BBA - Bioenergetics (v.1857, #10)
Editorial Board (i).
Energizing the light harvesting antenna: Insight from CP29 by Nikolaos E. Ioannidis; Sotiris Papadatos; Vangelis Daskalakis (1643-1650).
How do plants cope with excess light energy? Crop health and stress tolerance are governed by molecular photoprotective mechanisms. Protective exciton quenching in plants is activated by membrane energization, via unclear conformational changes in proteins called antennas. Here we show that pH and salt gradients stimulate the response of such an antenna under low and high energization by all-atom Molecular Dynamics Simulations. Novel insight establishes that helix-5 (H5) conformation in CP29 from spinach is regulated by chemiosmotic factors. This is selectively correlated with the chl-614 macrocycle deformation and interactions with nearby pigments, that could suggest a role in plant photoprotection. Adding to the significance of our findings, H5 domain is conserved among five antennas (LHCB1–5). These results suggest that light harvesting complexes of Photosystem II, one of the most abundant proteins on earth, can sense chemiosmotic gradients via their H5 domains in an upgraded role from a solar detector to also a chemiosmotic sensor.Display Omitted
Keywords: Photosystem II; Antenna proteins; Photoprotection; Non photochemical quenching; Proton motive force;
Dynamic reorganization of photosystem II supercomplexes in response to variations in light intensities by Pascal Albanese; Marcello Manfredi; Andrea Meneghesso; Emilio Marengo; Guido Saracco; James Barber; Tomas Morosinotto; Cristina Pagliano (1651-1660).
Plants are sessile organisms and need to acclimate to ever-changing light conditions in order to survive. These changes trigger a dynamic reorganization of the membrane protein complexes in the thylakoid membranes. Photosystem II (PSII) and its light harvesting system (LHCII) are the major target of this acclimation response, and accumulating evidences indicate that the amount and composition of PSII–LHCII supercomplexes in thylakoids are dynamically adjusted in response to changes in light intensity and quality.In this study, we characterized the PSII–LHCII supercomplexes in thylakoid membranes of pea plants in response to long-term acclimation to different light intensities. We provide evidence of a reorganization of the PSII–LHCII supercomplexes showing distinct changes in their antenna moiety. Mass spectrometry analysis revealed a specific reduction of Lhcb3, Lhcb6 and M-LHCII trimers bound to the PSII cores, while the Lhcb4.3 isoform increased in response to high light intensities. The modulation of Lhcb protein content correlates with the reduction of the functional PSII antenna size. These results suggest that the Lhcb3, Lhcb4.3 and Lhcb6 antenna subunits are major players in modulation of the PSII antenna size upon long-term acclimation to increased light levels. PsbS was not detected in the isolated PSII–LHCII supercomplexes at any light condition, despite an increased accumulation in thylakoids of high light acclimated plants, suggesting that PsbS is not a constitutive component of PSII–LHCII supercomplexes.
Keywords: Light acclimation; Photosystem II; Proteomics; PSII–LHCII supercomplex; SWATH analysis; Thylakoids;
Identifying involvement of Lys251/Asp252 pair in electron transfer and associated proton transfer at the quinone reduction site of Rhodobacter capsulatus cytochrome bc 1 by Patryk Kuleta; Marcin Sarewicz; Pekka Postila; Tomasz Róg; Artur Osyczka (1661-1668).
Describing dynamics of proton transfers in proteins is challenging, but crucial for understanding processes which use them for biological functions. In cytochrome bc 1, one of the key enzymes of respiration or photosynthesis, proton transfers engage in oxidation of quinol (QH2) and reduction of quinone (Q) taking place at two distinct catalytic sites. Here we evaluated by site-directed mutagenesis the contribution of Lys251/Asp252 pair (bacterial numbering) in electron transfers and associated with it proton uptake to the quinone reduction site (Qi site). We showed that the absence of protonable group at position 251 or 252 significantly changes the equilibrium levels of electronic reactions including the Qi-site mediated oxidation of heme b H, reverse reduction of heme b H by quinol and heme b H/Qi semiquinone equilibrium. This implicates the role of H-bonding network in binding of quinone/semiquinone and defining thermodynamic properties of Q/SQ/QH2 triad. The Lys251/Asp252 proton path is disabled only when both protonable groups are removed. With just one protonable residue from this pair, the entrance of protons to the catalytic site is sustained, albeit at lower rates, indicating that protons can travel through parallel routes, possibly involving water molecules. This shows that proton paths display engineering tolerance for change as long as all the elements available for functional cooperation secure efficient proton delivery to the catalytic site.
