevaluated. The position between Asp170 and Glu189 in the D1 polypeptide is a good candidate for the initial high-affinity site for photoactivation. Based on a comparison with the PELDOR results, the two EM structures were evaluated.

Conformational ensemble of a multidomain protein explored by Gd3+ electron paramagnetic resonance.

Despite their importance in function, the conformational state of proteins and its changes are often poorly understood, mainly because of the lack of an efficient tool. MurD, a 47-kDa protein enzyme responsible for peptidoglycan biosynthesis, is one of those proteins whose conformational states and changes during their catalytic cycle are not well understood. Although it has been considered that MurD takes a single conformational state in solution as shown by a crystal structure, the solution nuclear magnetic resonance (NMR) study suggested the existence of multiple conformational state of apo MurD in solution. However, the conformational distribution has not been evaluated. In this work, we investigate the conformational states of MurD by the use of electron paramagnetic resonance (EPR), especially intergadolinium distance measurement using double electron-electron resonance (DEER) measurement. The gadolinium ions are fixed on specific positions on MurD via a rigid double-arm paramagnetic lanthanide tag that has been originally developed for paramagnetic NMR. The combined use of NMR and EPR enables accurate interpretation of the DEER distance information to the structural information of MurD. The DEER distance measurement for apo MurD shows a broad distance distribution, whereas the presence of the inhibitor narrows the distance distribution. The results suggest that MurD exists in a wide variety of conformational states in the absence of ligands, whereas binding of the inhibitor eliminates variation in conformational states. The multiple conformational states of MurD were previously implied by NMR experiments, but our DEER data provided structural characterization of the conformational variety of MurD.

A Peptoid with Extended Shape in Water.

The term "peptoids" was introduced decades ago to describe peptide analogues that exhibit better physicochemical and pharmacokinetic properties than peptides. Oligo(N-substituted glycine) (oligo-NSG) was previously proposed as a peptoid due to its high proteolytic resistance and membrane permeability. However, oligo-NSG is conformationally flexible, and ensuring a defined shape in water is difficult. This conformational flexibility severely limits the biological application of oligo-NSG. Here, we propose oligo(N-substituted alanine) (oligo-NSA) as a peptoid that forms a defined shape in water. The synthetic method established in this study enabled the first isolation and conformational study of optically pure oligo-NSA. Computational simulations, crystallographic studies, and spectroscopic analysis demonstrated the well-defined extended shape of oligo-NSA realized by backbone steric effects. This new class of peptoid achieves the constrained conformation without any assistance of N-substituents and serves as a scaffold for displaying functional groups in well-defined three-dimensional space in water, which leads to effective biomolecular recognition.

Location of the extrinsic subunit PsbP in photosystem II studied by pulsed electron-electron double resonance.

The binding site of the extrinsic protein PsbP in plant photosystem II was mapped by pulsed electron-electron double resonance, using mutant spinach PsbP (Pro20Cys, Ser82Cys, Ala111Cys, and Ala186Cys) labeled with 4-maleimido-TEMPO (MSL) spin label. The distances between the spin label and the Tyr160 neutral radical (YD) in PsbD, the D2 subunit of plant photosystem II, were 50.8 ±â€¯3.5 Å, 54.9 ±â€¯4.0 Å, 57.8 ±â€¯4.9 Å, and 58.4 ±â€¯14.1 Å, respectively. The geometry inferred from these distances was fitted to the PsbP crystal structure (PDB: 4RTI) to obtain the coordinates of YD relative to PsbP. These coordinates were then fitted under boundary conditions to the structure of cyanobacterial photosystem II (PDB: 4UB6), by rotating on Euler angles centered at fixed YD coordinates. The result proposed two models which show possible acidic amino acid residues in CP43, CP47 and D2 that can bind the basic amino acids Arg48, Lys143, and Lys160 in PsbP.

Electronic structure of S(2) state of the oxygen-evolving complex of photosystem II studied by PELDOR.

Photosynthetic water splitting is catalyzed by a Mn(4)CaO(5) cluster in photosystem II, whose structure was recently determined at a resolution of 1.9Å [Umena, Y. et al. 2011, Nature, 473:55-60]. To determine the electronic structure of the Mn(4)CaO(5) cluster, pulsed electron-electron double resonance (PELDOR) measurements were performed for the tyrosine residue Y(D)() and S(2) state signals with non-oriented and oriented photosystem II (PS II) samples. Based on these measurements, the spin density distributions were calculated by comparing with the experimental results. The best fitting parameters were obtained with a model in which Mn1 has a large positive projection, Mn3 has a small positive projection, and Mn2 and Mn4 have negative projections (the numbering of Mni (i=1-4) is based on the crystal structure at a 1.9Å resolution), which yielded spin projections of 1.97, -1.20, 1.19 and -0.96 for Mn1-4 ions. The results show that the Mn1 ion, which is coordinated by H332, D342 and E189, has a valence of Mn(III) in the S(2) state. The sign of the exchange interactions J(13) is positive, and the other signs are negative.

Guest-responsive coherence time of radical qubits in a metal-organic framework.

Metal-organic frameworks (MOFs) integrated with molecular qubits are promising for quantum sensing. In this study, a new UiO-type MOF with a 5,12-diazatetracene (DAT)-containing ligand is synthesized, and the radicals generated in the MOF exhibit high stability and a relatively long coherence time (T2) responsive to the introduction of various guest molecules.

