Biological Light-harvesting Complexes Research Articles

Environment-Assisted Modulation of Heat Flux in a Bio-Inspired System Based on Collision Model.

The high energy transfer efficiency of photosynthetic complexes has been a topic of research across many disciplines. Several attempts have been made in order to explain this energy transfer enhancement in terms of quantum mechanical resources such as energetic and vibration coherence and constructive effects of environmental noise. The developments in this line of research have inspired various biomimetic works aiming to use the underlying mechanisms in biological light harvesting complexes for the improvement of synthetic systems. In this article, we explore the effect of an auxiliary hierarchically structured environment interacting with a system on the steady-state heat transport across the system. The cold and hot baths are modeled by a series of identically prepared qubits in their respective thermal states, and we use a collision model to simulate the open quantum dynamics of the system. We investigate the effects of system-environment, inter-environment couplings and coherence of the structured environment on the steady state heat flux and find that such a coupling enhances the energy transfer. Our calculations reveal that there exists a non-monotonic and non-trivial relationship between the steady-state heat flux and the mentioned parameters.

Active control of strong plasmon-exciton coupling in biomimetic pigment-polymer antenna complexes grown by surface-initiated polymerisation from gold nanostructures.

Plexcitonic antenna complexes, inspired by photosynthetic light-harvesting complexes, are formed by attachment of chlorophylls (Chl) to poly(cysteine methacrylate) (PCysMA) scaffolds grown by atom-transfer radical polymerisation from gold nanostructure arrays. In these pigment–polymer antenna complexes, localised surface plasmon resonances on gold nanostructures are strongly coupled to Chl excitons, yielding hybrid light–matter states (plexcitons) that are manifested in splitting of the plasmon band. Modelling of the extinction spectra of these systems using a simple coupled oscillator model indicates that their coupling energies are up to twice as large as those measured for LHCs from plants and bacteria. Coupling energies are correlated with the exciton density in the grafted polymer layer, consistent with the collective nature of strong plasmon–exciton coupling. Steric hindrance in fully-dense PCysMA brushes limits binding of bulky chlorophylls, but the chlorophyll concentration can be increased to ∼2 M, exceeding that in biological light-harvesting complexes, by controlling the grafting density and polymerisation time. Moreover, synthetic plexcitonic antenna complexes display pH- and temperature-responsiveness, facilitating active control of plasmon–exciton coupling. Because of the wide range of compatible polymer chemistries and the mild reaction conditions, plexcitonic antenna complexes may offer a versatile route to programmable molecular photonic materials.

2D Electronic Spectroscopic Techniques for Quantum Technology Applications.

2D electronic spectroscopy (2DES) techniques have gained particular interest given their capability of following ultrafast coherent and noncoherent processes in real-time. Although the fame of 2DES is still majorly linked to the investigation of energy and charge transport in biological light-harvesting complexes, 2DES is now starting to be recognized as a particularly valuable tool for studying transport processes in artificial nanomaterials and nanodevices. Particularly meaningful is the possibility of assessing coherent mechanisms active in the transport of excitation energy in these materials toward possible quantum technology applications. The diverse nature of these new target samples poses significant challenges and calls for a critical rethinking of the technique and its different realizations. With the confluence of promising new applications and rapidly developing technical capabilities, the enormous potential of 2DES techniques to impact the field of nanosystems, quantum technologies, and quantum devices is here delineated.

Ultrafast spectroscopic investigation of discrete co-assemblies of a Zn-porphyrin–polymer conjugate with a hexapyridyl template

One of the key features of biological light harvesting complexes (LHCs) is their incorporation of multi-chromophoric reaction centres via non-covalent interactions. Most synthetic mimics require relatively complex syntheses and are constructed in organic solvents. Here, we report the use of polymer self-assembly to enable the formation of Zn-porphyrin–pyridine complexes in aqueous solution. Time-resolved femtosecond pump–probe spectroscopy revealed four time constants, each associated with significant ground state bleach recovery, suggesting energy transfer between the porphyrin and pyridine. Self-assembly opens up new photophysical relaxation pathways, making it a useful additional strategy for the construction of more advanced LHC mimics.

Polarization control of radiation and energy flow in dipole-coupled nanorings

Collective optical excitations in dipole-coupled nanorings of sub-wavelength spaced quantum emitters exhibit extreme sub-radiance and field confinement facilitating an efficient and low-loss ring-to-ring energy transfer. We show that energy shifts, radiative lifetimes, and emission patterns of excitons and biexcitons in such rings can be tailored via the orientation of the individual dipoles. Tilting the polarization from perpendicular to tangential to the ring dramatically changes the lifetime of the symmetric exciton state from superradiance to subradiance with the radiated field acquiring orbital angular momentum. At a magic tilt angle all excitons are degenerate and the transport fidelity between two rings exhibits a minimum. Further simulations suggest that, for certain parameters, the decay decreases double-exponentially with the emitter’s density. Disorder in the rings’ structure can even enhance radiative lifetimes. The transport efficiency strongly depends on polarization and size, which we demonstrate by simulating a bio-inspired example of two rings with 9 and 16 dipoles as found in biological light harvesting complexes (LHC). The field distribution in the most superradiant state in a full LHC multi-ring structure shows tight sub-wavelength field confinement in the central ring, while long-lived subradiant states store energy in the outer rings.

