Tyrosine-Z in Oxygen-Evolving Photosystem II:  A Hydrogen-Bonded Tyrosinate

Abstract

In oxygen-evolving photosystem II (PSII), a tyrosine residue, D1Tyr161 (Y Z ), serves as the intermediate electron carrier between the catalytic Mn cluster and the photochemically active chlorophyll moiety P 680 . A more direct catalytic role of Y Z , as a hydrogen abstractor from bound water, has been postulated. That Y Z ox appears as a neutral (i.e. deprotonated) radical, Y Z • , in EPR studies is compatible with this notion. Data based on electrochromic absorption transients, however, are conflicting because they indicate that the phenolic proton remains on or near to Y Z ox . In Mn-depleted PSII the electron transfer between Y Z and P 680 + can be almost as fast as in oxygen-evolving material, however, only at alkaline pH. With an apparent pK of about 7 the fast reaction is suppressed and converted into an about 100-fold slower one which dominates at acid pH. In the present work we investigated the optical difference spectra attributable to the transition Y Z f Y Z ox as function of the pH. We scanned the UV and VIS range and used Mn-depleted PSII core particles and also oxygen-evolving ones. Comparing these spectra with published in vitro and in vivo spectra of phenolic compounds, we arrived at the following conclusions: In oxygen-evolving PSII Y Z resembles a hydrogen-bonded tyrosinate, Y Z (-) ‚‚‚H (+) ‚B. The phenolic proton is shifted toward a base B already in the reduced state and even more so in the oxidized state. The retention of the phenolic proton in a hydrogen-bonded network gives rise to a positive net charge in the immediate vicinity of the neutral radical Y Z • . It may be favorable both for the very rapid reduction by Y Z of P 680 + and for electron (not hydrogen) abstraction by Y Z • from the Mn-water cluster.Photosystem II (PSII) 1 produces molecular oxygen from water. It is located in photosynthetic membranes of plants and cyanobacteria. The inner core of PSII is a heterodimer of the D1D2 subunits which show homology with the L and M subunits of the purple bacterial RC (1). The primary electron donor of PSII, P 680 , is located close to the lumenal side of the membrane. The absorption of a quantum of light drives the charge separation between P 680 and the quinone acceptor at the stromal side (2). The very high redox potential of P 680 + drives water oxidation. It is a four-stepped process with at least four increasingly oxidized, metastable states S 0 to S 3 , plus a transient state S 4 that decays in milliseconds into S 0 under release of O 2 . P 680 + is reduced (in nanoseconds) by a redox-active tyrosine residue, Y Z (D1Tyr161 (3, 4)). Y Z ox is, in turn, reduced in microseconds by the oxygenevolving complex (OEC). The structure and exact location of the OEC is still ill-defined. It is formed by four manganese atoms (5, 6), possibly another redox cofactor, X (7-9), plus at least one Cl -ion (10) and one Ca 2+ (11, 12) ion. These cofactors serve various functions during water oxidation: The Mn cluster stores at least two of the oxidizing equivalents (namely on transitions S ...

B3LYP studies of the formation of neutral tyrosyl radical Yz⋅ and regeneration of neutral tyrosine Yz in PSII

“…In this case, the neutral tyrosyl radical is ready to accept a new proton or H atom from the manganese cluster. This result, however, contradicts Junge's flash spectrometry results, which suggests that histidine is present in its charged form, i.e., Y z · --H + -His [17]. One of the key points is hence whether a hydrogen atom or a proton (following or preceding electron transfer) can transfer from the manganese cluster water via a water bridge (5-10 Å) to the tyrosyl radical or anion, if the proton (connecting to histidine) has already been transferred into the bulk.…”

The mechanism for proton–coupled electron transfer from tyrosine in a model complex and comparisons with Y Z oxidation in photosystem II

“…Other mechanisms for tyrosine oxidation in Mndepleted PSII at high pH have been suggested, e.g. a consecutive PTET (Ahlbrink et al 1998;Diner et al 1998;Haumann et al 1999;Rappaport & Lavergne 2001). We showed in § 2 1 that when tyrosine is not hydrogen bonded to a base, deprotonation is too slow to explain the observed microsecond rates.…”

Evidence That Bicarbonate Is Not the Substrate in Photosynthetic Oxygen Evolution

“…After addition of the electron acceptor (200 mM 2,5-dichloro-p-benzoquinone), the sample was excited under pressure with a group of five flashes from a Q-switched Nd-YAG laser (wavelength 532 nm, duration 6 ns FWHM, saturating energy, 100 ms between flashes) and the absorption transients were recorded at a wavelength of 360 nm. This wavelength was chosen to reveal charge transfer bands of the Mn 4 Ca complex with minimal contributions from Tyr (Dekker et al, 1984;Schatz and van Gorkom, 1985;Weiss and Renger, 1986;Gerken et al, 1989;Haumann et al, 1999). Data were recorded at an analog bandwidth of 10 kHz and digitized at 50 ms or 100 ms per bin.…”