Characterization of the water oxidizing complex of photosystem II of the Chl d-containing cyanobacterium Acaryochloris marina via its reactivity towards endogenous electron donors and acceptors

Shevela, Dmitriy; Nöring, Birgit; Eckert, Hann-Jörg; Messinger, Johannes; Ренгер, Г.

doi:10.1039/b604389e

Cited by 36 publications

(26 citation statements)

References 35 publications

(50 reference statements)

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“…However, for another study using partially purified samples, a different component (Chl a and Chl d heterodimer) was proposed for the special pair (30). Additionally, in an earlier study, Shevela et al (31) proposed that the redox potentials of the wateroxidizing complex in its different S i states (donor side of PS II) are almost the same for A. marina cells and spinach thylakoids. However, experimental evidence for this interpretation was completely indirect.…”

Section: Discussionmentioning

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

Proc. Natl. Acad. Sci. U.S.A.

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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 ...

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Section: Discussionmentioning

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

Proc. Natl. Acad. Sci. U.S.A.

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“…In a more advanced approach, the fit program also includes (i) the reduced S -1 state and (ii) S i state dependent misses (Isgandarova et al 2003;Messinger et al 1997b;Shevela et al 2006). This extended Kok model is summarized in Eq.…”

Section: Analysis Of Fiopsmentioning

confidence: 99%

“…S 3 and S 3 ? S 0 were set as free running parameters, but fixed to be equal, i.e., a 2 = a 3 (Isgandarova et al 2003;Shevela et al 2006). For b n it is assumed that the double hit of the first flash (b 1 ) is greater or equal to the value of b in the remaining flashes, which are assumed to then cause identical double hits; i.e., b 1 C b 2 = b 3 ….…”

Section: Analysis Of Fiopsmentioning

confidence: 99%

“…Dark-adapted S 1 Y D -tylakoids were excited with one (S 2 state formation) or two (S 3 state formation) pre-flash(es). After various dark times, t d (0.5 to 120 s) the O 2 -yields induced by flash train were recorded and deconvoluted into S i state populations (Isgandarova et al 2003;Shevela et al 2006Shevela et al , 2007.…”

Section: Measurements Of Flash-induced O 2 -Evolution Patterns (Fiops)mentioning

confidence: 99%

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Effects of methanol on the S i -state transitions in photosynthetic water-splitting

Nöring¹,

Shevela

Ренгер

et al. 2008

Photosynth Res

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From a chemical point of view methanol is one of the closest analogues of water. Consistent with this idea EPR spectroscopy studies have shown that methanol binds at-or at least very close to-the Mn 4 O x Ca cluster of photosystem II (PSII). In contrast, Clark-type oxygen rate measurements demonstrate that the O 2 evolving activity of PSII is surprisingly unaffected by methanol concentrations of up to 10%. Here we study for the first time in detail the effect of methanol on photosynthetic water-splitting by employing a Joliot-type bare platinum electrode. We demonstrate a linear dependence of the miss parameter for S i state advancement on the methanol concentrations in the range of 0-10% (v/v). This finding is consistent with the idea that methanol binds in PSII with similar affinity as water to one or both substrate binding sites at the Mn 4 O x Ca cluster. The possibility is discussed that the two substrate water molecules bind at different stages of the cycle, one during the S 4 ? S 0 and the other during the S 2 ? S 3 transition.

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“…Previous work has shown that chlorophylls in both reaction centers, photosystem (PS)I and PSII, have been replaced by Chl d, which absorbs light with a wavelength up to 30 nm red-shifted from Chl a (7,8). Although it was anticipated that the Chl d-PSII in A. marina would harvest insufficient energy to cleave water molecules during oxygen evolution, Shevela et al (9) showed that the redox potential of the A. marina PSII-special pair was within 0.1 eV of that in other cyanobacteria and would thus not present an energetic barrier to water oxidation.…”

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confidence: 99%

Niche adaptation and genome expansion in the chlorophyll d -producing cyanobacterium Acaryochloris marina

Swingley

Chen

Cheung³

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

199

184

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Acaryochloris marina is a unique cyanobacterium that is able to produce chlorophyll d as its primary photosynthetic pigment and thus efficiently use far-red light for photosynthesis. Acaryochloris species have been isolated from marine environments in association with other oxygenic phototrophs, which may have driven the niche-filling introduction of chlorophyll d. To investigate these unique adaptations, we have sequenced the complete genome of A. marina. The DNA content of A. marina is composed of 8.3 million base pairs, which is among the largest bacterial genomes sequenced thus far. This large array of genomic data is distributed into nine single-copy plasmids that code for >25% of the putative ORFs. Heavy duplication of genes related to DNA repair and recombination (primarily recA) and transposable elements could account for genetic mobility and genome expansion. We discuss points of interest for the biosynthesis of the unusual pigments chlorophyll d and ␣-carotene and genes responsible for previously studied phycobilin aggregates. Our analysis also reveals that A. marina carries a unique complement of genes for these phycobiliproteins in relation to those coding for antenna proteins related to those in Prochlorococcus species. The global replacement of major photosynthetic pigments appears to have incurred only minimal specializations in reaction center proteins to accommodate these alternate pigments. These features clearly show that the genus Acaryochloris is a fitting candidate for understanding genome expansion, gene acquisition, ecological adaptation, and photosystem modification in the cyanobacteria.comparative microbial genomics ͉ photosynthesis ͉ oxygenic phototrophs ͉ evolution

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Characterization of the water oxidizing complex of photosystem II of the Chl d-containing cyanobacterium Acaryochloris marina via its reactivity towards endogenous electron donors and acceptors

Cited by 36 publications

References 35 publications

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

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

Effects of methanol on the S i -state transitions in photosynthetic water-splitting

Niche adaptation and genome expansion in the chlorophyll d -producing cyanobacterium Acaryochloris marina

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Characterization of the water oxidizing complex of photosystem II of the Chl d-containing cyanobacterium Acaryochloris marina via its reactivity towards endogenous electron donors and acceptors

Cited by 36 publications

References 35 publications

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

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

Effects of methanol on the S i -state transitions in photosynthetic water-splitting

Niche adaptation and genome expansion in the chlorophyll d -producing cyanobacterium Acaryochloris marina

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Product

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

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