DNA scaffold supports long-lived vibronic coherence in an indodicarbocyanine (Cy5) dimer.

Vibronic coupling between pigment molecules is believed to prolong coherences in photosynthetic pigment–protein complexes. Reproducing long-lived coherences using vibronically coupled chromophores in synthetic DNA constructs presents a biomimetic route to efficient artificial light harvesting. Here, we present two-dimensional (2D) electronic spectra of one monomeric Cy5 construct and two dimeric Cy5 constructs (0 bp and 1 bp between dyes) on a DNA scaffold and perform beating frequency analysis to interpret observed coherences. Power spectra of quantum beating signals of the dimers reveal high frequency oscillations that correspond to coherences between vibronic exciton states. Beating frequency maps confirm that these oscillations, 1270 cm−1 and 1545 cm−1 for the 0-bp dimer and 1100 cm−1 for the 1-bp dimer, are coherences between vibronic exciton states and that these coherences persist for ∼300 fs. Our observations are well described by a vibronic exciton model, which predicts the excitonic coupling strength in the dimers and the resulting molecular exciton states. The energy spacing between those states closely corresponds to the observed beat frequencies. MD simulations indicate that the dyes in our constructs lie largely internal to the DNA base stacking region, similar to the native design of biological light harvesting complexes. Observed coherences persist on the timescale of photosynthetic energy transfer yielding further parallels to observed biological coherences, establishing DNA as an attractive scaffold for synthetic light harvesting applications.

Optical excitations of chlorophyll a and b monomers and dimers.

A necessary first step in the development of technologies such as artificial photosynthesis is understanding the photoexcitation process within the basic building blocks of naturally occurring light harvesting complexes (LHCs). The most important of these building blocks in biological LHCs such as LHC II from green plants are the chlorophyll a (Chl a) and chlorophyll b (Chl b) chromophores dispersed throughout the protein matrix. However, efforts to describe such systems are still hampered by the lack of computationally efficient and accurate methods that are able to describe optical absorption in large biomolecules. In this work, we employ a highly efficient linear combination of atomic orbitals (LCAOs) to represent the Kohn-Sham (KS) wave functions at the density functional theory (DFT) level and perform time-dependent density functional theory (TDDFT) calculations in either the reciprocal space and frequency domain (LCAO-TDDFT-k-ω) or real space and time domain (LCAO-TDDFT-r-t) of the optical absorption spectra of Chl a and b monomers and dimers. We find that our LCAO-TDDFT-k-ω and LCAO-TDDFT-r-t calculations reproduce results obtained with a plane-wave (PW) representation of the KS wave functions (PW-TDDFT-k-ω) but with a significant reduction in computational effort. Moreover, by applying the Gritsenko, van Leeuwen, van Lenthe, and Baerends solid and correlation derivative discontinuity correction Δx to the KS eigenenergies, with both LCAO-TDDFT-k-ω and LCAO-TDDFT-r-t methods, we are able to semiquantitatively reproduce the experimentally measured photoinduced dissociation results. This work opens the path to first principles calculations of optical excitations in macromolecular systems.

Coupling biology to synthetic nanomaterials for semi-artificial photosynthesis.

Biohybrid artificial photosynthesis aims to combine the advantages of biological specificity with a range of syntheticnanomaterials to create innovative semi-synthetic systems for solar-to-chemical conversion. Biological systems utilize highly efficient molecular catalysts for reduction-oxidation reactions. They can operate with minimal overpotentials while selectively channeling reductant energy into specific transformation chemistries and product forming pathways. Nanomaterials can be synthesized to have efficient light-absorption capacity and tuneability of charge separation by manipulation of surface chemistries and bulk compositions. These complementary aspects have been combined in a variety of ways, for example, where biological light-harvesting complexes function as antenna for nanoparticle catalysts or where nanoparticles function as light capture, charge separation components for coupling to chemical conversion by redox enzymes and whole cells. The synthetic diversity that is possible with biohybrids is still being explored. The progress arising from creative approaches is generating new model systems to inspire scale-up technologies and generate understanding of the fundamental mechanisms that control energy conversion at the molecular scale. These efforts are leading to discoveries of essential design principles that can enable the development of scalable artificial photosynthesis systems.

