BBA - Bioenergetics (v.1857, #9)
Editorial Board (i).
The H-bond network surrounding the pyranopterins modulates redox cooperativity in the molybdenum-bisPGD cofactor in arsenite oxidase by Simon Duval; Joanne M. Santini; David Lemaire; Florence Chaspoul; Michael J. Russell; Stephane Grimaldi; Wolfgang Nitschke; Barbara Schoepp-Cothenet (1353-1362).
While the molybdenum cofactor in the majority of bisPGD enzymes goes through two consecutive 1-electron redox transitions, previous protein-film voltammetric results indicated the possibility of cooperative (n = 2) redox behavior in the bioenergetic enzyme arsenite oxidase (Aio). Combining equilibrium redox titrations, optical and EPR spectroscopies on concentrated samples obtained via heterologous expression, we unambiguously confirm this claim and quantify Aio's redox cooperativity. The stability constant, Ks, of the MoV semi-reduced intermediate is found to be lower than 10− 3. Site-directed mutagenesis of residues in the vicinity of the Mo-cofactor demonstrates that the degree of redox cooperativity is sensitive to H-bonding interactions between the pyranopterin moieties and amino acid residues. Remarkably, in particular replacing the Gln-726 residue by Gly results in stabilization of (low-temperature) EPR-observable MoV with KS = 4. As evidenced by comparison of room temperature optical and low temperature EPR titrations, the degree of stabilization is temperature-dependent. This highlights the importance of room-temperature redox characterizations for correctly interpreting catalytic properties in this group of enzymes.Geochemical and phylogenetic data strongly indicate that molybdenum played an essential biocatalytic roles in early life. Molybdenum's redox versatility and in particular the ability to show cooperative (n = 2) redox behavior provide a rationale for its paramount catalytic importance throughout the evolutionary history of life. Implications of the H-bonding network modulating Molybdenum's redox properties on details of a putative inorganic metabolism at life's origin are discussed.Display Omitted
Keywords: Arsenite oxidase; Molybdenum enzyme; Optical spectroscopy; EPR spectroscopy; Redox titrations;
cis-4-Decenoic and decanoic acids impair mitochondrial energy, redox and Ca2 + homeostasis and induce mitochondrial permeability transition pore opening in rat brain and liver: Possible implications for the pathogenesis of MCAD deficiency by Alexandre Umpierrez Amaral; Cristiane Cecatto; Janaína Camacho da Silva; Alessandro Wajner; Kálita dos Santos Godoy; Rafael Teixeira Ribeiro; Moacir Wajner (1363-1372).
Medium-chain acyl-CoA dehydrogenase (MCAD) deficiency is biochemically characterized by tissue accumulation of octanoic (OA), decanoic (DA) and cis-4-decenoic (cDA) acids, as well as by their carnitine by-products. Untreated patients present episodic encephalopathic crises and biochemical liver alterations, whose pathophysiology is poorly known. We investigated the effects of OA, DA, cDA, octanoylcarnitine (OC) and decanoylcarnitine (DC) on critical mitochondrial functions in rat brain and liver. DA and cDA increased resting respiration and diminished ADP- and CCCP-stimulated respiration and complexes II-III and IV activities in both tissues. The data indicate that these compounds behave as uncouplers and metabolic inhibitors of oxidative phosphorylation. Noteworthy, metabolic inhibition was more evident in brain as compared to liver. DA and cDA also markedly decreased mitochondrial membrane potential, NAD(P)H content and Ca2 + retention capacity in Ca2 +-loaded brain and liver mitochondria. The reduction of Ca2 + retention capacity was more pronounced in liver and totally prevented by cyclosporine A and ADP, as well as by ruthenium red, demonstrating the involvement of mitochondrial permeability transition (mPT) and Ca2 +. Furthermore, cDA induced lipid peroxidation in brain and liver mitochondria and increased hydrogen peroxide formation in brain, suggesting the participation of oxidative damage in cDA-induced alterations. Interestingly, OA, OC and DC did not alter the evaluated parameters, implying lower toxicity for these compounds. Our results suggest that DA and cDA, in contrast to OA and medium-chain acylcarnitines, disturb important mitochondrial functions in brain and liver by multiple mechanisms that are possibly involved in the neuropathology and liver alterations observed in MCAD deficiency.
Keywords: Medium-chain acyl-CoA dehydrogenase deficiency; Medium-chain fatty acids; Medium-chain acylcarnitines; Mitochondrial dysfunction; Mitochondrial permeability transition;
Involvement of the Lhcx protein Fcp6 of the diatom Cyclotella meneghiniana in the macro-organisation and structural flexibility of thylakoid membranes by Artur Ghazaryan; Parveen Akhtar; Győző Garab; Petar H. Lambrev; Claudia Büchel (1373-1379).
Diatoms possess special light-harvesting proteins involved in the photoprotection mechanism called non-photochemical quenching (NPQ). These Lhcx proteins were shown to be subunits of trimeric fucoxanthin-chlorophyll complexes (FCPa) in centric diatoms, but their mode of action is still unclear. Here we investigated the influence of Fcp6, an orthologue to Lhcx1 of Thalassiosira pseudonana in the diatom Cyclotella meneghiniana, by reducing its amount using an antisense approach. Whereas the pigment interactions inside FCPa were not influenced by the presence or absence of Fcp6, as demonstrated by unaltered spectra of circular dichroism, changes could be observed on the level of thylakoids and cells in the mutants compared to WT. This fits to recent models of NPQ in diatoms, where FCP aggregation or supramolecular reorganisation is thought to be a major feature. Thus, Fcp6 (Lhcx1) appears to alter pigment–pigment interactions inside the aggregates, but not inside (un-aggregated) FCPa itself.
Keywords: Anisotropic circular dichroism; FCPa; LHCSR; Lhcx1; Non-photochemical quenching;
The Oxygen quantum yield in diverse algae and cyanobacteria is controlled by partitioning of flux between linear and cyclic electron flow within photosystem II by Gennady Ananyev; Colin Gates; G. Charles Dismukes (1380-1391).
