Post-translational amino acid conversion in photosystem II as a possible origin of photosynthetic oxygen evolution.
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ABSTRACT:
SUBMITTER: Shimada Y
PROVIDER: S-EPMC9304363 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Two major geological problems regarding the origin of oxygenic photosynthesis are (i) identifying a source of oxygen pre-dating the biological oxygen production and capable of driving the evolution of oxygen tolerance, and (ii) determining when oxygenic photosynthesis evolved. One solution to the first problem is the accumulation of photochemically produced H(2)O(2) at the surface of the glaciers and its subsequent incorporation into ice. Melting at the glacier base would release H(2)O(2), which interacts with seawater to produce O(2) in an environment shielded from the lethal levels of ultraviolet radiation needed to produce H(2)O(2). Answers to the second problem are controversial and range from 3.8 to 2.2 Gyr ago. A sceptical view, based on the metals that have the redox potentials close to oxygen, argues for the late end of the range. The preponderance of geological evidence suggests little or no oxygen in the Late Archaean atmosphere (less than 1 ppm). The main piece of evidence for an earlier evolution of oxygenic photosynthesis comes from lipid biomarkers. Recent work, however, has shown that 2-methylhopanes, once thought to be unique biomarkers for cyanobacteria, are also produced anaerobically in significant quantities by at least two strains of anoxygenic phototrophs. Sterane biomarkers provide the strongest evidence for a date 2.7 Gyr ago or above, and could also be explained by the common evolutionary pattern of replacing anaerobic enzymes with oxygen-dependent ones. Although no anaerobic sterol synthesis pathway has been identified in the modern biosphere, enzymes that perform the necessary chemistry do exist. This analysis suggests that oxygenic photosynthesis could have evolved close in geological time to the Makganyene Snowball Earth Event and argues for a causal link between the two.
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Project description:An open question regarding the evolution of photosynthesis is how cyanobacteria came to possess the two reaction center (RC) types, Type I reaction center (RCI) and Type II reaction center (RCII). The two main competing theories in the foreground of current thinking on this issue are that either 1) RCI and RCII are related via lineage divergence among anoxygenic photosynthetic bacteria and became merged in cyanobacteria via an event of large-scale lateral gene transfer (also called "fusion" theories) or 2) the two RC types are related via gene duplication in an ancestral, anoxygenic but protocyanobacterial phototroph that possessed both RC types before making the transition to using water as an electron donor. To distinguish between these possibilities, we studied the evolution of the core (bacterio)chlorophyll biosynthetic pathway from protoporphyrin IX (Proto IX) up to (bacterio)chlorophyllide a. The results show no dichotomy of chlorophyll biosynthesis genes into RCI- and RCII-specific chlorophyll biosynthetic clades, thereby excluding models of fusion at the origin of cyanobacteria and supporting the selective-loss hypothesis. By considering the cofactor demands of the pathway and the source genes from which several steps in chlorophyll biosynthesis are derived, we infer that the cell that first synthesized chlorophyll was a cobalamin-dependent, heme-synthesizing, diazotrophic anaerobe.
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Project description:Photosystem II (PSII) is an intrinsic membrane protein complex that functions as a light-driven water:plastoquinone oxidoreductase in oxygenic photosynthesis. Electron transport in PSII is associated with formation of reactive oxygen species (ROS) responsible for oxidative modifications of PSII proteins. In this study, oxidative modifications of the D1 and D2 proteins by the superoxide anion (O2•-) and the hydroxyl (HO•) radicals were studied in WT and a tocopherol cyclase (vte1) mutant, which is deficient in the lipid-soluble antioxidant α-tocopherol. In the absence of this antioxidant, high-resolution tandem mass spectrometry was used to identify oxidation of D1:130E to hydroxyglutamic acid by O2•- at the PheoD1 site. Additionally, D1:246Y was modified to either tyrosine hydroperoxide or dihydroxyphenylalanine by O2•- and HO•, respectively, in the vicinity of the nonheme iron. We propose that α-tocopherol is localized near PheoD1 and the nonheme iron, with its chromanol head exposed to the lipid-water interface. This helps to prevent oxidative modification of the amino acid's hydrogen that is bonded to PheoD1 and the nonheme iron (via bicarbonate), and thus protects electron transport in PSII from ROS damage.