Modulation of triplet quantum coherence by guest-induced structural changes in a flexible metal-organic framework.

Quantum sensing has the potential to improve the sensitivity of chemical sensing by exploiting the characteristics of qubits, which are sensitive to the external environment. Modulation of quantum coherence by target analytes can be a useful tool for quantum sensing. Using molecular qubits is expected to provide excellent sensitivity due to the proximity of the sensor to the target analyte. However, many molecular qubits are used at cryogenic temperatures, and how to make molecular qubits respond to specific analytes remains unclear. Here, we propose a material design in which the coherence time changes in response to a variety of analytes at room temperature. We used the photoexcited triplet, which can be initialized at room temperature, as qubits and introduce them to a metal-organic framework that can flexibly change its pore structure in response to guest adsorption. By changing the local molecular density around the triplet qubits by adsorption of a specific analyte, the mobility of the triplet qubit can be changed, and the coherence time can be made responsive.

Radical qubits photo-generated in acene-based metal-organic frameworks.

A series of metal-organic frameworks (MOFs) assembled with diazatetracene (DAT)-based linkers were synthesized and characterized. Despite different chromophore orientations and spacings, photoinduced persistent radicals were generated in all the MOFs, and their spin-lattice relaxation time (T1) and spin-spin relaxation time (T2) were found to be relatively long even at room temperature. The generality of long T1 and T2 values of photogenerated radicals in the chromophore-assembled MOFs provides a new platform towards quantum sensing applications.

Insights into the protonation state and spin structure for the g = 2 multiline electron paramagnetic resonance signal of the oxygen-evolving complex.

In photosystem II (PSII), one-electron oxidation of the most stable oxidation state of the Mn4CaO5 cluster (S1) leads to formation of two distinct states, the open-cubane S2 conformation [Mn1(III)Mn2(IV)Mn3(IV)Mn4(IV)] with low spin and the closed-cubane S2 conformation [Mn1(IV)Mn2(IV)Mn3(IV)Mn4(III)] with high spin. In electron paramagnetic resonance (EPR) spectroscopy, the open-cubane S2 conformation exhibits a g = 2 multiline signal. However, its protonation state remains unclear. Here, we investigated the protonation state of the open-cubane S2 conformation by calculating exchange couplings in the presence of the PSII protein environment and simulating the pulsed electron-electron double resonance (PELDOR). When a ligand water molecule, which forms an H-bond with D1-Asp61 (W1), is deprotonated at dangling Mn4(IV), the first-exited energy (34 cm-1) in manifold spin excited states aligns with the observed value in temperature-dependent pulsed EPR analyses, and the PELDOR signal is best reproduced. Consequently, the g = 2 multiline signal observed in EPR corresponds to the open-cubane S2 conformation with the deprotonated W1 (OH-).

Magnetic structure of manganese cluster in photosystem II investigated by electron paramagnetic resonance.

The electronic structure of manganese (Mn) cluster in photosystem II was investigated by electron paramagnetic resonance (EPR) spectroscopy. In order to determine the spin density distribution in magnetically coupled Mn in the S2 state Mn cluster, pulsed electron-electron double resonance (PELDOR) measurement was performed. The local environment of the Mn cluster was investigated by electron-nuclear double resonance (ENDOR). Using spin projections determined by PELDOR, ENDOR signals were assigned to the water molecules ligated to the Mn cluster. The location of a high-affinity Mn2+ site in apo-photosystem II, which is the initial site of photoactivation of the Mn cluster, was determined by PELDOR.

Two-dimensional sp2 carbon-conjugated covalent organic frameworks.

We synthesized a two-dimensional (2D) crystalline covalent organic framework (sp2c-COF) that was designed to be fully π-conjugated and constructed from all sp2 carbons by C=C condensation reactions of tetrakis(4-formylphenyl)pyrene and 1,4-phenylenediacetonitrile. The C=C linkages topologically connect pyrene knots at regular intervals into a 2D lattice with π conjugations extended along both x and y directions and develop an eclipsed layer framework rather than the more conventionally obtained disordered structures. The sp2c-COF is a semiconductor with a discrete band gap of 1.9 electron volts and can be chemically oxidized to enhance conductivity by 12 orders of magnitude. The generated radicals are confined on the pyrene knots, enabling the formation of a paramagnetic carbon structure with high spin density. The sp2 carbon framework induces ferromagnetic phase transition to develop spin-spin coherence and align spins unidirectionally across the material.

Location of the High-Affinity Mn(2+) Site in Photosystem II Detected by PELDOR.

The location of the high-affinity Mn(2+) site in apo-photosystem (PS) II was investigated by pulsed EPR. The electron-electron magnetic dipole interaction of 1.7 MHz between the YD(•) radical and Mn(2+) ion was observed using the pulsed electron-electron double resonance (PELDOR) technique, and the Mn(2+) ion was bound to one apo-PS II in the absence and presence of Ca(2+). PELDOR signals were calculated using the previously determined spin distribution on the YD(•) radical and its known position in the crystal structure, assuming that the specific Mn(2+) site was located in the oxygen evolving complex. The results show that the high-affinity Mn(2+) site is located at the position denoted by Mn4(A) in the native crystal structure. The Mn(2+) is coordinated with axial ligands Asp170 and Glu333 in the D1 polypeptide.