We have measured flash-induced oxygen quantum yields (O2-QYs) and primary charge separation (Chl variable fluorescence yield, Fv/Fm) in vivo among phylogenetically diverse microalgae and cyanobacteria. Higher O2-QYs can be attained in cells by releasing constraints on charge transfer at the Photosystem II (PSII) acceptor side by adding membrane-permeable benzoquinone (BQ) derivatives that oxidize plastosemiquinone QB − and QBH2. This method allows uncoupling PSII turnover from its natural regulation in living cells, without artifacts of isolating PSII complexes. This approach reveals different extents of regulation across species, controlled at the QB − acceptor site. Arthrospira maxima is confirmed as the most efficient PSII-WOC (water oxidizing complex) and exhibits the least regulation of flux. Thermosynechococcus elongatus exhibits an O2-QY of 30%, suggesting strong downregulation. WOC cycle simulations with the most accurate model (VZAD) show that a light-driven backward transition (net addition of an electron to the WOC, distinct from recombination) occurs in up to 25% of native PSIIs in the S2 and S3 states, while adding BQ prevents backward transitions and increases the lifetime of S2 and S3 by 10-fold. Backward transitions occur in PSIIs that have plastosemiquinone radicals in the QB site and are postulated to be physiologically regulated pathways for storing light energy as proton gradient through direct PSII-cyclic electron flow (PSII-CEF). PSII-CEF is independent of classical PSI/cyt-b6f-CEF and provides an alternative proton translocation pathway for energy conversion. PSII-CEF enables variable fluxes between linear and cyclic electron pathways, thus accommodating species-dependent needs for redox and ion-gradient energy sources powered by a single photosystem.Display Omitted
Keywords: PSII quantum yield; VZAD model S states; Arthrospira maxima; Nannochloropsis oceanica; Phaeodactylum tricornutum; Synechococcus 7002;
Inherent conformational flexibility of F1-ATPase α-subunit by Otto Hahn-Herrera; Guillermo Salcedo; Xavier Barril; Enrique García-Hernández (1392-1402).
The core of F1-ATPase consists of three catalytic (β) and three noncatalytic (α) subunits, forming a hexameric ring in alternating positions. A wealth of experimental and theoretical data has provided a detailed picture of the complex role played by catalytic subunits. Although major conformational changes have only been seen in β-subunits, it is clear that α-subunits have to respond to these changes in order to be able to transmit information during the rotary mechanism. However, the conformational behavior of α-subunits has not been explored in detail. Here, we have combined unbiased molecular dynamics (MD) simulations and calorimetrically measured thermodynamic signatures to investigate the conformational flexibility of isolated α-subunits, as a step toward deepening our understanding of its function inside the α3β3 ring. The simulations indicate that the open-to-closed conformational transition of the α-subunit is essentially barrierless, which is ideal to accompany and transmit the movement of the catalytic subunits. Calorimetric measurements of the recombinant α-subunit from Geobacillus kaustophilus indicate that the isolated subunit undergoes no significant conformational changes upon nucleotide binding. Simulations confirm that the nucleotide-free and nucleotide-bound subunits show average conformations similar to that observed in the F1 crystal structure, but they reveal an increased conformational flexibility of the isolated α-subunit upon MgATP binding, which might explain the evolutionary conserved capacity of α-subunits to recognize nucleotides with considerable strength. Furthermore, we elucidate the different dependencies that α- and β-subunits show on Mg(II) for recognizing ATP.
Keywords: FOF1-ATP synthase; Noncatalytic subunit; Conformational flexibility; Isothermal titration calorimetry; Molecular dynamics simulation;
Palmitate-induced changes in energy demand cause reallocation of ATP supply in rat and human skeletal muscle cells by Raid B. Nisr; Charles Affourtit (1403-1411).
Mitochondrial dysfunction has been associated with obesity-related muscle insulin resistance, but the causality of this association is controversial. The notion that mitochondrial oxidative capacity may be insufficient to deal appropriately with excessive nutrient loads is for example disputed. Effective mitochondrial capacity is indirectly, but largely determined by ATP-consuming processes because skeletal muscle energy metabolism is mostly controlled by ATP demand. Probing the bioenergetics of rat and human myoblasts in real time we show here that the saturated fatty acid palmitate lowers the rate and coupling efficiency of oxidative phosphorylation under conditions it causes insulin resistance. Stearate affects the bioenergetic parameters similarly, whereas oleate and linoleate tend to decrease the rate but not the efficiency of ATP synthesis. Importantly, we reveal that palmitate influences how oxidative ATP supply is used to fuel ATP-consuming processes. Direct measurement of newly made protein demonstrates that palmitate lowers the rate of de novo protein synthesis by more than 30%. The anticipated decrease of energy demand linked to protein synthesis is confirmed by attenuated cycloheximide-sensitivity of mitochondrial respiratory activity used to make ATP. This indirect measure of ATP turnover indicates that palmitate lowers ATP supply reserved for protein synthesis by at least 40%. This decrease is also provoked by stearate, oleate and linoleate, albeit to a lesser extent. Moreover, palmitate lowers ATP supply for sodium pump activity by 60–70% and, in human cells, decreases ATP supply for DNA/RNA synthesis by almost three-quarters. These novel fatty acid effects on energy expenditure inform the ‘mitochondrial insufficiency’ debate.Display Omitted
Keywords: Palmitate-induced insulin resistance; Skeletal muscle; Mitochondrial dysfunction; ATP turnover; Obesity; Type 2 diabetes;
Electron transfer and docking between cytochrome cd 1 nitrite reductase and different redox partners — A comparative study by Humberto A. Pedroso; Célia M. Silveira; Rui M. Almeida; Ana Almeida; Stéphane Besson; Isabel Moura; José J.G. Moura; M. Gabriela Almeida (1412-1421).
Cytochrome cd 1 nitrite reductases (cd 1NiRs) catalyze the reduction of nitrite to nitric oxide in denitrifying bacteria, such as Marinobacter hydrocarbonoclasticus. Previous work demonstrated that the enzymatic activity depends on a structural pre-activation triggered by the entry of electrons through the electron transfer (ET) domain, which houses a heme c center. The catalytic activity of M. hydrocarbonoclasticus cd 1NiR (Mhcd 1NiR) was tested by mediated electrochemistry, using small ET proteins and chemical redox mediators. The rate of enzymatic reaction depends on the nature of the redox partner, with cytochrome (cyt) c 552 providing the highest value. In situations where cyt c 552 is replaced by either a biological (cyt c from horse heart) or a chemical mediator the catalytic response was only observed at very low scan rates, suggesting that the intermolecular ET rate is much slower.Molecular docking simulations with the 3D model structure of Mhcd 1NiR and cyt c 552 or cyt c showed that hydrophobic interactions favor the formation of complexes where the heme c domain of the enzyme is the principal docking site. However, only in the case of cyt c 552 the preferential areas of contact and Fe–Fe distances between heme c groups of the redox partners allow establishing competent ET pathways. The coupling of the enzyme with chemical redox mediators was also found not to be energetically favorable. These results indicate that although low activity functional complexes can be formed between Mhcd 1NiR and different types of redox mediators, efficient ET is only observed with the putative physiological electron donor cyt c 552.Display Omitted
Keywords: Cytochrome cd 1 nitrite reductase; Cytochrome c 552; Intermolecular electron transfer; Mediated electrochemistry; Molecular coupling; Electronic pathways;
The small iron-sulfur protein from the ORP operon binds a [2Fe-2S] cluster by Biplab K. Maiti; Isabel Moura; José J.G. Moura; Sofia R. Pauleta (1422-1429).
