Chirality-based signatures of local protein environments in two-dimensional optical spectroscopy of two species photosynthetic complexes of green sulfur bacteria: simulation study

Two-dimensional electronic chirality-induced signals of excitons in the photosynthetic Fenna-Matthews-Olson complex from two species of green sulfur bacteria (Chlorobium tepidum and Prosthecochloris aestuarii) are compared. The spectra are predicted to provide sensitive probes of local protein environment of the constituent bacteriochlorophyll a chromophores and reflect electronic structure variations (site energies and couplings) of the two complexes. Pulse polarization configurations are designed that can separate the coherent and incoherent exciton dynamics contributions to the two-dimensional spectra.     

Coherent phenomena in photosynthetic light harvesting: part one—theory and spectroscopy

The role of non-trivial quantum mechanical effects in biology has been the subject of intense scrutiny over the past decade. Much of the focus on potential “quantum biology” has been on energy transfer processes in photosynthetic light harvesting systems. Ultrafast laser spectroscopy of several light harvesting proteins has uncovered coherent oscillations dubbed “quantum beats” that persist for hundreds of femtoseconds and are putative signatures for quantum transport phenomena. This review describes the language and basic quantum mechanical phenomena that underpin quantum transport in open systems such as light harvesting and photosynthetic proteins, including the photosystem reaction centre. Coherent effects are discussed in detail, separating various meanings of the term, from delocalized excitations, or excitons, to entangled states and coherent transport. In particular, we focus on the time, energy and length scales of energy transport processes, as these are critical in understanding whether or not coherent processes are important. The role played by the protein in maintaining chromophore systems is analysed. Finally, the spectroscopic techniques that are used to probe energy transfer dynamics and that have uncovered the quantum beats are described with reference to coherent phenomena in light harvesting.     

Coherent phenomena in photosynthetic light harvesting: part two—observations in biological systems

Considerable debate surrounds the question of whether or not quantum mechanics plays a significant, non-trivial role in photosynthetic light harvesting. Many have proposed that quantum superpositions and/or quantum transport phenomena may be responsible for the efficiency and robustness of energy transport present in biological systems. The critical experimental observations comprise the observation of coherent oscillations or “quantum beats” via femtosecond laser spectroscopy, which have been observed in many different light harvesting systems. Part Two of this review aims to provide an overview of experimental observations of energy transfer in the most studied light harvesting systems. Length scales, derived from crystallographic studies, are combined with energy and time scales of the beats observed via spectroscopy. A consensus is emerging that most long-lived (hundreds of femtoseconds) coherent phenomena are of vibrational or vibronic origin, where the latter may result in coherent excitation transport within a protein complex. In contrast, energy transport between proteins is likely to be incoherent in nature. The question of whether evolution has selected for these non-trivial quantum phenomena may be an unanswerable question, as dense packings of chromophores will lead to strong coupling and hence non-trivial quantum phenomena. As such, one cannot discern whether evolution has optimised light harvesting systems for high chromophore density or for the ensuing quantum effects as these are inextricably linked and cannot be switched off.     

Quantum nanomagnets: From relaxation to coherence

At the nanometer scale, a magnet is quantum. A single crystal made of a network of nanomagnets is a macroscopic quantum object (incoherent). The first object of this class which was discovered is the so-called molecular complex Mn₁₂-ac with a spin S = 10 per molecule. With vanishingly small tunneling gaps this system opened the field of slow quantum dynamics, allowing in particular the study of interplays between classical and quantum magnetism. The first part of this paper gives an overview of this new type of mesoscopic physics. An extension to the case non-interacting rare-earth ions is presented in the second part, showing that mesoscopic magnetism can reach the atomic scale. Modifications occur in the spin-bath allowing the observation of two- and four-spins entanglements of electro-nuclear states. If rare-earth ions are more diluted this system undergoes a progressive transition from the relaxation regime to the coherence regime where Rabi oscillations are observed. This leads to the rare-earth spin qubits with new possibilities in quantum computation.     