Keywords: Cytochrome bc 1; Mitochondrial complex III; Electron transfer; Proton transfer; Quinone;
Vibrational fingerprints of the Mn4CaO5 cluster in Photosystem II by mixed quantum-classical molecular dynamics by Daniele Bovi; Matteo Capone; Daniele Narzi; Leonardo Guidoni (1669-1677).
A detailed knowledge of the structures of the catalytic steps along the Kok-Joliot cycle of Photosystem II may help to understand the strategies adopted by this unique enzyme to achieve water oxidation. Vibrational spectroscopy has probed in the last decades the intermediate states of the catalytic cycle, although the interpretation of the data turned out to be often problematic. In the present work we use QM/MM molecular dynamics on the S2 state to obtain the vibrational density of states at room temperature. To help the interpretation of the computational and experimental data we propose a decomposition of the Mn4CaO5 moiety into five separate parts, composed by “diamond” motifs involving four atoms. The spectral signatures arising from this analysis can be easily interpreted to assign experimentally known bands to specific molecular motions. In particular, we focused in the low frequency region of the vibrational spectrum of the S2 state. We can therefore identify the observed bands around 600–620 cm− 1 as characteristic for the stretching vibrations involving Mn1-O1-Mn2 or Mn3-O5 moieties.
Keywords: Infrared spectra; FTIR; Photosystem II; Density functional theory; VDOS;
Mitochondrial involvement in skeletal muscle insulin resistance: A case of imbalanced bioenergetics by Charles Affourtit (1678-1693).
Skeletal muscle insulin resistance in obesity associates with mitochondrial dysfunction, but the causality of this association is controversial. This review evaluates mitochondrial models of nutrient-induced muscle insulin resistance. It transpires that all models predict that insulin resistance arises as a result of imbalanced cellular bioenergetics. The nature and precise origin of the proposed insulin-numbing molecules differ between models but all species only accumulate when metabolic fuel supply outweighs energy demand. This observation suggests that mitochondrial deficiency in muscle insulin resistance is not merely owing to intrinsic functional defects, but could instead be an adaptation to nutrient-induced changes in energy expenditure. Such adaptive effects are likely because muscle ATP supply is fully driven by energy demand. This market-economic control of myocellular bioenergetics offers a mechanism by which insulin-signalling deficiency can cause apparent mitochondrial dysfunction, as insulin resistance lowers skeletal muscle anabolism and thus dampens ATP demand and, consequently, oxidative ATP synthesis.
Keywords: Muscle insulin sensitivity; Mitochondria; Oxidative phosphorylation; Reactive oxygen species; ATP turnover; Control of cellular bioenergetics;
Membrane-bound electron transport systems of an anammox bacterium: A complexome analysis by Naomi M. de Almeida; Hans J.C.T. Wessels; Rob M. de Graaf; Christina Ferousi; Mike S.M. Jetten; Jan T. Keltjens; Boran Kartal (1694-1704).
Electron transport, or oxidative phosphorylation, is one of the hallmarks of life. To this end, prokaryotes evolved a vast variety of protein complexes, only a small part of which have been discovered and studied. These protein complexes allow them to occupy virtually every ecological niche on Earth. Here, we applied the method of proteomics-based complexome profiling to get a better understanding of the electron transport systems of the anaerobic ammonium-oxidizing (anammox) bacteria, the N2-producing key players of the global nitrogen cycle. By this method nearly all respiratory complexes that were previously predicted from genome analysis to be involved in energy and cell carbon fixation were validated. More importantly, new and unexpected ones were discovered. We believe that complexome profiling in concert with (meta)genomics offers great opportunities to expand our knowledge on bacterial respiratory processes at a rapid and massive pace, in particular in new and thus far poorly investigated non-model and environmentally-relevant species.Display Omitted
Keywords: Anaerobic ammonium oxidation (anammox); Complexome profiling; Blue Native gel electrophoresis; Respiratory complexes;
The obligate respiratory supercomplex from Actinobacteria by Wei-Chun Kao; Thomas Kleinschroth; Wolfgang Nitschke; Frauke Baymann; Yashvin Neehaul; Petra Hellwig; Sebastian Richers; Janet Vonck; Michael Bott; Carola Hunte (1705-1714).
