Antenna systems serve to absorb light and to transmit excitation energy to the reaction center (RC) in photosynthetic organisms. As the emitted (bacterio)chlorophyll fluorescence competes with the photochemical utilization of the excitation, the measured fluorescence yield is informed by the migration of the excitation in the antenna. In this work, the fluorescence yield concomitant with the oxidized dimer (P+) of the RC were measured during light excitation (induction) and relaxation (in the dark) for whole cells of photosynthetic bacterium Rhodobacter sphaeroides lacking cytochrome c_2 as natural electron donor to P+ (mutant cycA). The relationship between the fluorescence yield and P+ (fraction of closed RC) showed deviations from the standard Joliot-Lavergne-Trissl model: 1) the hyperbola is not symmetric and 2) exhibits hysteresis. These phenomena originate from the difference between the delays of fluorescence relative to P+ kinetics during induction and relaxation, and in structural terms from the non-random distribution of the closed RCs during induction. The experimental findings are supported by Monte Carlo simulations and by results from statistical physics based on random walk approximations of the excitation in the antenna. The applied mathematical treatment demonstrates the generalization of the standard theory and sets the stage for a more adequate description of the long-debated kinetics of fluorescence and of the delicate control and balance between efficient light harvest and photoprotection in photosynthetic organisms.
In photosynthetic organisms, the energy of light during illumination is absorbed by the antenna complexes, which is transmitted by excitons and is either absorbed by the reaction centers (RCs), which have been closed in this way, or emitted by fluorescence. The basic components of the dynamics of light absorption have been integrated into a simple model of exciton migration, which contains two parameters: the exciton hopping probability and the exciton lifetime. During continuous radiation with light the fraction of closed RCs, $x$, continuously increases and at a critical threshold, $x_c$, a …
We investigate the effect of coherence to the excitation transfer efficiency (ETE) in photosynthetic bacteria Chlorobium Tepidum. We have modeled the monomer of Fenna-Matthews-Olson (FMO) complex as consisting of eight bacteriochlorophyll-a sites, while explicitly consider reaction center core complex (RCC) as an additional site. With the use of realistic bath spectrum and several dominant vibronic modes in the non-Markovian master equation, in an effective 9-site model, we have compared the ETE for an initial pure state and an initial mixed state. We observe that the initial pure state relaxe…
We present a variation of two-dimensional electronic spectroscopy that is capable of mapping spatially-varying differences in electronic couplings using a correlated map of excitation and detection frequencies, with sensitivity orders of magnitude better than conventional spatially-averaged electronic spectroscopies. The approach performs fluorescence-detection-based fully collinear two-dimensional electronic spectroscopy in a microscope, combining femtosecond time-resolution, sub-micron spatial resolution, and the sensitivity of fluorescence detection. We demonstrate the approach on a mixture…
Photosynthesis is remarkable, achieving near unity light harvesting quantum efficiency in spite of dynamic light conditions and noisy physiological environment. Under these adverse conditions, it remains unknown whether there exists a fundamental organizing principle that gives rise to robust photosynthetic light harvesting. Here, we present a noise-canceling network model that relates noisy physiological conditions, power conversion efficiency, and the resulting absorption spectrum of photosynthetic organisms. Taking external light conditions in three distinct niches - full solar exposure, li…
Advances in time resolved spectroscopy have provided new insight into the energy transmission in natural photosynthetic complexes. Novel theoretical tools and models are being developed in order to explain the experimental results. We provide a model calculation for the two-dimensional electronic spectra of Cholorobaculum tepidum which correctly describes the main features and transfer time scales found in recent experiments. From our calculation one can infer the coupling of the antenna chlorosome with the environment and the coupling between the chlorosome and the Fenna-Matthews-Olson comple…
Photosynthetic organisms rely on a series of self-assembled nanostructures with tuned electronic energy levels in order to transport energy from where it is collected by photon absorption, to reaction centers where the energy is used to drive chemical reactions. In the photosynthetic bacteria Chlorobaculum tepidum (Cba. tepidum), a member of the green sulphur bacteria (GSB) family, light is absorbed by large antenna complexes called chlorosomes. The exciton generated is transferred to a protein baseplate attached to the chlorosome, before traveling through the Fenna-Matthews-Olson (FMO) comple…