A linear cluster formulated as [S2MoS2CuS2MoS2]3 −, a unique heterometallic cluster found in biological systems, was identified in a small monomeric protein (named as Orange Protein). The gene coding for this protein is part of an operon mainly present in strict anaerobic bacteria, which is composed (in its core) by genes coding for the Orange Protein and two ATPase proposed to contain Fe-S clusters. In Desulfovibrio desulfuricans G20, there is an ORF, Dde_3197 that encodes a small protein containing several cysteine residues in its primary sequence. The heterologously produced Dde_3197 aggregates mostly in inclusion bodies and was isolated by unfolding with a chaotropic agent and refolding by dialysis. The refolded protein contained sub-stoichiometric amounts of iron atoms/protein (0.5 ± 0.2), but after reconstitution with iron and sulfide, high iron load contents were detected (1.8 ± 0.1 or 3.4 ± 0.2) using 2- and 4-fold iron excess. The visible absorption spectral features of the iron-sulfur clusters in refolded and reconstituted Dde_3197 are similar and resemble the ones of [2Fe-2S] cluster containing proteins. The refolded and reconstituted [2Fe-2S] Dde_3197 are EPR silent, but after reduction with dithionite, a rhombic signal is observed with g max = 2.00, g med = 1.95 and g min = 1.92, consistent with a one-electron reduction of a [2Fe-2S]2 + cluster into a [2Fe-2S]1 + state, with an electron spin of S = ½. The data suggests that Dde_3197 can harbor one or two [2Fe-2S] clusters, one being stable and the other labile, with quite identical spectroscopic properties, but stable to oxygen.Display Omitted
Keywords: Orange protein complex; Oxidative stress; Desulfovibrio; Iron-sulfur cluster biosynthesis; Fe-S cluster reconstitution;
Carotenoid-induced non-photochemical quenching in the cyanobacterial chlorophyll synthase–HliC/D complex by Dariusz M. Niedzwiedzki; Tomasz Tronina; Haijun Liu; Hristina Staleva; Josef Komenda; Roman Sobotka; Robert E. Blankenship; Tomáš Polívka (1430-1439).
Chl synthase (ChlG) is an important enzyme of the Chl biosynthetic pathway catalyzing attachment of phytol/geranylgeraniol tail to the chlorophyllide molecule. Here we have investigated the Flag-tagged ChlG (f.ChlG) in a complex with two different high-light inducible proteins (Hlips) HliD and HliC. The f.ChlG–Hlips complex binds a Chl a and three different carotenoids, β-carotene, zeaxanthin and myxoxanthophyll. Application of ultrafast time-resolved absorption spectroscopy performed at room and cryogenic temperatures revealed excited-state dynamics of complex-bound pigments. After excitation of Chl a in the complex, excited Chl a is efficiently quenched by a nearby carotenoid molecule via energy transfer from the Chl a Qy state to the carotenoid S1 state. The kinetic analysis of the spectroscopic data revealed that quenching occurs with a time constant of ~ 2 ps and its efficiency is temperature independent. Even though due to its long conjugation myxoxanthophyll appears to be energetically best suited for role of Chl a quencher, based on comparative analysis and spectroscopic data we propose that β-carotene bound to Hlips acts as the quencher rather than myxoxanthophyll and zeaxanthin, which are bound at the f.ChlG and Hlips interface. The S1 state lifetime of the quencher has been determined to be 13 ps at room temperature and 21 ps at 77 K. These results demonstrate that Hlips act as a conserved functional module that prevents photodamage of protein complexes during photosystem assembly or Chl biosynthesis.
Keywords: Carotenoids; Non-photochemical quenching; Energy transfer; High-light inducible proteins; Cyanobacteria; Femtosecond spectroscopy;
Trehalose matrix effects on charge-recombination kinetics in Photosystem I of oxygenic photosynthesis at different dehydration levels by Marco Malferrari; Anton Savitsky; Mahir D. Mamedov; Georgy E. Milanovsky; Wolfgang Lubitz; Klaus Möbius; Alexey Yu. Semenov; Giovanni Venturoli (1440-1454).
Matrix effects on long-range electron transfer were studied in cyanobacterial Photosystem I (PS I) complexes, embedded into trehalose glasses at different hydration levels. W-band EPR studies demonstrated, via nitroxide spin probes, structural homogeneity of the dry PS I-trehalose matrix and no alteration of cofactors' distance and relative orientation under temperature and matrix variation. In dry trehalose glasses at room temperature (RT), PS I was stable for months. Flash-induced charge recombination kinetics were examined by high-field time-resolved EPR and optical spectroscopies. The kinetics in hydrated PS I-trehalose glasses mostly reflected the reduction of the photooxidized primary donor P700 •+ by the reduced terminal iron-sulfur clusters. Upon dehydration, the P700 •+ decay accelerated and became more distributed. Continuous distributions of lifetimes τ were extracted from the kinetics by two numerical approaches: a maximum entropy method (MemExp program) and a constrained regularization method (CONTIN program). Both analyses revealed that upon dehydration the contribution of the two slowest components (lifetimes τ ~ 300 ms and ~ 60 ms), attributed to P700 •+[FA/FB]• − recombination, decreased in parallel with the increase of the fastest component (τ ~ 150 μs), and of additional distributed phases with intermediate lifetimes. Dehydration at RT mimicked the effects of freezing water-glycerol PS I systems, suggesting an impairment of PS I protein dynamics in the dry trehalose glass. Similar effects were observed previously in bacterial reaction centers. The work presented for PS I provides new insights into the crucial issue of protein-matrix interactions for protein functionality as controlled by hydrogen-bond networks of the hydration shell.Display Omitted
Keywords: Oxygenic photosynthesis; Conformational dynamics; Trehalose glassy matrices; Charge recombination; Cyanobacterial Photosystem I;
Perturbation of bacteriochlorophyll molecules in Fenna–Matthews–Olson protein complexes through mutagenesis of cysteine residues by Rafael Saer; Gregory S. Orf; Xun Lu; Hao Zhang; Matthew J. Cuneo; Dean A.A. Myles; Robert E. Blankenship (1455-1463).