Actinobacteria are closely linked to human life as industrial producers of bioactive molecules and as human pathogens. Respiratory cytochrome bcc complex and cytochrome aa 3 oxidase are key components of their aerobic energy metabolism. They form a supercomplex in the actinobacterial species Corynebacterium glutamicum. With comprehensive bioinformatics and phylogenetic analysis we show that genes for cyt bcc-aa 3 supercomplex are characteristic for Actinobacteria (Actinobacteria and Acidimicrobiia, except the anaerobic orders Actinomycetales and Bifidobacteriales). An obligatory supercomplex is likely, due to the lack of genes encoding alternative electron transfer partners such as mono-heme cyt c. Instead, subunit QcrC of bcc complex, here classified as short di-heme cyt c, will provide the exclusive electron transfer link between the complexes as in C. glutamicum. Purified to high homogeneity, the C. glutamicum bcc-aa 3 supercomplex contained all subunits and cofactors as analyzed by SDS-PAGE, BN-PAGE, absorption and EPR spectroscopy. Highly uniform supercomplex particles in electron microscopy analysis support a distinct structural composition. The supercomplex possesses a dimeric stoichiometry with a ratio of a-type, b-type and c-type hemes close to 1:1:1. Redox titrations revealed a low potential bcc complex (Em ISP = + 160 mV, Em b L = − 291 mV, Em b H = − 163 mV, Em cc = + 100 mV) fined-tuned for oxidation of menaquinol and a mixed potential aa 3 oxidase (Em CuA = + 150 mV, Em a/a3 = + 143/+317 mV) mediating between low and high redox potential to accomplish dioxygen reduction. The generated molecular model supports a stable assembled supercomplex with defined architecture which permits energetically efficient coupling of menaquinol oxidation and dioxygen reduction in one supramolecular entity.Display Omitted
Keywords: menaquinone; Actinobacteria; respiratory chain; cytochrome oxidase; cytochrome bc 1 complex; supercomplex;
Metabolite transport and associated sugar signalling systems underpinning source/sink interactions by Cara A. Griffiths; Matthew J. Paul; Christine H. Foyer (1715-1725).
Metabolite transport between organelles, cells and source and sink tissues not only enables pathway co-ordination but it also facilitates whole plant communication, particularly in the transmission of information concerning resource availability. Carbon assimilation is co-ordinated with nitrogen assimilation to ensure that the building blocks of biomass production, amino acids and carbon skeletons, are available at the required amounts and stoichiometry, with associated transport processes making certain that these essential resources are transported from their sites of synthesis to those of utilisation. Of the many possible posttranslational mechanisms that might participate in efficient co-ordination of metabolism and transport only reversible thiol-disulphide exchange mechanisms have been described in detail. Sucrose and trehalose metabolism are intertwined in the signalling hub that ensures appropriate resource allocation to drive growth and development under optimal and stress conditions, with trehalose-6-phosphate acting as an important signal for sucrose availability. The formidable suite of plant metabolite transporters provides enormous flexibility and adaptability in inter-pathway coordination and source-sink interactions. Focussing on the carbon metabolism network, we highlight the functions of different transporter families, and the important of thioredoxins in the metabolic dialogue between source and sink tissues. In addition, we address how these systems can be tailored for crop improvement.Metabolite transport not only allows the flawless coordination of pathways in different organelles and between cells, but it is also balances energy provision and utilisation throughout the whole plant. Plant metabolite transport displays enormous plasticity and flexible regulation. Focussing particularly on carbon transporters, this review discusses transport functions in source and sinks organs, with sucrose and trehalose in source-sink communication that encompasses sophisticated perception and signalling systems.Display Omitted
Keywords: Phloem loading; Redox regulation; Source-sink interactions; Sucrose transporters; Sugar signalling; Trehalose;