Glycinebetaine protects the D1/D2/Cytb559 complex of photosystem II against photo-induced and heat-induced inactivation

125

127

The composition of photosystem II (PSII) in the chlorophyll (Chl) d-dominated cyanobacterium Acaryochloris marina MBIC 11017 was investigated to enhance the general understanding of the energetics of the PSII reaction center. We first purified photochemically active complexes consisting of a 47-kDa Chl protein (CP47), CP43 (PcbC), D1, D2, cytochrome b 559, PsbI, and a small polypeptide. The pigment composition per two pheophytin (Phe) a molecules was 55 ؎ 7 Chl d, 3.0 ؎ 0.4 Chl a, 17 ؎ 3 ␣-carotene, and 1.4 ؎ 0.2 plastoquinone-9. The special pair was detected by a reversible absorption change at 713 nm (P713) together with a cation radical band at 842 nm. FTIR difference spectra of the specific bands of a 3-formyl group allowed assignment of the special pair. The combined results indicate that the special pair comprises a Chl d homodimer. The primary electron acceptor was shown by photoaccumulation to be Phe a, and its potential was shifted to a higher value than that in the Chl a/Phe a system. The overall energetics of PSII in the Chl d system are adjusted to changes in the redox potentials, with P713 as the special pair using a lower light energy at 713 nm. Taking into account the reported downward shift in the potential of the special pair of photosystem I (P740) in A. marina, our findings lend support to the idea that changes in photosynthetic pigments combine with a modification of the redox potentials of electron transfer components to give rise to an energetic adjustment of the total reaction system. Acaryochloris marina ͉ FTIR ͉ reaction center ͉ photosynthesis ͉ electron transfer C hlorophyll (Chl) a has a ubiquitous role as an electron donor in the photochemical reactions of oxygenic photosynthesis, in which two kinds of photosystem, namely photosystem I (PSI) and photosystem II (PSII), cooperatively drive photosynthetic electron flow from water to NADP ϩ . The reduced cofactor, NADPH, is then used for CO 2 fixation. Chl a is a key pigment that serves as an electron donor called the special pair in PSI and PSII. Acaryochloris spp. are unique cyanobacteria that differ from the majority of photosynthetic organisms by having Chl d (3-desvinyl-3-formyl Chl a) (1-4) as the major pigment (Ͼ95%); Chl a is a minor component but is never absent (5, 6). In photosynthetic organisms, changes in pigment composition affect both the function of pigments and their reaction environments, including the modified proteins that accommodate them. Photosynthetic pigments function in two roles: as lightharvesting components and as electron transfer components. Light harvesting is mainly governed by the orientation and energy levels of pigments, and, in this context, a particular excitation energy level is not an absolute precondition for function, but a relative one. On the other hand, electron transfer reactions are governed by an absolute redox potential, because the photosynthetic oxidation of water requires a very high potential, whereas reduction of NADP ϩ requires a very low potential. For this reason, it is of particul...

Section: Resultsmentioning

confidence: 99%

Identification of the special pair of photosystem II in a chlorophyll d -dominated cyanobacterium

Tomo

Okubo

Akimoto

et al. 2007

125

127

“…Betaine stabilizes PS II complexes under stress conditions such as dehydration (34), heat (35,36), cold (37), and osmotic pressure (38). These effects may result from an overall stabilization of the structure of PS II or more directly, from binding of peripheral proteins needed for water oxidation to the PS II core complex (39).…”

Section: Discussionmentioning

confidence: 99%

Redox potential of pheophytin a in photosystem II of two cyanobacteria having the different special pair chlorophylls