The Fenna–Matthews–Olson (FMO) pigment–protein complex in green sulfur bacteria transfers excitation energy from the chlorosome antenna complex to the reaction center. In understanding energy transfer in the FMO protein, the individual contributions of the bacteriochlorophyll pigments to the FMO complex's absorption spectrum could provide detailed information with which molecular and energetic models can be constructed. The absorption properties of the pigments, however, are such that their spectra overlap significantly. To overcome this, we used site-directed mutagenesis to construct a series of mutant FMO complexes in the model green sulfur bacterium Chlorobaculum tepidum (formerly Chlorobium tepidum). Two cysteines at positions 49 and 353 in the C. tepidum FMO complex, which reside near hydrogen bonds between BChls 2 and 3, and their amino acid binding partner serine 73 and tyrosine 15, respectively, were changed to alanine residues. The resulting C49A, C353A, and C49A C353A double mutants were analyzed with a combination of optical absorption and circular dichroism (CD) spectroscopies. Our results revealed changes in the absorption properties of several underlying spectral components in the FMO complex, as well as the redox behavior of the complex in response to the reductant sodium dithionite. A high-resolution X-ray structure of the C49A C353A double mutant reveals that these spectral changes appear to be independent of any major structural rearrangements in the FMO mutants. Our findings provide important tests for theoretical calculations of the C. tepidum FMO absorption spectrum, and additionally highlight a possible role for cysteine residues in the redox activity of the pigment–protein complex.Display Omitted
Keywords: Fenna–Matthews–Olson; Bacteriochlorophyll; Exciton; Spectroscopy; Energy transfer; Photosynthesis;
Positive feedback during sulfide oxidation fine-tunes cellular affinity for oxygen by Abbas Abou-Hamdan; Céline Ransy; Thomas Roger; Hala Guedouari-Bounihi; Erwan Galardon; Frédéric Bouillaud (1464-1472).
Sulfide (H2S in the gas form) is the third gaseous transmitter found in mammals. However, in contrast to nitric oxide (NO) or carbon monoxide (CO), sulfide is oxidized by a sulfide quinone reductase and generates electrons that enter the mitochondrial respiratory chain arriving ultimately at cytochrome oxidase, where they combine with oxygen to generate water. In addition, sulfide is also a strong inhibitor of cytochrome oxidase, similar to NO, CO and cyanide. The balance between the electron donor and the inhibitory role of sulfide is likely controlled by sulfide and oxygen availability. The present study aimed to evaluate if and how sulfide release and oxidation impacts on the cellular affinity for oxygen. Results: i) when sulfide delivery approaches the maximal sulfide oxidation rate cells become exquisitely dependent on oxygen; ii) a positive feedback makes the balance between sulfide-releasing and -oxidizing rates the relevant parameter rather than the absolute values of these rates, and; iii) this altered dependence on oxygen is detected with sulfide concentrations that remain in the low micromolar range. Conclusions: i) within the context of continuous release of sulfide stemming from cellular metabolism, alterations in the activity of the sulfide oxidation pathway fine-tunes the cell's affinity for oxygen, and; ii) a decrease in the expression of the sulfide oxidation pathway greatly enhances the cell's dependence on oxygen concentration.Display Omitted
Keywords: Hydrogen sulfide; Hypoxia; Mitochondria; Positive feedback; Sulfide quinone reductase;
Visualizing heterogeneity of photosynthetic properties of plant leaves with two-photon fluorescence lifetime imaging microscopy by Ievgeniia Iermak; Jochem Vink; Arjen N. Bader; Emilie Wientjes; Herbert van Amerongen (1473-1478).
Two-photon fluorescence lifetime imaging microscopy (FLIM) was used to analyse the distribution and properties of Photosystem I (PSI) and Photosystem II (PSII) in palisade and spongy chloroplasts of leaves from the C3 plant Arabidopsis thaliana and the C4 plant Miscanthus x giganteus. This was achieved by separating the time-resolved fluorescence of PSI and PSII in the leaf. It is found that the PSII antenna size is larger on the abaxial side of A. thaliana leaves, presumably because chloroplasts in the spongy mesophyll are “shaded” by the palisade cells. The number of chlorophylls in PSI on the adaxial side of the A. thaliana leaf is slightly higher. The C4 plant M. x giganteus contains both mesophyll and bundle sheath cells, which have a different PSI/PSII ratio. It is shown that the time-resolved fluorescence of bundle sheath and mesophyll cells can be analysed separately. The relative number of chlorophylls, which belong to PSI (as compared to PSII) in the bundle sheath cells is at least 2.5 times higher than in mesophyll cells. FLIM is thus demonstrated to be a useful technique to study the PSI/PSII ratio and PSII antenna size in well-defined regions of plant leaves without having to isolate pigment-protein complexes.
Keywords: Photosynthesis; Microscopy; Time-resolved fluorescence; Photosystem I; Photosystem II;
Fingerprinting the macro-organisation of pigment–protein complexes in plant thylakoid membranes in vivo by circular-dichroism spectroscopy by Tünde N. Tóth; Neha Rai; Katalin Solymosi; Ottó Zsiros; Wolfgang P. Schröder; Győző Garab; Herbert van Amerongen; Peter Horton; László Kovács (1479-1489).
Macro-organisation of the protein complexes in plant thylakoid membranes plays important roles in the regulation and fine-tuning of photosynthetic activity. These delicate structures might, however, undergo substantial changes during isolating the thylakoid membranes or during sample preparations, e.g., for electron microscopy. Circular-dichroism (CD) spectroscopy is a non-invasive technique which can thus be used on intact samples. Via excitonic and psi-type CD bands, respectively, it carries information on short-range excitonic pigment–pigment interactions and the macro-organisation (chiral macrodomains) of pigment–protein complexes (psi, polymer or salt-induced). In order to obtain more specific information on the origin of the major psi-type CD bands, at around (+)506, (−)674 and (+)690 nm, we fingerprinted detached leaves and isolated thylakoid membranes of wild-type and mutant plants and also tested the effects of different environmental conditions in vivo. We show that (i) the chiral macrodomains disassemble upon mild detergent treatments, but not after crosslinking the protein complexes; (ii) in different wild-type leaves of dicotyledonous and monocotyledonous angiosperms the CD features are quite robust, displaying very similar excitonic and psi-type bands, suggesting similar protein composition and (macro-) organisation of photosystem II (PSII) supercomplexes in the grana; (iii) the main positive psi-type bands depend on light-harvesting protein II contents of the membranes; (iv) the (+)506 nm band appears only in the presence of PSII–LHCII supercomplexes and does not depend on the xanthophyll composition of the membranes. Hence, CD spectroscopy can be used to detect different macro-domains in the thylakoid membranes with different outer antenna compositions in vivo.