Electronic excitations in condensed biological matter

In living matter, electronic excitations may have a collective character which is reviewed here in simple physical terms. In liquids and ordered solids the collective excitations appear as plasmons or excitons. Plasmons are delocalized electronic perturbations of a huge number of oscillating electrons decaying very quickly into localized electronic perturbations, mainly low-energy ionizations. Excitons are very light, moving quantum quasi-particles carrying energy, charge and information in structured biological systems. In deformable soft structures collective excitations appear as solitons behaving as rather massive quasi-particles of combined quantum and classical character. Solitons are relatively stable micro-objects able to transfer energy, charge, mass, and biological information along such biological structures as (chains of) macromolecules, fibres, membranes and surfaces. Some photobiological and radiation biological consequences of collective electronic excitations are suggested.     

Efficiency of excitation energy trapping in the green photosynthetic bacterium Chlorobaculum tepidum

During the millions of years of evolution, photosynthetic organisms have adapted to almost all terrestrial and aquatic habitats, although some environments are obviously more suitable for photosynthesis than others. Photosynthetic organisms living in low-light conditions require on the one hand a large light-harvesting apparatus to absorb as many photons as possible. On the other hand, the excitation trapping time scales with the size of the light-harvesting system, and the longer the distance over which the formed excitations have to be transferred, the larger the probability to lose excitations. Therefore a compromise between photon capture efficiency and excitation trapping efficiency needs to be found. Here we report results on the whole cells of the green sulfur bacterium Chlorobaculum tepidum. Its efficiency of excitation energy transfer and charge separation enables the organism to live in environments with very low illumination. Using fluorescence measurements with picosecond resolution, we estimate that despite a rather large size and complex composition of its light-harvesting apparatus, the quantum efficiency of its photochemistry is around ~87% at 20?°C, ~83% at 45?°C, and about ~81% at 77?K when part of the excitation energy is trapped by low-energy bacteriochlorophyll a molecules. The data are evaluated using target analysis, which provides further insight into the functional organization of the low-light adapted photosynthetic apparatus.     

A theory of excitation transfer in photosynthetic units

A theory of the excitation kinetics in the bacteria photosynthetic unit with regard to its globular structure is presented. It assumes that the excitation transfer between globulae is carried out by means of the mechanism of incoherent excitons, at the same time considering the finite time of the excitation fixation in the reaction center. A method of local perturbations is used with a view to finding a solution to the given problem. The expressions obtained for the fluorescence decay time and its quantum yield are discussed in connection with the multiple experiments considering the cubic as well as the hexagonal probable structure of the photosynthetic unit. The analysis given shows that the period of the excitation transfer between globulae equals 10 to 100 psec and the number of the globulae is less than 35. These conclusions fall in with the initial assumption of the energy transfer between globulae by incoherent excitons. Without considering the globularity, the consistency of the theory with experimental data becomes difficult.     

Analysis of exciton parameters in DNA. Exciton waves in DNA as one of the reasons of mutagenesis

Formulae were obtained for the quantitative analysis of the following parameters of excitons in DNA: 1) the lifetime of electronic excitation; 2) the numbers of exciton runs along the DNA sequence; 3) the energy loss by an exciton for one run; 4) the maximum length of the DNA sequence capable of deactivating an exciton for one run. The maximum and minimum ranges for the constant of electronic excitation migration was determined to meet the requirement of inductive-resonance energy transfer for the case of strong interaction. The constant of exciton energy migration was shown to depend on the activation energy, which is equal to the energy of absorbed quantum. An analytical formula was derived to determine the number of quanta the DNA molecule is able to absorb, depending on its length, without nonlinear effects (without overlapping of spatial areas of electronic excitation). By this formula, DNA sequences consisting of only identical AT and GC nucleotide pairs and aggregate AT + GC (in the ratio 1:1) DNA sequences ranging from 1 up to 10(10) base pairs were analyzed. The results of the analysis suggest that the overlapping of spatial areas of electronic excitation induced by a single ultraviolet quantum occurs in short DNA sequences characteristic of prokaryotes. To achieve the same effects on long DNA sequences specific for eukaryotes, DNA must synchronously absorb a great number of ultraviolet quanta. Based on the above results, the following conclusions were made: 1) disturbances in the normal activity of DNA and RNA polymerases may be due to electromagnetic field, which is caused by the oscillatory relaxation of vibronic levels of nucleotides. The energy enters the vibronic levels of nucleotides from an exciton running along the DNA sequence; 2) the increase in the noncoding DNA sequences in eukaryotes due to evolution is a way of DNA protection from undesirable mutations; 3) prokaryotes must possess a greater potentiality and a higher rate of mutagenesis in comparison with eukaryotes, which is proved by their greater diversity in nature.     

