Directly probing redox-linked quinones in photosystem II membrane fragments via UV resonance Raman scattering

Abstract

In photosynthesis, photosystem II (PSII) harvests sunlight with bound pigments to oxidize water and reduce quinone to quinol, which serves as electron and proton mediators for solar-to-chemical energy conversion. At least two types of quinone cofactors in PSII are redox-linked: QA, and QB. Here, we for the first time apply 257-nm ultraviolet resonance Raman (UVRR) spectroscopy to acquire the molecular vibrations of plastoquinone (PQ) in PSII membranes. Owing to the resonance enhancement effect, the vibrational signal of PQ in PSII membranes is prominent. A strong band at 1661 cm(-1) is assigned to ring CC/CO symmetric stretch mode (ν8a mode) of PQ, and a weak band at 469 cm(-1) to ring stretch mode. By using a pump-probe difference UVRR method and a sample jet technique, the signals of QA and QB can be distinguished. A frequency difference of 1.4 cm(-1) in ν8a vibrational mode between QA and QB is observed, corresponding to ~86 mV redox potential difference imposed by their protein environment. In addition, there are other PQs in the PSII membranes. A negligible anharmonicity effect on their combination band at 2130 cm(-1) suggests that the 'other PQs' are situated in a hydrophobic environment. The detection of the 'other PQs' might be consistent with the view that another functional PQ cofactor (not QA or QB) exists in PSII. This UVRR approach will be useful to the study of quinone molecules in photosynthesis or other biological systems.

Encapsulation of a Quinhydrone Cofactor in the Inner Pocket of Cobalt Triangular Prisms: Combined Light‐Driven Reduction of Protons and Hydrogenation of Nitrobenzene

“…[8] Recently,wemodulated the properties of amodel fragment of nicotinamide adenine dinucleotide cofactor in aredox-active molecular flask to combine biomimetic hydrogenation with in situ regeneration of the active site in ao ne-pot reaction using light as aclean energy source. [9] Ther ecognition of the bio-inspired cofactor in the pocket of the molecular flask was postulated to be asimply and easily handled approach to the construction of artificial systems.H erein, we formulated anew system (Scheme 1) that was inspired by the redox relays of photosystem II [10] and involved the encapsulation of aQ HQ cofactor in ar edox-active host. Our host comprises six redox-active cobalt ions connected by three alternating ligands with amide-containing tridentate N 2 Ou nits positioned at the meta sites of the biphenyl rings.W ee nvisioned that the special redox-modulated environment of the metalorganic host and the proximity effects of the host-guest interactions would facilitate the formation of ac harge-transfer complex that is typically too unstable to form in normal homogeneous systems.Extensive electron delocalization and suitable redox potentials could then be engineered into these new complexes to decrease the overpotential of the metal sites for proton reduction and to enhance the efficiency of the hydrogenation of nitrobenzene.…”

Proton-Coupled Electron Transfer of Plastoquinone Redox Reactions in Photosystem II: A Pump–Probe Ultraviolet Resonance Raman Study

“…Most of these bands, except the band at 1661 cm −1 , can be attributed to tryptophan residues and chlorophyll-a (Chl-a) molecules, indicating that the signals of Trp and Chl-a are enhanced to some extent because of the resonance Raman effect. As concluded from the 257 nm-excited Raman characterization of plant thylakoid membranes, 30 the vibrational band at 1661 cm −1 is assigned to the ring C=C/C=O symmetric stretch mode (ν8a mode) of PQ. For comparison, we also investigated the Mn-depleted PSII sample in which the Mn 4 CaO 5 cluster was removed.…”

“…These pump−probe spectral features at 257 nm-excited Raman scattering of the PSII core from the cyanobacterium T. vulcanus are similar to those of plant thylakoid membranes. 30 For the Mn-depleted PSII, the difference spectrum (Figure 3Bc) from the pump−probe measurements shows many different features when compared to the native PSII sample, e.g., positive bands are present at 1696, 1623, 1565, 1509, 1410, 1160, 980, and 816 cm −1 in addition to the negative band at 1660 cm −1 .…”

“…28 Previously, we observed the greatly resonanceenhanced Raman signal of PQ in plant thylakoid membranes with excitation at 257 nm wavelength, showing the ν8a mode at 1661 cm −1 , whose shift in frequency can be correlated with the redox potential regulation between Q A and Q B . 30 Here we apply ultraviolet resonance Raman (UVRR) spectroscopy at 257 and 244 nm excitations to directly probe the PQs and their chemical bond vibrations in the PSII from a thermophilic cyanobacterium, Thermosynechococcus vulcanus (T. vulcanus). By developing a pump−probe approach in combination with a sample jet technique, we are able to observe the structural changes of Q A upon electron-transfer reactions directly and therefore propose a regulation mechanism of Q A redox for photoprotection.…”

Encapsulation of a Quinhydrone Cofactor in the Inner Pocket of Cobalt Triangular Prisms: Combined Light‐Driven Reduction of Protons and Hydrogenation of Nitrobenzene

“…[7] Thef undamental transformations of biological syntheses include large numbers of redox events. [9] Ther ecognition of the bio-inspired cofactor in the pocket of the molecular flask was postulated to be asimply and easily handled approach to the construction of artificial systems.H erein, we formulated anew system (Scheme 1) that was inspired by the redox relays of photosystem II [10] and involved the encapsulation of aQ HQ cofactor in ar edox-active host. [9] Ther ecognition of the bio-inspired cofactor in the pocket of the molecular flask was postulated to be asimply and easily handled approach to the construction of artificial systems.H erein, we formulated anew system (Scheme 1) that was inspired by the redox relays of photosystem II [10] and involved the encapsulation of aQ HQ cofactor in ar edox-active host.…”