Keywords: Circular dichroism; Chiral macrodomain; Light-harvesting complexes; Photosystem II supercomplexes; Psi-type CD; Thylakoid membrane;
Probing the pigment binding sites in LHCII with resonance Raman spectroscopy: The effect of mutations at S123 by Elizabeth Kish; Ke Wang; Manuel J. Llansola-Portoles; Cristian Ilioaia; Andrew A. Pascal; Bruno Robert; Chunhong Yang (1490-1496).
Resonance Raman spectroscopy was used to evaluate the structure of light-harvesting chlorophyll (Chl) a/b complexes of photosystem II (LHCII), reconstituted from wild-type (WT) and mutant apoproteins over-expressed in Escherichia coli. The point mutations involved residue S123, exchanged for either P (S123P) or G (S123G). In all reconstituted proteins, lutein 2 displayed a distorted conformation, as it does in purified LHCII trimers. Reconstituted WT and S123G also exhibited a conformation of bound neoxanthin (Nx) molecules identical to the native protein, while the S123P mutation was found to induce a change in Nx conformation. This structural change of neoxanthin is accompanied by a blue shift of the absorption of this carotenoid molecule. The interactions assumed by (and thus the structure of the binding sites of) the bound Chls b were found identical in all the reconstituted proteins, and only marginally perturbed as compared to purified LHCII. The interactions assumed by bound Chls a were also identical in purified LHCII and the reconstituted WT. However, the keto carbonyl group of one Chl a, originally free-from-interactions in WT LHCII, becomes involved in a strong H-bond with its environment in LHCII reconstituted from the S123P apoprotein. As the absorption in the Qy region of this protein is identical to that of the LHCII reconstituted from the WT apoprotein, we conclude that the interaction state of the keto carbonyl of Chl a does not play a significant role in tuning the binding site energy of these molecules.
Keywords: Carotenoid; Electronic absorption; LHCII; Lutein; Neoxanthin; Resonance Raman;
Photocurrents from photosystem II in a metal oxide hybrid system: Electron transfer pathways by Katharina Brinkert; Florian Le Formal; Xiaoe Li; James Durrant; A. William Rutherford; Andrea Fantuzzi (1497-1505).
We have investigated the nature of the photocurrent generated by Photosystem II (PSII), the water oxidizing enzyme, isolated from Thermosynechococcus elongatus, when immobilized on nanostructured titanium dioxide on an indium tin oxide electrode (TiO2/ITO). We investigated the properties of the photocurrent from PSII when immobilized as a monolayer versus multilayers, in the presence and absence of an inhibitor that binds to the site of the exchangeable quinone (QB) and in the presence and absence of exogenous mobile electron carriers (mediators). The findings indicate that electron transfer occurs from the first quinone (QA) directly to the electrode surface but that the electron transfer through the nanostructured metal oxide is the rate-limiting step. Redox mediators enhance the photocurrent by taking electrons from the nanostructured semiconductor surface to the ITO electrode surface not from PSII. This is demonstrated by photocurrent enhancement using a mediator incapable of accepting electrons from PSII. This model for electron transfer also explains anomalies reported in the literature using similar and related systems. The slow rate of the electron transfer step in the TiO2 is due to the energy level of electron injection into the semiconducting material being below the conduction band. This limits the usefulness of the present hybrid electrode. Strategies to overcome this kinetic limitation are discussed.Display Omitted
Keywords: Water oxidizing enzyme; Photosynthetic reaction centre; Photosynthesis; Protein electrode interface; Protein film photoelectrochemistry; Quinone;
Direct electrochemistry of nitrate reductase from the fungus Neurospora crassa by Palraj Kalimuthu; Phillip Ringel; Tobias Kruse; Paul V. Bernhardt (1506-1513).
We report the first direct (unmediated) catalytic electrochemistry of a eukaryotic nitrate reductase (NR). NR from the filamentous fungus Neurospora crassa, is a member of the mononuclear molybdenum enzyme family and contains a Mo, heme and FAD cofactor which are involved in electron transfer from NAD(P)H to the (Mo) active site where reduction of nitrate to nitrite takes place. NR was adsorbed on an edge plane pyrolytic graphite (EPG) working electrode. Non-turnover redox responses were observed in the absence of nitrate from holo NR and three variants lacking the FAD, heme or Mo cofactor. The FAD response is due to dissociated cofactor in all cases. In the presence of nitrate, NR shows a pronounced cathodic catalytic wave with an apparent Michaelis constant (K M) of 39 μM (pH 7). The catalytic cathodic current increases with temperature from 5 to 35 °C and an activation enthalpy of 26 kJ mol− 1 was determined. In spite of dissociation of the FAD cofactor, catalytically activity is maintained.
Keywords: Molybdenum; Enzyme; Voltammetry; Nitrate reductase;
Excitation dynamics and structural implication of the stress-related complex LHCSR3 from the green alga Chlamydomonas reinhardtii by Nicoletta Liguori; Vladimir Novoderezhkin; Laura M. Roy; Rienk van Grondelle; Roberta Croce (1514-1523).
LHCSR3 is a member of the Light-Harvesting Complexes (LHC) family, which is mainly composed of pigment-protein complexes responsible for collecting photons during the first steps of photosynthesis. Unlike related LHCs, LHCSR3 is expressed in stress conditions and has been shown to be essential for the fast component of photoprotection, non-photochemical quenching (NPQ), in the green alga Chlamydomonas reinhardtii. In plants, which do not possess LHCSR homologs, NPQ is triggered by the PSBS protein. Both PSBS and LHCSR3 possess the ability to sense pH changes but, unlike PSBS, LHCSR3 binds multiple pigments. In this work we have analyzed the properties of the pigments bound to LHCSR3 and their excited state dynamics. The data show efficient excitation energy transfer between pigments with rates similar to those observed for the other LHCs. Application of an exciton model based on a template of LHCII, the most abundant LHC, satisfactorily explains the collected steady state and time-resolved spectroscopic data, indicating that LHCSR3 has a LHC-like molecular architecture, although it probably binds less pigments. The model suggests that most of the chlorophylls have similar energy and interactions as in LHCII. The most striking difference is the localization of the lowest energy state, which is not on the Chlorophyll a (Chl a) 610-611-612 triplet as in all the LHCB antennas, but on Chl a613, which is located close to the lumen and to the pH-sensing region of the protein.