Photosynthetic organisms use networks of chromophores to absorb sunlight and deliver the energy to reaction centres, where charge separation triggers a cascade of chemical steps to store the energy. We present a detailed model of the light-harvesting complexes in purple bacteria, including explicit interaction with sunlight; energy loss through radiative and non-radiative processes; and dephasing and thermalizing effects of coupling to a vibrational bath. An important feature of the model is that we capture the effect of slow vibrational modes by introducing time-dependent disorder. Our model …
The study of how photosynthetic organisms convert light offers insight not only into nature's evolutionary process, but may also give clues as to how best to design and manipulate artificial photosynthetic systems -- and also how far we can drive natural photosynthetic systems beyond normal operating conditions, so that they can harvest energy for us under otherwise extreme conditions. In addition to its interest from a basic scientific perspective, therefore, the goal to develop a deep quantitative understanding of photosynthesis offers the potential payoff of enhancing our current arsenal of…
The remarkable rotational symmetry of the photosynthetic antenna complexes of purple bacteria has long been thought to enhance their light harvesting and excitation energy transport. We study the role of symmetry by modeling hypothetical antennas whose symmetry is broken by altering the orientations of the bacteriochlorophyll pigments. We find that in both LH2 and LH1 complexes, symmetry increases energy transfer rates by enabling the cooperative, coherent process of supertransfer. The enhancement is particularly pronounced in the LH1 complex, whose natural geometry outperforms the average ran…
The photosynthetic reaction center of plants and bacteria is an extremely efficient energy to charge conversion device. Solar photons create excitons in the pigment molecules. These excitons are then transferred to the reaction center where charge separation takes place. These processes - excitonic generation and subsequent charge separation are extremely efficient with almost unity efficiency. Taking pointers from this biophysical process, we propose a GaN quantum dot based solid state energy to charge conversion device idea that emulates the photosynthetic reaction center. This further sugge…
We report two-dimensional electronic spectroscopy (2DES) experiments on the bacterial reaction center (BRC) from purple bacteria, revealing hidden excitonic and vibronic structure. Through analysis of the coherent dynamics of the BRC we resolve specific coherent signatures that allow us to definitively assign the upper exciton energy of the "special pair." This assignment is supported by simulations of coherent dynamics of a reduced excitonic model of the BRC. The simulations also identify nonsecular vibronic coherence transfer processes neglected in standard models of photosynthetic energy tr…
Photosynthetic systems utilize adaptability to respond efficiently to fluctuations in their light environment. As a result, large photosynthetic yields can be achieved in conditions of low light intensity, while photoprotection mechanisms are activated in conditions of elevated light intensity. In sharp contrast with these observations, current theoretical models predict bacterial cell death for physiologically high light intensities. To resolve this discrepancy, we consider a unified framework to describe three stages of photosynthesis in natural conditions, namely light absorption, exciton t…
Chlorosomes are likely the largest and most efficient natural light-harvesting photosynthetic antenna systems. They are composed of large numbers of bacteriochlorophylls organized into supramolecular aggregates. We explore the microscopic origin of the fast excitation energy transfer in the chlorosome using the recently-resolved structure and atomistic-detail simulations. Despite the dynamical disorder effects on the electronic transitions of the bacteriochlorophylls, our simulations show that the exciton delocalizes over the entire aggregate in about 200 fs. The memory effects associated to t…
Light-harvesting complexes in natural photosynthetic systems, such as those in purple bacteria, consist of photo-reactive chromophores embedded in densely packed "antenna" systems organized in well-defined nanostructures. In the case of purple bacteria, the chromophore antennas are composed of natural J-aggregates such as bacteriochlorophylls and carotenoids. Inspired by the molecular composition of such biological systems, we create a library of organic materials composed of densely packed J-aggregates in a polymeric matrix, in which the matrix mimics a protein scaffold. This library of organ…
We study intact and bulging Escherichia coli cells using atomic force microscopy to separate the contributions of the cell wall and turgor pressure to the overall cell stiffness. We find strong evidence of power-law stress-stiffening in the E. coli cell wall, with an exponent of 1.22 \pm 0.12, such that the wall is significantly stiffer in intact cells (E = 23 \pm 8 MPa and 49 \pm 20 MPa in the axial and circumferential directions) than in unpressurized sacculi. These measurements also indicate that the turgor pressure in living cells E. coli is 29 \pm 3 kPa.