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Project description:2-Amino-1,1,3-tricyanopropene inhibits photosynthetic O(2) evolution, but, unlike 3-(3,4-dichlorophenyl)-1,1-dimethylurea, has little effect on the steady-state fluorescence of chlorophyll. In chloroplasts prepared from spinach leaves and inhibited by 2-amino-1,1,3-tricyanopropene, a 3-(3,4-dichlorophenyl)-1,1-dimethylurea-sensitive photoreduction of ferricyanide may be restored by addition of semicarbazide. It is concluded that 2-amino-1,1,3-tricyanopropene acts at a point close to the photo-oxidation of water.
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Project description:In photosynthesis, photosystem II evolves oxygen from water by the accumulation of photooxidizing equivalents at the oxygen-evolving complex (OEC). The OEC is a Mn4CaO5 cluster, and its sequentially oxidized states are termed the Sn states. The dark-stable state is S1, and oxygen is released during the transition from S3 to S0. In this study, a laser flash induces the S1 to S2 transition, which corresponds to the oxidation of Mn(III) to Mn(IV). A broad infrared band, at 2,880 cm(-1), is produced during this transition. Experiments using ammonia and (2)H2O assign this band to a cationic cluster of internal water molecules, termed "W5(+)." Observation of the W5(+) band is dependent on the presence of calcium, and flash dependence is observed. These data provide evidence that manganese oxidation during the S1 to S2 transition results in a coupled proton transfer to a substrate-containing, internal water cluster in the OEC hydrogen-bonded network.
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Project description:In oxygenic photosynthesis, photosystem II (PSII) is the multisubunit membrane protein responsible for the oxidation of water to O2 and the reduction of plastoquinone to plastoquinol. One electron charge separation in the PSII reaction center is coupled to sequential oxidation reactions at the oxygen-evolving complex (OEC), which is composed of four manganese ions and one calcium ion. The sequentially oxidized forms of the OEC are referred to as the S(n) states. S(1) is the dark-adapted state of the OEC. Flash-induced oxygen production oscillates with period four and occurs during the S(3) to S(0) transition. Chloride plays an important, but poorly understood role in photosynthetic water oxidation. Chloride removal is known to block manganese oxidation during the S(2) to S(3) transition. In this work, we have used azide as a probe of proton transfer reactions in PSII. PSII was sulfate-treated to deplete chloride and then treated with azide. Steady state oxygen evolution measurements demonstrate that azide inhibits oxygen evolution in a chloride-dependent manner and that azide is a mixed or noncompetitive inhibitor. This result is consistent with two azide binding sites, one at which azide competes with chloride and one at which azide and chloride do not compete. At pH 7.5, the K(i) for the competing site was estimated as 1 mM, and the K(i)' for the uncompetitive site was estimated as 8 mM. Vibrational spectroscopy was then used to monitor perturbations in the frequency and amplitude of the azide antisymmetric stretching band. These changes were induced by laser-induced charge separation in the PSII reaction center. The results suggest that azide is involved in proton transfer reactions, which occur before manganese oxidation, on the donor side of chloride-depleted PSII.
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Project description:The chloride ion, Cl(-), is an essential cofactor for oxygen evolution of photosystem II (PSII) and is closely associated with the Mn(4)Ca cluster. Its detailed location and function have not been identified, however. We substituted Cl(-) with a bromide ion (Br(-)) or an iodide ion (I(-)) in PSII and analyzed the crystal structures of PSII with Br(-) and I(-) substitutions. Substitution of Cl(-) with Br(-) did not inhibit oxygen evolution, whereas substitution of Cl(-) with I(-) completely inhibited oxygen evolution, indicating the efficient replacement of Cl(-) by I(-). PSII with Br(-) and I(-) substitutions were crystallized, and their structures were analyzed. The results showed that there are 2 anion-binding sites in each PSII monomer; they are located on 2 sides of the Mn(4)Ca cluster at equal distances from the metal cluster. Anion-binding site 1 is close to the main chain of D1-Glu-333, and site 2 is close to the main chain of CP43-Glu-354; these 2 residues are coordinated directly with the Mn(4)Ca cluster. In addition, site 1 is located in the entrance of a proton exit channel. These results indicate that these 2 Cl(-) anions are required to maintain the coordination structure of the Mn(4)Ca cluster as well as the proposed proton channel, thereby keeping the oxygen-evolving complex fully active.