Application of matched filtering to identify behavioral modulation of brain oscillations

Brain oscillations modulated by motor behaviors are coupled to steady-state and other potentially unrelated to movement oscillations, with energy in the same frequency bands as the signals of interest. We applied matched filtering, a quasi-optimum signal detection technique, to decouple and extract movement-related signals from local field potentials (LFPs) recorded in monkey motor cortical areas during the execution of a visually instructed reach-out task. Using a matched-filterbank, we examined coupling and interference of pre-movement and initial steady-state oscillations with movement-induced signals. Once these signal contributions were eliminated, we were able to identify significant correlations of the residual signals with behavioral parameters, which appeared attenuated by pre-movement signal interference in the raw LFPs. Specifically, the maximum and minimum amplitudes of filtered LFPs were directly modulated by peak movement velocity and micro-movements, respectively, identified in recorded hand velocity profiles. In addition, we identified phase correlations between signals during the delay (when the instructional cue was presented) and movement intervals, as well as modulation of LFP phase by movement direction. For pairs of orthogonal movement directions, corresponding LFP signals were consistently out of phase. Finally, β-band energy which is typically reduced during movement execution, possibly partly due to destructive interference between the modulated by behavior signal and unrelated oscillations, appeared to be recovered in the filtered signals.     

Extracting the Excitonic Hamiltonian of the Fenna-Matthews-Olson Complex Using Three-Dimensional Third-Order Electronic Spectroscopy

We extend traditional two-dimensional (2D) electronic spectroscopy into a third Fourier dimension without the use of additional optical interactions. By acquiring a set of 2D spectra evenly spaced in waiting time and dividing the area of the spectra into voxels, we can eliminate population dynamics from the data and transform the waiting time dimension into frequency space. The resultant 3D spectrum resolves quantum beating signals arising from excitonic coherences along the waiting frequency dimension, thereby yielding up to 2n-fold redundancy in the set of frequencies necessary to construct a complete set of n excitonic transition energies. Using this technique, we have obtained, to our knowledge, the first fully experimental set of electronic eigenstates for the Fenna-Matthews-Olson (FMO) antenna complex, which can be used to improve theoretical simulations of energy transfer within this protein. Whereas the strong diagonal peaks in the 2D rephasing spectrum of the FMO complex obscure all but one of the crosspeaks at 77 K, extending into the third dimension resolves 19 individual peaks. Analysis of the independently collected nonrephasing data provides the same information, thereby verifying the calculated excitonic transition energies. These results enable one to calculate the Hamiltonian of the FMO complex in the site basis by fitting to the experimental linear absorption spectrum.     

Increased photosynthetic activities and thermostability of photosystem II with leaf development of elm seedlings (Ulmus pumila) probed by the fast fluorescence rise OJIP

Experiments were conducted to investigate the photosynthetic activity and thermostability of photosystem II (PSII) in elm seedling (Ulmus pumila) leaves from initiation to full expansion. During leaf development, photosynthesis, measured as CO₂ fixation, increased gradually and reached a maximum value when leaves were fully developed. In parallel with the increase of carbon assimilation, chlorophyll content increased. The chlorophyll a fluorescence measurements showed that the maximum quantum yield of PSII primary photochemistry (φ_po), the efficiency with which the energy of trapped excitons is converted into the electron transport beyond Q_A (Ψ_o) and the quantum yield of electron transport beyond Q_A (φ_Eo) increased gradually. The low light experiments confirmed these results independently. When subjected to heat stress, young leaves exhibited progressively lower φ_po and maximal fluorescence (F_m) values with considerably higher minimal fluorescence (F_o) than mature leaves, demonstrating that PSII in newly initiating leaves is more sensitive to heat stress. Further analysis revealed that PSII structure in newly initiating leaves showed a robust alteration under heat stress, which was reflected by the clear K phase in the OJIP curves. Therefore, we suggest that the enhanced thermostability of PSII in the case of leaf growth might be associated with an improvement of the stability of the oxygen-evolving complex (OEC) to heat stress during leaf development.     