The Fenna-Matthews-Olson (FMO) antennae complex, responsible for light harvesting in green sulfur bacteria, consists of three monomers, each with seven chromophores. Here we show that multiple subsystems of the seven chromophores can transfer energy from either chromophore 1 or 6 to the reaction center with an efficiency matching or in many cases exceeding that of the full seven chromophore system. In the FMO complex these functional subsystems support multiple quantum pathways for efficient energy transfer that provide a built-in quantum redundancy. There are many instances of redundancy in n…
Photosynthesis transfers energy efficiently through a series of antenna complexes to the reaction center where charge separation occurs. Energy transfer in vivo is primarily monitored by measuring fluorescence signals from the small fraction of excitations that fail to result in charge separation. Here, we use two-dimensional electronic spectroscopy to follow the entire energy transfer process in a thriving culture of the purple bacteria, Rhodobacter sphaeroides. By removing contributions from scattered light, we extract the dynamics of energy transfer through the dense network of antenna comp…
We analyze several aspects of the transport dynamics in the LH1-RC core of purple bacteria, which consists basically in a ring of antenna molecules that transport the energy into a target molecule, the reaction center, placed in the center of the ring. We show that the periodicity of the system plays an important role to explain the relevance of the initial state in the transport efficiency. This picture is modified, and the transport enhanced for any initial state, when considering that molecules have different energies, and when including their interaction with the environment. We study this…
Living organisms have to adjust to their surrounding in order to survive in stressful conditions. We study this mechanism in one of most primitive creatures - photosynthetic green sulfur bacteria. These bacteria absorb photons very efficiently using the chlorosome antenna complexes and perform photosynthesis in extreme low-light environments. How the chlorosomes in green sulfur bacteria are acclimated to the stressful light conditions, for instance, if the spectrum of light is not optimal for absorption, is unknown. Studying Chlorobaculum tepidum cultures with far-red to near-infrared light-em…
Photosynthetic complexes improve the transfer of excitation energy from peripheral antennas to reaction centers in several ways. In particular, a downward energy funnel can direct excitons in the right direction, while coherent excitonic delocalization can enhance transfer rates through the cooperative phenomenon of supertransfer. However, isolating the role of purely coherent effects is difficult because any change to the delocalization also changes the energy landscape. Here, we show that the relative importance of the two processes can be determined by comparing the natural light-harvesting…
It has been suggested that excitation transport in photosynthetic light harvesting complexes features speedups analogous to those found in quantum algorithms. Here we compare the dynamics in these light harvesting systems to the dynamics of quantum walks, in order to elucidate the limits of such quantum speedups. For the Fenna-Matthews-Olson (FMO) complex of green sulfur bacteria, we show that while there is indeed speedup at short times, this is short lived (70 fs) despite longer lived (ps) quantum coherence. Remarkably, this time scale is independent of the details of the decoherence model. …
Charge separation in light-harvesting complexes occurs in a pair of tightly coupled chlorophylls at the heart of photosynthetic reaction centers of both plants and bacteria. Recently it has been shown that quantum coherence can, in principle, enhance the efficiency of a solar cell, working like a quantum heat engine (QHE). Here, we propose a biological quantum heat engine (BQHE) motivated by Photosystem {\rm II} reaction center (PS{\rm II} RC) to describe the charge separation. Our model mainly considers two charge-separation pathways more than that in the published literature. The two pathway…
In this paper we consider dynamics of a molecular system subjected to external pumping by a light source. Within a completely quantum mechanical treatment, we derive a general formula, which enables to asses effects of different light properties on the photo-induced dynamics of a molecular system. We show that once the properties of light are known in terms of certain two-point correlation function, the only information needed to reconstruct the system dynamics is the reduced evolution superoperator. The later quantity is in principle accessible through ultrafast non-linear spectroscopy. Consi…
We present a study on the evolution of the Fenna-Matthews-Olson bacterial photosynthetic pigment-protein complex. This protein complex functions as an antenna. It transports absorbed photons - excitons - to a reaction center where photosynthetic reactions initiate. The efficiency of exciton transport is therefore fundamental for the photosynthetic bacterium's survival. We have reconstructed an ancestor of the complex to establish whether coherence in the exciton transport was selected for or optimized over time. We have also investigated on the role of optimizing free energy variation upon fol…
