Photosynthesis Research (v.97, #1)

The use of various computational techniques for the study of photosynthetic systems is described ranging from genome analysis to density functional simulations of the oxygen evolving complex of PSII. The use of simulations for analyzing protein structures can aid in clarifying ambiguous and incomplete experimental results to identifying underlying rules to create efficient light-initiated charge separation at high efficiency.
Keywords: Photosynthesis; Simulation; OEC; Solar energy; Continuum electrostatics; Molecular dynamics

Phototroph genomics ten years on by Jason Raymond; Wesley D. Swingley (5-19).
The onset of the genome era means different things to different people, but it is clear that this new age brings with it paradigm shifts that will forever affect biological research. Less clear is just how these shifts are changing the scope and scale of research. Are gigabases of raw data more useful than a single well-understood gene? Do we really need a full genome to understand the physiology of a single organism? The photosynthetic field is poised at the periphery of the bulk of genome sequencing work—understandably skewed toward health-related disciplines—and, as such, is subject to different motivations, limitations, and primary focus for each new genome. To understand some of these differences, we focus here on various indicators of the impact that genomics has had on the photosynthetic community, now a full decade since the publication of the first photosynthetic genome. Many useful indicators are indexed in public databases, providing pre- and post-genome sequence snapshots of changes in factors such as publication rate, number of proteins characterized, and sequenced genome coverage versus known diversity. As more genomes are sequenced and metagenomic projects begin to pour out billions of bases, it becomes crucial to understand how to harness this data in order to accumulate possible benefits and avoid possible pitfalls, especially as resources become increasingly directed toward natural environments governed by photosynthetic activity, ranging from hot springs to tropical forest ecosystems to the open ocean.
Keywords: Genome sequencing; Cyanobacteria; Proteobacteria; Heliobacteria; Chloroflexi; Chlorobi; Metagenomics

In photoexcitation and electron transfer, a new dipole or charge is introduced, and the structure is adjusted. This adjustment represents dielectric relaxation, which is the focus of this review. We concentrate on a few selected topics. We discuss linear response theory, as a unifying framework and a tool to describe non-equilibrium states. We review recent, molecular dynamics simulation studies that illustrate the calculation of dynamic and thermodynamic properties, such as Stokes shifts or reorganization free energies. We then turn to the macroscopic, continuum electrostatic view. We recall the physical definition of a dielectric constant and revisit the decomposition of the free energy into a reorganization and a static term. We review some illustrative continuum studies and discuss some difficulties that can arise with the continuum approach. In conclusion, we consider recent developments that will increase the accuracy and broaden the scope of all these methods.
Keywords: Charge transfer; Continuum electrostatics; Free energy; Molecular dynamics; Poisson-Boltzmann equation; Redox protein

Investigating the mechanisms of photosynthetic proteins using continuum electrostatics by G. Matthias Ullmann; Edda Kloppmann; Timm Essigke; Eva-Maria Krammer; Astrid R. Klingen; Torsten Becker; Elisa Bombarda (33-53).
Computational methods based on continuum electrostatics are widely used in theoretical biochemistry to analyze the function of proteins. Continuum electrostatic methods in combination with quantum chemical and molecular mechanical methods can help to analyze even very complex biochemical systems. In this article, applications of these methods to proteins involved in photosynthesis are reviewed. After giving a short introduction to the basic concepts of the continuum electrostatic model based on the Poisson–Boltzmann equation, we describe the application of this approach to the docking of electron transfer proteins, to the comparison of isofunctional proteins, to the tuning of absorption spectra, to the analysis of the coupling of electron and proton transfer, to the analysis of the effect of membrane potentials on the energetics of membrane proteins, and to the kinetics of charge transfer reactions. Simulations as those reviewed in this article help to analyze molecular mechanisms on the basis of the structure of the protein, guide new experiments, and provide a better and deeper understanding of protein functions.
Keywords: Poisson–Boltzmann equation; Electrostatic potential; Membrane potential; Master equation; Docking; Spectral tuning; pH and redox titration