Allakhverdiev

Tomo

Shimada

et al. 2010

Self Cite

Water oxidation by photosystem (PS) II in oxygenic photosynthetic organisms is a major source of energy on the earth, leading to the production of a stable reductant. Mechanisms generating a high oxidation potential for water oxidation have been a major focus of photosynthesis research. This potential has not been estimated directly but has been measured by the redox potential of the primary electron acceptor, pheophytin (Phe) a. However, the reported values for Phe a are still controversial. Here, we measured the redox potential of Phe a under physiological conditions (pH 7.0; 25°C) in two cyanobacteria with different special pair chlorophylls (Chls): Synechocystis sp. PCC 6803, whose special pair for PS II consists of Chl a, and Acaryochloris marina MBIC 11017, whose special pair for PS II consists of Chl d. We obtained redox potentials of −536 ± 8 mV for Synechocystis sp. PCC 6803 and −478 ± 24 mV for A. marina on PS II complexes in the presence of 1.0 M betaine. The difference in the redox potential of Phe a between the two species closely corresponded with the difference in the light energy absorbed by Chl a versus Chl d. We estimated the potentials of the special pair of PS II to be 1.20 V and 1.18 V for Synechocystis sp. PCC 6803 (P680) and A. marina (P713), respectively. This clearly indicates conservation in the properties of water-oxidation systems in oxygenic photosynthetic organisms, irrespective of the special-pair chlorophylls.hotosynthesis mediates the conversion of solar light energy to chemical-bond energy through multistep reactions. Two photosystems (PSs) are present in oxygenic photosynthetic organisms, and these two PSs function cooperatively to capture light energy and drive electron flow. PS II supplies an energy source (i.e., an electron) by water oxidation, and PS I supplies a highly reduced compound, NADPH, to reduce CO 2 to carbohydrates.Reaction processes in the electron transfer system in photosynthesis are governed by two major factors: the relative geometry and the redox potentials of the electron transfer components. The molecular environment supplied by the amino acid matrix of the components will give a supplemental effect(s). Crystal structures of PS II complexes at atomic resolution have been reported from several laboratories (1-4). Thus, with the exception of some inconsistencies in the water-oxidation reaction system, an essential part of the primary charge separation machinery has been characterized (5). The electron transfer mechanisms, in contrast,have not yet been clarified in most cases.Pheophytin (Phe) a is the primary electron acceptor in PS II (6-8), although the primary electron donor of PS II is still controversial [P680 or accessory chlorophyll (Chl) a] (9, 10). These two are not in disagreement with respect to the nature of the primary charge separation, but they differ in the value of rate constants and the question of "transfer to the trap limited" or "trap-limited reaction" (5). In this report, we used the term the special pair instead of the primary electron...

“…Titration. All experiments were performed in the presence of betaine, a natural osmolyte, at pH 7.0, because it has previously been shown that PS II preparations are more stable in the presence of 1 M glycine betaine (12,(38)(39)(40)(41)(42)(43). Details of the physiological conditions used for various species are summarized in SI Materials and Methods, Figs.…”

Section: Methodsmentioning

confidence: 99%

Redox potentials of primary electron acceptor quinone molecule (Q _A ) ⁻ and conserved energetics of photosystem II in cyanobacteria with chlorophyll a and chlorophyll d

Allakhverdiev

Watabe

Kojima

et al. 2011

Self Cite

In a previous study, we measured the redox potential of the primary electron acceptor pheophytin (Phe) a of photosystem (PS) II in the chlorophyll d-dominated cyanobacterium Acaryochloris marina and a chlorophyll a-containing cyanobacterium, Synechocystis. We obtained the midpoint redox potential (E m ) values of −478 mV for A. marina and −536 mV for Synechocystis. In this study, we measured the redox potentials of the primary electron acceptor quinone molecule (Q A ), i. ) of A. marina was determined to be +64 mV without the Mn cluster and was estimated to be −66 to −86 mV with a Mn-depletion shift (130-150 mV), as observed with other organisms. The E m (Phe a/Phe a − ) in Synechocystis was measured to be −525 mV with the Mn cluster, which is consistent with our previous report. The Mn-depleted downshift of the potential was measured to be approximately −77 mV in Synechocystis, and this value was applied to A. marina (−478 mV); the E m (Phe a/Phe a − ) was estimated to be approximately −401 mV. These values gave rise to a ΔG PhQ of −325 mV for A. marina and −383 mV for Synechocystis. In the two cyanobacteria, the energetics in PS II were conserved, even though the potentials of Q A − and Phe a − were relatively shifted depending on the special pair, indicating a common strategy for electron transfer in oxygenic photosynthetic organisms.photosynthesis | photochemical reaction C hlorophylls (Chls) are key pigments for photosynthesis, and oxygenic photosynthetic organisms containing Chls are found all over the world-they sustain all terrestrial life through the primary production of organic molecules and the production of oxygen. Chl a and its derivatives, pheophytin (Phe) a and Chl a epimer (Chl a′), are used as the electron transfer components in photosystem (PS) II and PS I, respectively, except for in two taxonomic groups, marine cyanobacteria Prochlorococcus spp. containing divinyl-Chl a (1) and marine cyanobacteria Acaryochloris spp. containing Chl d (2). Consequently, experimental and theoretical analyses of the electron transfer system in oxygenic photosynthesis have been exclusively performed in Chl a-containing organisms, and the basic concept of the photosynthetic electron flow has been constructed on the basis of Chl a. However, our understanding of photosynthetic electron transfer is not yet complete because the reaction systems with divinyl-Chl a and Chl d have not been fully analyzed as yet.Since the discovery of Chl d in Acaryochloris marina in 1996 (3, 4), questions have arisen on the whether the electron transfer system in this organism is significantly different from those with Chl a. Interestingly, the functional "special pair" are Chl d molecules in the reaction centers of PS I and II in A. marina (5, 6); however, in PS II, Phe a is the primary electron acceptor. Chl d gains light energy at longer wavelengths and with a lowered redox potential, by ∼80 mV, compared with that of Chl a in Synechocystis sp. PCC 6803 (hereafter referred to as Synechocystis) and spinach (7-11). However, the overall ...