Natural organisms such as photosynthetic bacteria, algae, and plants employ complex molecular machinery to convert solar energy into biochemical fuel. An important common feature shared by most of these photosynthetic organisms is that they capture photons in the form of excitons typically delocalized over a few to tens of pigment molecules embedded in protein environments of light harvesting complexes (LHCs). Delocalized excitons created in such LHCs remain well protected despite being swayed by environmental fluctuations, and are delivered successfully to their destinations over hundred nano…
Phototrophic organisms such as plants, photosynthetic bacteria and algae use microscopic complexes of pigment molecules to absorb sunlight. Within the light-harvesting complexes, which frequently have several functional and structural subunits, the energy is transferred in the form of molecular excitations with very high efficiency. Green sulfur bacteria are considered to be amongst the most efficient light-harvesting organisms. Despite multiple experimental and theoretical studies of these bacteria the physical origin of the efficient and robust energy transfer in their light-harvesting compl…
Long lasting coherence in photosynthetic pigment-protein complexes has been observed even at physiological temperatures. Experiments have demonstrated quantum coherent behaviour in the long-time operation of the D-Wave quantum computer as well. Quantum coherence is the common feature between the two phenomena. An explanations for eight orders of magnitude discrepancy between the single flux qubit coherence time and the long-time quantum behaviour of an array of thousand flux qubits in the quantum computer was suggested within a theory where the flux qubits are coupled to an environment of part…
Two distinct approaches, the Frenkel-Dirac time-dependent variation and the Haken-Strobl model, are adopted to study energy transfer dynamics in single-ring and double-ring light-harvesting systems in purple bacteria. It is found that inclusion of long-range dipolar interactions in the two methods results in significant increases in intra- or inter-ring exciton transfer efficiency. The dependence of exciton transfer efficiency on trapping positions on single rings of LH2 (B850) and LH1 is similar to that in toy models with nearest-neighbor coupling only. However, owing to the symmetry breaking…
For more than 50 years we have known that photosynthetic systems harvest solar energy with almost unit {\it quantum efficiency}. However, recent experimental evidence of {\it quantum coherence} during the excitonic energy transport in photosynthetic organisms challenges our understanding of this fundamental biological function. Currently, and despite numerous efforts, the causal connection between coherence and efficiency is still a matter of debate. We show, through the study of extensive simulations of quantum coherent transport on networks, that three dimensional structures characterized by…
Self-assembled supramolecular aggregates are excellent candidates for the design of efficient excitation transport devices. Both artificially prepared and natural photosynthetic aggregates in plants and bacteria present an important degree of disorder that is supposed to hinder excitation transport. Besides, molecular excitations couple to nuclear motion affecting excitation transport in a variety of ways. We present an exhaustive study of exciton dynamics in disordered nanorings with long-range interactions under the influence of a phonon bath and take the LH2 system of purple bacteria as a m…
The electronic excitation population and coherence dynamics in the chromophores of the photosynthetic light harvesting complex 2 (LH2) B850 ring from purple bacteria (Rhodopseudomonas acidophila) have been studied theoretically at both physiological and cryogenic temperatures. Similar to the well-studied Fenna-Matthews-Olson (FMO) protein, oscillations of the excitation population and coherence in the site basis are observed in LH2 by using a scaled hierarchical equation of motion (HEOM) approach. However, this oscillation time (300 fs) is much shorter compared to the FMO protein (650 fs) at c…
Excitation transfer through interacting systems plays an important role in many areas of physics, chemistry, and biology. The uncontrollable interaction of the transmission network with a noisy environment is usually assumed to deteriorate its transport capacity, especially so when the system is fundamentally quantum mechanical. Here we identify key mechanisms through which noise such as dephasing, perhaps counter intuitively, may actually aid transport through a dissipative network by opening up additional pathways for excitation transfer. We show that these are processes that lead to the inh…
The Fenna Mathews Olson (FMO) complex of green sulphur bacteria is an example of a photosynthetic pigment protein complex, in which the electronic properties of the pigments are modified by the protein environment to promote efficient excitonic energy transfer from antenna complexes to the reaction centres. Many of the electronic properties of the FMO complex can be extracted from knowledge of the static crystal structure. However, the recent observation and analysis of long lasting quantum dynamics in the FMO complex point to protein dynamics as a key factor in protecting and generating quant…