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Project description:We investigated the effects of elevated O(2) pressure on the production of O(2) by photosynthetic organisms in several species of plants, algae, and a cyanobacterium. Using a noninvasive fluorometry technique to monitor sequential turnover of the photosystem II (PSII) reaction center as a function of O(2) pressures, we showed that none of the reactions of water oxidation are affected by elevated O(2) pressures up to 50-fold greater than atmospheric conditions. Thus, the terminal step of O(2) release from the water oxidation complex (S(4) --> S(0) + O(2) + nH(+)) is not reversible in whole cells, leaves, or isolated thylakoid membranes containing PSII, in contrast to reports using detergent-extracted PSII complexes. This implies that there is no thermodynamically accessible intermediate that can be populated by preventing or reversing the O(2) release step with O(2) at atmospheric pressure. To assess the sensitivity of PSII charge recombination to O(2) pressure, we quantitatively modeled the consequences of two putative perturbations to the catalytic cycle of water oxidation within the framework of the Kok model. On the basis of the breadth of oxygenic phototrophs examined in this study, we conclude that O(2) accumulation in cells or the atmosphere does not suppress photosynthetic productivity through the reversal of water oxidation in contemporary phototrophs and would have been unlikely to influence the evolution of oxygenic photosynthesis.
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Project description:Land plants encountering low water potentials (low psiw) close their stomata, restricting CO2 entry and potentially photosynthesis. To determine the impact of stomatal closure, photosynthetic O2 evolution was investigated in leaf discs from sunflower (Helianthus annuus L.) plants after removing the lower epidermis at low psiw. Wounding was minimal as evidenced by O2 evolution nearly as rapid as that in intact discs. O2 evolution was maximal in 1% CO2 in the peeled discs and was markedly inhibited when psiw was below -1.1 MPa. CO2 entered readily at all psiw, as demonstrated by varying the CO2 concentration. Results were the same whether the epidermis was removed before or after low psiw was imposed. Due to the lack of an epidermis and ready movement or CO2 through the mesophyll, the loss in O2 evolving activity was attributed entirely to photosynthetic metabolism. Intact leaf discs showed a similar loss in activity when measured at a CO2 concentration of 5%, which supported maximum O2 evolution at low psiw. In 1% CO2, however, O2 evolution at low psiw was below the maximum, presumably because stomatal closure restricted CO2 uptake. The inhibition was larger than in peeled discs at psiw between -1 and -1.5 MPa but became the same as in peeled discs at lower psiw. Therefore. as photosynthesis began to be inhibited by metabolism at low psiw, stomatal closure added to the inhibition. As psiw became more negative, the inhibition became entirely metabolic.
| S-EPMC4233803 | biostudies-literature
Project description:Photosystem II is a photochemical reaction center that catalyzes the light-driven oxidation of water to molecular oxygen. Water oxidation is the distinctive photochemical reaction that permitted the evolution of oxygenic photosynthesis and the eventual rise of eukaryotes. At what point during the history of life an ancestral photosystem evolved the capacity to oxidize water still remains unknown. Here, we study the evolution of the core reaction center proteins of Photosystem II using sequence and structural comparisons in combination with Bayesian relaxed molecular clocks. Our results indicate that a homodimeric photosystem with sufficient oxidizing power to split water had already appeared in the early Archean about a billion years before the most recent common ancestor of all described Cyanobacteria capable of oxygenic photosynthesis, and well before the diversification of some of the known groups of anoxygenic photosynthetic bacteria. Based on a structural and functional rationale, we hypothesize that this early Archean photosystem was capable of water oxidation to oxygen and had already evolved protection mechanisms against the formation of reactive oxygen species. This would place primordial forms of oxygenic photosynthesis at a very early stage in the evolutionary history of life.
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