Direct !AgO2 Generation by Triplet-triplet Interaction

The ground state of the most molecules including biological materials (proteins, lipids, carbohydrates) has a closed electron shell with singlet spin configuration. These spin state properties are of paramount importance, because the transition state of the two electron oxidation of a molecule in the singlet state by 32 g O2 is “spin-forbidden” and, therefore, the reaction is very slow. This also accounts for the back reaction from the singlet to the triplet state. This situation drastically changes through two types of reactions which transform 32 g O2 into highly reactive oxygen species (ROS): i) Electronic excitation leads to population of two forms of singlet O2 characterized by the term symbols 3Ag and 12 g . The 12 g state with slightly higher energy rapidly relaxes into 1AgO2 so that only the latter species is of physiological relevance (type I). ii) Chemical reduction of 32g O2 (or 1AgO2) by radicals with non-integer spin state (often doublet state) leads to formation of O 2*, which quickly reacts to HO 2 and is subsequently transferred to H2O2 and HO* (vide infra) (type II). In plants, the electronic excitation of 3 2 g O2 occurs due to close contact to chlorophyll triplets that are produced during the photoexcitation cycle (Schmitt et al., 2014a) (see eq. 63, Figure 52, Figure 53). Singlet oxygen is predominantly formed via the reaction sensitized by interaction between a chlorophyll triplet (3Chl) and ground state triplet 3 2 g O2:

3Chl can be populated either via intersystem crossing (ISC) of antenna Chls or via radical pair recombination in the reaction centers (RCs) of photosystem II (PS II) (for reviews, see Vass and Aro, 2008; Renger, 2008; Rutherford et al., 2012; Schmitt et al., 2014a). Alternatively, 1AgO2 can also be formed in a controlled fashion by chemical reactions, which play an essential role in programmed cell death upon pathogenic infections (e.g. by viruses).

Production of ROS by interaction of oxygen with Chlorophyll triplet states (type I) to Ю or chemical reduction of oxygen to O (type II)

Figure 52. Production of ROS by interaction of oxygen with Chlorophyll triplet states (type I) to Ю2 or chemical reduction of oxygen to O (type II).

Figure 53 schematically illustrates the pattern of one-electron redox

steps of oxygen forming the ROS species HO*, H2O2 and HO2/Oin a four-step reaction sequence with water as the final product. The sequence comprises the water splitting, leading from water to O2 + 4H+ and the corresponding mechanism vice versa of the ROS reaction sequence. The production of :Ag O2 is a mechanism next to that.

The singlet state :AgO2 has a long intrinsic lifetime decaying during phosphorescence emission with maximum at 1268 nm. However, it can decay via both radiative and especially non-radiative routes. The lifetime of 1AgO2 is especially speeded up from its natural half time of 72 min. by collisions with other molecules and its high reactivity (Mattila et al., 2015).

Rapid non-radiative decay of both singlet forms of oxygen ^ g O2 and :AgO2 occurs via (i) conversion of excitation energy of g O2 and

:AgO2 to vibrational and rotational energy and (ii) a charge-transfer mechanism and (iii) electronic energy transfer (Mattila et al., 2015).

Electronic energy transfer of g O2 and :AgO2 and a singlet ground state of a quenching molecule produces a triplet state of both the quencher and oxygen.

The final lifetime of :AgO2 in aqueous solution is about 3.5 ps (Egorov et al., 1989). But in cells the broad variety of reactive protein residua, lipids and other ROS together with the high reactivity of :AgO2 finally reduces the lifetime to a regime in the order of 200 ns reported for :AgO2

Scheme of ROS formation and water redox chemistry (water-water cycle) according to (Schmitt et al., 2014a). Image reproduced with permission

Figure 53. Scheme of ROS formation and water redox chemistry (water-water cycle) according to (Schmitt et al., 2014a). Image reproduced with permission.