Keywords: LHCSR3; Chlamydomonas reinhardtii; Light-Harvesting Complex; Redfield model; transient absorption;
The PsbY protein of Arabidopsis Photosystem II is important for the redox control of cytochrome b 559 by Lotta von Sydow; Serena Schwenkert; Jörg Meurer; Christiane Funk; Fikret Mamedov; Wolfgang P. Schröder (1524-1533).
Photosystem II is a protein complex embedded in the thylakoid membrane of photosynthetic organisms and performs the light driven water oxidation into electrons and molecular oxygen that initiate the photosynthetic process. This important complex is composed of more than two dozen of intrinsic and peripheral subunits, of those half are low molecular mass proteins. PsbY is one of those low molecular mass proteins; this 4.7–4.9 kDa intrinsic protein seems not to bind any cofactors. Based on structural data from cyanobacterial and red algal Photosystem II PsbY is located closely or in direct contact with cytochrome b 559. Cytb 559 consists of two protein subunits (PsbE and PsbF) ligating a heme-group in-between them. While the exact function of this component in Photosystem II has not yet been clarified, a crucial role for assembly and photo-protection in prokaryotic complexes has been suggested. One unique feature of Cytb 559 is its redox-heterogeneity, forming high, medium and low potential, however, neither origin nor mechanism are known. To reveal the function of PsbY within Photosystem II of Arabidopsis we have analysed PsbY knock-out plants and compared them to wild type and to complemented mutant lines. We show that in the absence of PsbY protein Cytb 559 is only present in its oxidized, low potential form and plants depleted of PsbY were found to be more susceptible to photoinhibition.
Keywords: Photosystem II; Thylakoid membrane; PsbY protein; Cytochrome b 559;
Nanosecond ligand migration and functional protein relaxation in ba 3 oxidoreductase: Structures of the B0, B1 and B2 intermediate states by Antonis Nicolaides; Tewfik Soulimane; Constantinos Varotsis (1534-1540).
Nanosecond time-resolved step-scan FTIR spectroscopy (nTRS 2 -FTIR) has been applied to literally probe the active site of the carbon monoxide (CO)-bound thermophilic ba 3 heme-copper oxidoreductase as it executes its function. The nTRS 2 - snapshots of the photolysed heme a 3 Fe-CO/CuB species captured a “transition state” whose side chains prevent the photolysed CO to enter the docking cavity. There are three sets of ba 3 photoproduct bands of docked CO with different orientation exhibiting different kinetics. The trajectories of the “docked” CO at 2122, 2129 and 2137 cm− 1 is referred to in the literature as B2, B1 and B0 intermediate states, respectively. The present data provided direct evidence for the role of water in controlling ligand orientation in an intracavity protein environment.
Keywords: Cytochrome c oxidase; Time-resolved step-scan FTIR; Dynamics;
Effect of ionic strength on intra-protein electron transfer reactions: The case study of charge recombination within the bacterial reaction center by Mauro Giustini; Matteo Parente; Antonia Mallardi; Gerardo Palazzo (1541-1549).
It is a common believe that intra-protein electron transfer (ET) involving reactants and products that are overall electroneutral are not influenced by the ions of the surrounding solution. The results presented here show an electrostatic coupling between the ionic atmosphere surrounding a membrane protein (the reaction center (RC) from the photosynthetic bacterium Rhodobacter sphaeroides) and two very different intra-protein ET processes taking place within it. Specifically we have studied the effect of salt concentration on: i) the kinetics of the charge recombination between the reduced primary quinone acceptor QA − and the primary photoxidized donor P+; ii) the thermodynamic equilibrium (QA − ↔ QB −) for the ET between QA − and the secondary quinone acceptor QB. A distinctive point of this investigation is that reactants and products are overall electroneutral. The protein electrostatics has been described adopting the lowest level of complexity sufficient to grasp the experimental phenomenology and the impact of salt on the relative free energy level of reactants and products has been evaluated according to suitable thermodynamic cycles. The ionic strength effect was found to be independent on the ion nature for P+ QA − charge recombination where the leading electrostatic term was the dipole moment. In the case of the QA − ↔ QB − equilibrium, the relative stability of QA − and QB − was found to depend on the salt concentration in a fashion that is different for chaotropic and kosmotropic ions. In such a case both dipole moment and quadrupole moments of the RC must be considered.Display Omitted
Keywords: Intra-protein electron transfer; Rhodobacter sphaeroides; Charge recombination; Hofmeister series, Debye screening length;
The strontium inorganic mutant of the water oxidizing center (CaMn4O5) of PSII improves WOC efficiency but slows electron flux through the terminal acceptors by Colin Gates; Gennady Ananyev; G. Charles Dismukes (1550-1560).
Herein we extend prior studies of biosynthetic strontium replacement of calcium in PSII-WOC core particles to characterize whole cells. Previous studies of Thermosynechococcus elongatus found a lower rate of light-saturated O2 from isolated PSII-WOC(Sr) cores and 5–8 × slower rate of oxygen release. We find similar properties in whole cells, and show it is due to a 20% larger Arrhenius activation barrier for O2 evolution. Cellular adaptation to the sluggish PSII-WOC(Sr) cycle occurs in which flux through the QAQB acceptor gate becomes limiting for turnover rate in vivo. Benzoquinone derivatives that bind to QB site remove this kinetic chokepoint yielding 31% greater O2 quantum yield (QY) of PSII-WOC(Sr) vs. PSII-WOC(Ca). QY and efficiency of the WOC(Sr) catalytic cycle are greatly improved at low light flux, due to fewer misses and backward transitions and 3-fold longer lifetime of the unstable S3 state, attributed to greater thermodynamic stabilization of the WOC(Sr) relative to the photoactive tyrosine YZ. More linear and less cyclic electron flow through PSII occurs per PSII-WOC(Sr). The organismal response to the more active PSII centers in Sr-grown cells at 45 °C is to lower the number of active PSII-WOC per Chl, producing comparable oxygen and energy per cell. We conclude that redox and protonic energy fluxes created by PSII are primary determinants for optimal growth rate of T. elongatus. We further conclude that the (Sr-favored) intermediate-spin S = 5/2 form of the S2 state is the active form in the catalytic cycle relative to the low-spin S = 1/2 form.Display Omitted
Keywords: Photosystem II; Strontium; Thermosynechococcus; Water oxidizing complex; Manganese; Oxygen;
Differential susceptibility of mitochondrial complex II to inhibition by oxaloacetate in brain and heart by Anna Stepanova; Yevgeniya Shurubor; Federica Valsecchi; Giovanni Manfredi; Alexander Galkin (1561-1568).