Visualization of excitonic structure in the Fenna-Matthews-Olson photosynthetic complex by polarization-dependent two-dimensional electronic spectroscopy

Photosynthetic light-harvesting proceeds by the collection and highly efficient transfer of energy through a network of pigment-protein complexes. Interchromophore electronic couplings and interactions between pigments and the surrounding protein determine energy levels of excitonic states, and dictate the mechanism of energy flow. The excitonic structure (orientation of excitonic transition dipoles) of pigment-protein complexes is generally deduced indirectly from x-ray crystallography, in combination with predictions of transition energies and couplings in the chromophore site basis. We demonstrate that coarse-grained, excitonic, structural information in the form of projection angles between transition dipole moments can be obtained from the polarization-dependent, two-dimensional electronic spectroscopy of an isotropic sample, particularly when the nonrephasing or free polarization decay signal, rather than the photon echo signal, is considered. This method provides an experimental link between atomic and electronic structure, and accesses dynamical information with femtosecond time resolution. In an investigation of the Fenna-Matthews-Olson complex from green sulfur bacteria, the energy transfer connecting two particular exciton states in the protein was isolated as the primary contributor to a crosspeak in the nonrephasing two-dimensional spectrum at 400 femtoseconds under a specific sequence of polarized excitation pulses. The results suggest the possibility of designing experiments using combinations of tailored polarization sequences to separate and monitor individual relaxation pathways.     

Energy upconversion theory of the primary photochemical reaction in plant photosynthesis

In this paper we suggest a basic mechanism for the utilization of light quanta in photosynthesis. Through interactions between the lowest lying triplet state of the reaction-center chlorophylls and the first excited singlet state of the antenna chlorophylls, absorbed light quanta are upconverted to a higher-lying charge transfer state of the reaction-center Chl molecules. It is shown that the efficiency of the upconversion process is maximized by the parallel configuration of the two Chl porphyrin rings in the reaction-center water adduct proposed by the writer. Steady-state solutions are obtained, and the theoretical results are shown to account for a variety of crucial experimental observations including (1) the doubling (in whole cells) of in vivo fluorescence quantum yield of system II in strong light, (2) the observation by Dutton et al. of the light-induced triplet-state reaction-center bacteriochlorophyll when the primary electron acceptor is reduced and (3) despite the apparent involvement of two excitations in the energy upconversion process, only one quantum is needed for the transfer of one electron in the primary photo-chemical reaction, satisfying the eight-quanta requirement for the evolution of one O₂ molecule in photosynthesis.     

Effects of hypo- and hypersalinity on photosynthetic performance of Sargassum fusiforme (Fucales,Heterokontophyta)

Photoprotection mechanisms protect photosynthetic organisms, especially under stress conditions, against photodamage that may inhibit photosynthesis. We investigated the effects of short-term immersion in hypo- and hypersalinity sea water on the photosynthesis and xanthophyll cycle in Sargassum fusiforme (Harvey) Setchell. The results indicated that under moderate light [110 μmol(photon) m^?2 s^?1], the effective quantum yield of PSII was not reduced in S. fusiforme fronds after 1 h in hyposalinity conditions, even in fresh water, but it was significantly affected by extreme hypersalinity treatment (90‰ sea water). Under high light [HL, 800 μmol(photon) m^?2 s^?1], photoprotective mechanisms operated efficiently in fronds immersed in fresh water as indicated by high reversible nonphotochemical quenching of chlorophyll fluorescence (NPQ) and de-epoxidation state; the quantum yield of PSII recovered during the subsequent relaxation period. In contrast, fronds immersed in 90‰ sea water did not withstand HL, barely developed reversible NPQ, and accumulated little antheraxanthin and zeaxanthin during HL, while recovery of the quantum yield of PSII was severely inhibited during the subsequent relaxation period. The data provided concrete evidence supporting the short-term tolerance of S. fusiforme to immersion in fresh water compared to hypersalinity conditions. The potential practical implications of these results were also discussed.     

Protein interactions and dynamics probed by quantum chemistry, computer simulations and neutron experiments

We review some recent experiments and calculations on aspects of the structure and dynamics of proteins and related systems. The use of quantum chemical techniques to determine geometries and energies of supramolecular complexes of biological interest is illustrated, and the concomitant development of empirical energy functions for use in protein simulations outlined. We describe how simulations of crystalline peptides and amino-acids using an empirical force field can be combined with appropriate coherent and incoherent inelastic neutron scattering experiments to elucidate the characteristics of lattice vibrations and diffusive atomic motions in the crystals. The application of molecular dynamics simulations to the interpretation of incoherent neutron scattering experiments on proteins is examined and the resulting ideas on the general characteristics of protein motion discussed in terms of their functional implications.     