Semi-continuum electrostatic calculations of redox potentials in photosystem I by Vasily V. Ptushenko; Dmitry A. Cherepanov; Lev I. Krishtalik; Alexey Yu. Semenov (55-74).
The midpoint redox potentials (E m ) of all cofactors in photosystem I from Synechococcus elongatus as well as of the iron–sulfur (Fe4S4) clusters in two soluble ferredoxins from Azotobacter vinelandii and Clostridium acidiurici were calculated within the framework of a semi-continuum dielectric approach. The widely used treatment of proteins as uniform media with single dielectric permittivity is oversimplified, particularly, because permanent charges are considered both as a source for intraprotein electric field and as a part of dielectric polarizability. Our approach overcomes this inconsistency by using two dielectric constants: optical ε o  = 2.5 for permanent charges pre-existing in crystal structure, and static ε s for newly formed charges. We also take into account a substantial dielectric heterogeneity of photosystem I revealed by photoelectric measurements and a liquid junction potential correction for E m values of relevant redox cofactors measured in aprotic solvents. We show that calculations based on a single permittivity have the discrepancy with experimental data larger than 0.7 V, whereas E m values calculated within our approach fall in the range of experimental estimates. The electrostatic analysis combined with quantum chemistry calculations shows that (i) the energy decrease upon chlorophyll dimerization is essential for the downhill mode of primary charge separation between the special pair P700 and the primary acceptor A0; (ii) the primary donor is apparently P700 but not a pair of accessory chlorophylls; (iii) the electron transfer from the A branch quinone QA to the iron–sulfur cluster FX is most probably downhill, whereas that from the B branch quinone QB to FX is essentially downhill.
Keywords: Chlorophyll; Electrometric data; Ferredoxin; Iron–sulfur cluster; Multilayer dielectric model; Optical and static dielectric permittivities; Photosystem I; Phylloquinone; Semi-continuum electrostatics

Conversion of light energy in photosynthesis is extremely fast and efficient, and understanding the nature of this complex photophysical process is challenging. This review describes current progress in understanding molecular mechanisms of light harvesting and charge separation in photosystem II (PSII). Breakthroughs in X-ray crystallography have allowed the development and testing of more detailed kinetic models than have previously been possible. However, due to the complexity of the light conversion processes, satisfactory descriptions remain elusive. Recent advances point out the importance of variations in the photochemical properties of PSII in situ in different thylakoid membrane regions as well as the advantages of combining sophisticated time-resolved spectroscopic experiments with atomic level computational modeling which includes the effects of molecular dynamics.
Keywords: Photosystem II; Energy transfer; Excited states; Charge separation; Light harvesting; Kinetic modeling; QM/MM; Chlorophyll fluorescence; Chlorophyll absorption

Computational insights into the O2-evolving complex of photosystem II by Eduardo M. Sproviero; James P. McEvoy; José A. Gascón; Gary W. Brudvig; Victor S. Batista (91-114).
Mechanistic investigations of the water-splitting reaction of the oxygen-evolving complex (OEC) of photosystem II (PSII) are fundamentally informed by structural studies. Many physical techniques have provided important insights into the OEC structure and function, including X-ray diffraction (XRD) and extended X-ray absorption fine structure (EXAFS) spectroscopy as well as mass spectrometry (MS), electron paramagnetic resonance (EPR) spectroscopy, and Fourier transform infrared spectroscopy applied in conjunction with mutagenesis studies. However, experimental studies have yet to yield consensus as to the exact configuration of the catalytic metal cluster and its ligation scheme. Computational modeling studies, including density functional (DFT) theory combined with quantum mechanics/molecular mechanics (QM/MM) hybrid methods for explicitly including the influence of the surrounding protein, have proposed chemically satisfactory models of the fully ligated OEC within PSII that are maximally consistent with experimental results. The inorganic core of these models is similar to the crystallographic model upon which they were based, but comprises important modifications due to structural refinement, hydration, and proteinaceous ligation which improve agreement with a wide range of experimental data. The computational models are useful for rationalizing spectroscopic and crystallographic results and for building a complete structure-based mechanism of water-splitting in PSII as described by the intermediate oxidation states of the OEC. This review summarizes these recent advances in QM/MM modeling of PSII within the context of recent experimental studies.
Keywords: Oxomanganese complexes; Photosystem II; Water oxidation; Oxygen evolution; Oxygen evolving center; Photosynthesis; Quantum mechanics/molecular mechanics (QM/MM); Density functional theory (DFT)