Mitochondrial Complex II is a key mitochondrial enzyme connecting the tricarboxylic acid (TCA) cycle and the electron transport chain. Studies of complex II are clinically important since new roles for this enzyme have recently emerged in cell signalling, cancer biology, immune response and neurodegeneration. Oxaloacetate (OAA) is an intermediate of the TCA cycle and at the same time is an inhibitor of complex II with high affinity (K d ~ 10− 8 M). Whether or not OAA inhibition of complex II is a physiologically relevant process is a significant, but still controversial topic. We found that complex II from mouse heart and brain tissue has similar affinity to OAA and that only a fraction of the enzyme in isolated mitochondrial membranes (30.2 ± 6.0% and 56.4 ± 5.6% in the heart and brain, respectively) is in the free, active form. Since OAA could bind to complex II during isolation, we established a novel approach to deplete OAA in the homogenates at the early stages of isolation. In heart, this treatment significantly increased the fraction of free enzyme, indicating that OAA binds to complex II during isolation. In brain the OAA-depleting system did not significantly change the amount of free enzyme, indicating that a large fraction of complex II is already in the OAA-bound inactive form. Furthermore, short-term ischemia resulted in a dramatic decline of OAA in tissues, but it did not change the amount of free complex II. Our data show that in brain OAA is an endogenous effector of complex II, potentially capable of modulating the activity of the enzyme.
Keywords: Mitochondrial complex II; Succinate dehydrogenase; Oxaloacetate; Ischemia; Krebs cycle;
From low- to high-potential bioenergetic chains: Thermodynamic constraints of Q-cycle function by Lucie Bergdoll; Felix ten Brink; Wolfgang Nitschke; Daniel Picot; Frauke Baymann (1569-1579).
The electrochemical parameters of all cofactors in the supercomplex formed by the Rieske/cytb complex and the SoxM/A-type O2-reductase from the menaquinone-containing Firmicute Geobacillus stearothermophilus were determined by spectroelectrochemistry and EPR redox titrations. All redox midpoint potentials (Em) were found to be lower than those of ubi- or plastoquinone-containing systems by a value comparable to the redox potential difference between the respective quinones. In particular, Em values of + 200 mV, − 360 mV, − 220 mV and − 50 mV (at pH 7) were obtained for the Rieske cluster, heme b L, heme b H and heme c i, respectively. Comparable values of − 330 mV, − 200 mV and + 120 mV for hemes b L, b H and the Rieske cluster were determined for an anaerobic Firmicute, Heliobacterium modesticaldum. Thermodynamic constraints, optimization of proton motive force build-up and the necessity of ROS-avoidance imposed by the rise in atmospheric O2 2.5 billion years ago are discussed as putative evolutionary driving forces resulting in the observed redox upshift. The close conservation of the entire redox landscape between low and high potential systems suggests that operation of the Q-cycle requires the precise electrochemical tuning of enzyme cofactors to the quinone substrate as stipulated in P. Mitchell's hypothesis.Display Omitted
Keywords: Q-cycle; Rieske/cytb complex; Cytochrome bc 1 complex; Quinone; Electron bifurcation; Great Oxidation Event;
The lowest-energy chlorophyll of photosystem II is adjacent to the peripheral antenna: Emitting states of CP47 assigned via circularly polarized luminescence by Jeremy Hall; Thomas Renger; Frank Müh; Rafael Picorel; Elmars Krausz (1580-1593).
The identification of low-energy chlorophyll pigments in photosystem II (PSII) is critical to our understanding of the kinetics and mechanism of this important enzyme. We report parallel circular dichroism (CD) and circularly polarized luminescence (CPL) measurements at liquid helium temperatures of the proximal antenna protein CP47. This assembly hosts the lowest-energy chlorophylls in PSII, responsible for the well-known “F695” fluorescence band of thylakoids and PSII core complexes. Our new spectra enable a clear identification of the lowest-energy exciton state of CP47. This state exhibits a small but measurable excitonic delocalization, as predicated by its CD and CPL. Using structure-based simulations incorporating the new spectra, we propose a revised set of site energies for the 16 chlorophylls of CP47. The significant difference from previous analyses is that the lowest-energy pigment is assigned as Chl 612 (alternately numbered Chl 11). The new assignment is readily reconciled with the large number of experimental observations in the literature, while the most common previous assignment for the lowest energy pigment, Chl 627(29), is shown to be inconsistent with CD and CPL results. Chl 612(11) is near the peripheral light-harvesting system in higher plants, in a lumen-exposed region of the thylakoid membrane. The low-energy pigment is also near a recently proposed binding site of the PsbS protein. This result consequently has significant implications for our understanding of the kinetics and regulation of energy transfer in PSII.Display Omitted
Keywords: Photosystem II; Fluorescence; Lowest excited states; CP47; Circularly polarized luminescence; PsbS;
Water exit pathways and proton pumping mechanism in B-type cytochrome c oxidase from molecular dynamics simulations by Longhua Yang; Åge A. Skjevik; Wen-Ge Han Du; Louis Noodleman; Ross C. Walker; Andreas W. Götz (1594-1606).