Near-Infrared Super Resolution Imaging with Metallic Nanoshell Particle Chain Array

We propose a near-infrared super resolution near field imaging system with an array of metallic nanoshell particle chain. The imaging array can plasmonically transfer the near field components of dipole sources and the super resolution images can be reconstructed in the output plane. By decreasing the metallic nanoshell’s thickness of the fixed size nanoparticle, the plasmon resonance wavelength of the isolate nanoshell particle is red-shifted to the near-infrared region. The operation wavelength of the imaging array is correspondingly red-shifted to the near-infrared region. In this paper, we study the incoherent and coherent super resolution imaging. The field intensity distributions at the different planes of imaging process are calculated using the finite element method. The simulation results demonstrate that the array has super resolution imaging capability at near-infrared wavelengths in the incoherent and coherent manners. The results also show that the image formation highly depends on the source coherence. In the same structural parameters, the reconstructed images under the illumination of incoherent light source reach to the higher image quality and spatial resolution than the images under the illumination of coherent light source of in phase. By reasonably designing parameters of the imaging array, the approximate spatial resolutions of λ/13 in incoherent case and λ/10 in coherent case are obtained at the near-infrared wavelength of 764 nm. Furthermore, the image–array distance and the chains’ spacing also affect the image reconstruction.     

Loss of the precise control of photosynthesis and increased yield of non‐radiative dissipation of excitation energy after mild heat treatment of barley leaves

The after effects of a short exposure of intact barley leaves to moderately elevated temperature (40°C, 5 min) on the induction transients and the irradiance dependencies of photosynthesis and chlorophyll fluorescence are presented. This mild heat treatment strongly reduced the oscillations in the rate of photosynthesis and in the yield of chlorophyll fluorescence. However, only a 25% irreversible inhibition of maximum photosynthetic capacity of photosystem II (PSII) measured by oxygen evolution was produced and the intrinsic quantum yield of PSII measured by the chlorophyll fluorescence ratio (F_m‐ F_o)/F_m decreased by only 15%. In contrast, the above treatment increased radiationless dissipation processes in PSII by a factor of two. In heat‐treated leaves, photosynthesis was not saturated even by strong light. Both ΔpH‐dependent quenching of excitons in PSII (including formation of zeaxanthin) and state 1/state 2 transition were found to be stimulated. Heat exposure enhanced the control of PSII activity by PSI, as evidenced by a significant increase in the quenching effect of far‐red light on the maximum yield of chlorophyll fluorescence. It was deduced that after mild heat treatment, the photosynthetic apparatus in leaves lacks the precise coordinating control of electron transport and carbon metabolism owing to the inability of PSII to support electron transport at a level adequate for carbon metabolism. This effect was not related to the small irreversible thermal damage to PSII, but was rather due to a significant increase in non‐photochemical quenching of excitation energy.     

A critical assessment of the information processing capabilities of neuronal microtubules using coherent excitations

Evidence for signaling, communication, and conductivity in microtubules (MTs) has been shown through both direct and indirect means, and theoretical models predict their potential use in both classical and quantum information processing in neurons. The notion of quantum information processing within neurons has been implicated in the phenomena of consciousness, although controversies have arisen in regards to adverse physiological temperature effects on these capabilities. To investigate the possibility of quantum processes in relation to information processing in MTs, a biophysical MT model is used based on the electrostatic interior of the tubulin protein. The interior is taken to constitute a double-well potential structure within which a mobile electron is considered capable of occupying at least two distinct quantum states. These excitonic states together with MT lattice vibrations determine the state space of individual tubulin dimers within the MT lattice. Tubulin dimers are taken as quantum well structures containing an electron that can exist in either its ground state or first excited state. Following previous models involving the mechanisms of exciton energy propagation, we estimate the strength of exciton and phonon interactions and their effect on the formation and dynamics of coherent exciton domains within MTs. Also, estimates of energy and timescales for excitons, phonons, their interactions, and thermal effects are presented. Our conclusions cast doubt on the possibility of sufficiently long-lived coherent exciton/phonon structures existing at physiological temperatures in the absence of thermal isolation mechanisms. These results are discussed in comparison with previous models based on quantum effects in non-polar hydrophobic regions, which have yet to be disproved.