in cells (Gorman and Rogers, 1992) so that the species can diffuse not much more than 10 nm under physiological conditions (Sies and Menck, 1992), thus permitting penetration through membranes (Schmitt et al., 2014a). But also distances up to 25 nm have been reported (Moan, 1990) suggesting that :AgO2 can permeate through the cell wall of E. coli. The singlet oxygen chemistry significantly depends on the environment, solvent conditions and the temperature (Ogilby and Foote, 1983). Higher values of up to 14 gs lifetime and 400 nm diffusion distance in lipid membranes suggest that AgO2 can indeed diffuse across membranes of cell organelles and cell walls (Baier et al., 2005). But as most proteins are prominent targets (Davies, 2003) with reaction rate constants in the range of 108—109 M-1s-1 the potential of :AgO2 to work directly as a messanger is rather limited (Wilkinson et al., 1995). Among the canonical amino acids, only five (Tyr, His, Trp, Met and Cys) are primarily attacked by a chemical reaction with :AgO2, from which Trp is unique by additionally exhibiting a significant physical deactivation channel that leads to the ground state 32g O2 in a similar way as by quenching with carotenoids. The reaction of :AgO2 with Trp primarily leads to the formation of peroxides, which are subsequently degraded into different stable products. One of these species is N-formylkynurenine (Gracanin et al., 2009). This compound exhibits optical and Raman spectroscopic characteristics that might be useful for the identification of ROS generation sites (Kasson and Barry, 2012). The reactivity of Trp in proteins was shown to markedly depend on the local environment of the target (Jensen et al., 2012). Detailed mass spectrometric studies revealed that a large number of oxidative modifications of amino acids are caused by ROS and reactive nitrogen species (Galetskiy et al., 2011).

The wealth of studies on damage of the photosynthetic apparatus (PA) by :AgO2 under light stress and repair mechanisms is described in several reviews and book chapters on photoinhibition (Li et al., 2012; Vass and Aro, 2008; Adir et al., 2003, Allakhverdiev and Murata, 2004; Nishiyama et al., 2006; Murata et al., 2007; Li et al., 2009; Goh et al., 2012, Allahverdiyeva and Aro, 2012). Such high reactivity leads to an extensive oxidation of fundamental structures of PS II where oxygen is formed in the water-oxidizing complex. :AgO2 is directly involved in the direct damage of PS II (Mishra et al., 1994, Hideg et al., 2007; Triantaphylides et al., 2008, Triantaphylides and Havaux, 2009; Vass and Cser, 2009), destroying predominantly the D1 protein, which plays a central role in the primary processes of charge separation and stabilization in PS II. The resulting photoinhibition of PS II (Nixon et al., 2010) leads to dysfunction of D1 and high turnover rates during the so called D1-repair cycle. D1 by far exhibits the highest turnover rate of all thylakoid proteins and underlies complex regulatory mechanisms (Loll et al., 2008).

Carotenoids play a pivotal role in 3Chl suppression and quenching (Frank et al., 1993; Pogson et al., 2005) but also direct depletion of :AgO2. In addition, NPQ developed under light stress also reduces the population of 3Chl in antenna systems as well as PSII of plants (Hartel et al., 1996; Carbonera et al., 2012, Ruban et al., 2012). The interaction between :AgO2 and singlet ground state carotenoids does not only lead to photophysical quenching, but also to oxidation of carotenoids by formation of species that can act as signal molecules for stress response (Ramel et al., 2012). Likewise, lipid (hydro)peroxides generated upon oxidation of polyunsaturated fatty acids by :AgO2 can act as triggers to initiate signal pathways, and propagation of cellular damage (Galvez- Valdivieso and Mullineaux, 2010; Triantaphylides and Havaux, 2009). Further mechanisms of :AgO2 generation and decay together with detailed reaction scemes of :AgO2 are shown in (Mattila et al., 2015). Detailed studies of the damage of the PA by :AgO2 are additionaly found in (Li et al., 2012; Allakhverdiev and Murata, 2004; Nishiyama at al., 2006; Allakhverdiyeva and Aro, 2012; Goh et al., 2012; Nishiyama at al., 2006).

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