Cytochrome c oxidase (CcO) is a vital enzyme that catalyzes the reduction of molecular oxygen to water and pumps protons across mitochondrial and bacterial membranes. While proton uptake channels as well as water exit channels have been identified for A-type CcOs, the means by which water and protons exit B-type CcOs remain unclear. In this work, we investigate potential mechanisms for proton transport above the dinuclear center (DNC) in ba3-type CcO of Thermus thermophilus. Using long-time scale, all-atom molecular dynamics (MD) simulations for several relevant protonation states, we identify a potential mechanism for proton transport that involves propionate A of the active site heme a3 and residues Asp372, His376 and Glu126II, with residue His376 acting as the proton-loading site. The proposed proton transport process involves a rotation of residue His376 and is in line with experimental findings. We also demonstrate how the strength of the salt bridge between residues Arg225 and Asp287 depends on the protonation state and that this salt bridge is unlikely to act as a simple electrostatic gate that prevents proton backflow. We identify two water exit pathways that connect the water pool above the DNC to the outer P-side of the membrane, which can potentially also act as proton exit transport pathways. Importantly, these water exit pathways can be blocked by narrowing the entrance channel between residues Gln151II and Arg449/Arg450 or by obstructing the entrance through a conformational change of residue Tyr136, respectively, both of which seem to be affected by protonation of residue His376.Display Omitted
Keywords: Cytochrome c oxidase; Proton pumping mechanism; Proton transport; Water exit pathway; Molecular dynamics; Computer simulation;
Far-red light photoacclimation: Chromophorylation of FR induced α- and β-subunits of allophycocyanin from Chroococcidiopsis thermalis sp. PCC7203 by Qian-Zhao Xu; Jia-Xin Han; Qi-Ying Tang; Wen-Long Ding; Dan Miao; Ming Zhou; Hugo Scheer; Kai-Hong Zhao (1607-1616).
Cyanobacterial light-harvesting complexes, phycobilisomes, can undergo extensive remodeling under varying light conditions. Acclimation to far-red light involves not only generation of red-shifted chlorophylls in the photosystems, but also induction of additional copies of core biliproteins that have been related to red-shifted components of the phycobilisome (Gan et al., Life 5, 4, 2015). We are studying the molecular basis for these acclimations in Chroococcidiopsis thermalis sp. PCC7203. Five far-red induced allophycocyanin subunits (ApcA2, ApcA3, ApcB2, ApcB3 and ApcF2) were expressed in Escherichia coli, together with S-type chromophore-protein lyases and in situ generated chromophore, phycocyanobilin. Only one subunit, ApcF2, shows an unusual red-shift (λAmax ~ 675 nm, λFmax ~ 698 nm): it binds the chromophore non-covalently, thereby preserving its full conjugation length. This mechanism operates also in two Cys-variants of the induced subunits of bulky APC. All other wild-type subunits bind phycocyanobilin covalently to the conventional Cys-81 under catalysis of the lyase, CpcS1. Although three of them also show binding to additional cysteines, all absorb and fluoresce similar to conventional APC subunits (λAmax ~ 610 nm, λFmax ~ 640 nm). Another origin of red-shifted complexes was identified, however, when different wild-type α- and β-subunits of the far-red induced bulky APC were combined in a combinatorial fashion. Strongly red-shifted complexes (λFmax ≤ 722 nm) were formed when the α-subunit, PCB-ApcA2, and the β-subunit, PCB-ApcB2, were generated together in E. coli. This extreme aggregation-induced red-shift of ~ 90 nm of covalently bound chromophores is reminiscent, but much larger, than the ~ 30 nm observed with conventional APC.
Keywords: Cyanobacteria; Phycobilisome; Allophycocyanin; Phycocyanobilin; Chromophorylation; Energy transfer; Far-red photoacclimation;
Corrigendum to “depletion of the “gamma-type carbonic anhydrase-like” subunits of complex I affects central mitochondrial metabolism in Arabidopsis thaliana” [Biochim. Biophys. Acta 1857 (2016) 60–71] by Steffanie Fromm; Jennifer Göing; Christin Lorenz; Christoph Peterhänsel; Hans-Peter Braun (1617-1618).
Cryo-EM structure of a tetrameric cyanobacterial photosystem I complex reveals novel subunit interactions by Dmitry A. Semchonok; Meng Li; Barry D. Bruce; Gert T. Oostergetel; Egbert J. Boekema (1619-1626).
Photosystem I (PSI) of the thermophilic cyanobacterium Chroococcidiopsis sp. TS-821 (TS-821) forms tetramers Li et al. (2014). Two-dimensional maps obtained by single particle electron microscopy (EM) clearly show that the tetramer lacks four-fold symmetry and is actually composed of a dimer of dimers with C2 symmetry. The resolution of these negative stain 2D maps did not permit the placement of most of the small PSI subunits, except for PsaL. Therefore cryo-EM was used for 3D reconstruction of the PSI tetramer complex. A 3D model at ~ 11.5 Å resolution was obtained and a 2D map within the membrane plane of ~ 6.1 Å. This data was used to build a model that was compared with the high-resolution structure of the PSI of Thermosynechococcus elongatus (T. elongatus) at 2.5 Å. This comparison reveals key differences in which subunits are involved in the two different interfaces, interface type 1 within a dimer and interface type 2 between dimers. The type 1 interface in TS-821 is similar to the monomer interface in the trimeric PSI from T. elongatus, with interactions between subunits PsaA, -B, -I, -L and M. In type 2 the interaction is only between PsaA, -B and -L. Unlike the trimeric PSI, the central cavity of the complex is not filled with the PsaL-derived helical bundle, but instead seems filled with lipids. The physiological or evolutionary advantage of the tetramer is unknown. However, the presence of both dimers and tetramers in the thylakoid membrane suggest a dynamic equilibrium that shifts towards the tetramers in high light.
Keywords: Photosystem I; Electron microscopy; Structure; Cyanobacteria; Chroococcidiopsis;
Challenges facing an understanding of the nature of low-energy excited states in photosynthesis by Jeffrey R. Reimers; Malgorzata Biczysko; Douglas Bruce; David F. Coker; Terry J. Frankcombe; Hideki Hashimoto; Jürgen Hauer; Ryszard Jankowiak; Tobias Kramer; Juha Linnanto; Fikret Mamedov; Frank Müh; Margus Rätsep; Thomas Renger; Stenbjörn Styring; Jian Wan; Zhuan Wang; Zheng-Yu Wang-Otomo; Yu-Xiang Weng; Chunhong Yang; Jian-Ping Zhang; Arvi Freiberg; Elmars Krausz (1627-1640).
While the majority of the photochemical states and pathways related to the biological capture of solar energy are now well understood and provide paradigms for artificial device design, additional low-energy states have been discovered in many systems with obscure origins and significance. However, as low-energy states are naively expected to be critical to function, these observations pose important challenges. A review of known properties of low energy states covering eight photochemical systems, and options for their interpretation, are presented. A concerted experimental and theoretical research strategy is suggested and outlined, this being aimed at providing a fully comprehensive understanding.Display Omitted
Keywords: Photosynthesis; Excited states; Exciton coupling; Charge transfer; Non-photochemical quenching; Primary charge separation;
Retraction notice to - Sirtuin-4 modulates sensitivity to induction of the mitochondrial permeability transition pore by Manish Verma; Nataly Shulga; John G. Pastorino (1641).