Coherence in carotenoid-to-chlorophyll energy transfer

The subtle details of the mechanism of energy flow from carotenoids to chlorophylls in biological light-harvesting complexes are still not fully understood, especially in the ultrafast regime. Here we focus on the antenna complex peridinin–chlorophyll a–protein (PCP), known for its remarkable efficiency of excitation energy transfer from carotenoids—peridinins—to chlorophylls. PCP solutions are studied by means of 2D electronic spectroscopy in different experimental conditions. Together with a global kinetic analysis and multiscale quantum chemical calculations, these data allow us to comprehensively address the contribution of the potential pathways of energy flow in PCP. These data support dominant energy transfer from peridinin S2 to chlorophyll Qy state via an ultrafast coherent mechanism. The coherent superposition of the two states is functional to drive population to the final acceptor state, adding an important piece of information in the quest for connections between coherent phenomena and biological functions.

Programming Light-Harvesting Efficiency Using DNA Origami

The remarkable performance and quantum efficiency of biological light-harvesting complexes has prompted a multidisciplinary interest in engineering biologically inspired antenna systems as a possible route to novel solar cell technologies. Key to the effectiveness of biological “nanomachines” in light capture and energy transport is their highly ordered nanoscale architecture of photoactive molecules. Recently, DNA origami has emerged as a powerful tool for organizing multiple chromophores with base-pair accuracy and full geometric freedom. Here, we present a programmable antenna array on a DNA origami platform that enables the implementation of rationally designed antenna structures. We systematically analyze the light-harvesting efficiency with respect to number of donors and interdye distances of a ring-like antenna using ensemble and single-molecule fluorescence spectroscopy and detailed Förster modeling. This comprehensive study demonstrates exquisite and reliable structural control over multichromophoric geometries and points to DNA origami as highly versatile platform for testing design concepts in artificial light-harvesting networks.

Retaining individualities: the photodynamics of self-ordering porphyrin assemblies.

The retention of photochemical properties of individual chromophores is a key feature of biological light harvesting complexes. This is achieved despite extensive aggregation of the chromophores, which in synthetic chromophore assemblies often yields a change in spectral characteristics. As an alternative approach towards mimicking biological light harvesting complexes, we report the synthesis of porphyrin assemblies which retained the photochemical properties of the individual chromophore units despite their substantial aggregation. These new materials highlight a new bottom-up approach towards the design and understanding of more complex biomimetic and naturally occurring biological systems.

Interplay between Dephasing and Geometry and Directed Heat Flow in Exciton Transfer Complexes

The striking efficiency of energy transfer in natural photosynthetic systems and the recent evidence of long-lived quantum coherence in biological light harvesting complexes has triggered much excitement, due to the evocative possibility that these systems—essential to practically all life on earth–use quantum mechanical effects to achieve optimal functionality. A large body of theoretical work has addressed the role of local environments in determining the transport properties of excitons in photosynthetic networks and the survival of quantum coherence in a classical environment. Nonetheless, understanding the connection between quantum coherence, exciton network geometry, and energy transfer efficiency remains a challenge. Here we address this connection from the perspective of heat transfer within the exciton network. Using a nonequilibrium open quantum system approach and focusing on the Fenna–Matthews–Olson complex, we demonstrate that finite local dephasing can be beneficial to the overall power out...

Impact of quantized vibrations on the efficiency of interfacial charge separation in photovoltaic devices

We demonstrate that charge separation at donor-acceptor interfaces is a complex process that is controlled by the combined action of Coulomb binding for electron-hole pairs and partial relaxation due to quantized phonons. A joint electron-vibration quantum dynamical study reveals that high-energy vibrations sensitively tune the charge transfer probability as a function of time and injection energy, due to polaron formation. These results have bearings on the optimization of energy transfer both in organic and quantum dot photovoltaics, as well as in biological light harvesting complexes.

Polariton-mediated energy transfer between organic dyes in a strongly coupled optical microcavity.

Strongly coupled optical microcavities containing different exciton states permit the creation of hybrid-polariton modes that can be described in terms of a linear admixture of cavity-photon and the constituent excitons. Such hybrid states have been predicted to have optical properties that are different from their constituent parts, making them a test bed for the exploration of light-matter coupling. Here, we use strong coupling in an optical microcavity to mix the electronic transitions of two J-aggregated molecular dyes and use both non-resonant photoluminescence emission and photoluminescence excitation spectroscopy to show that hybrid-polariton states act as an efficient and ultrafast energy-transfer pathway between the two exciton states. We argue that this type of structure may act as a model system to study energy-transfer processes in biological light-harvesting complexes.

Computational Study on the Dependence of Electronic Transition Energies of Porphin, Chlorin, Mg-Chlorin and Chlorophyll a on an External Charge

SummaryIn order to understand the diversity in electronic transitionenergy of the chlorophyll molecules in biological lightharvesting complexes, we studied model systems of fourporphyrin derivatives, porphin, chlorin, Mg-chlorin, and Chla interacting with an external positive point charge locatedabove the tetrapyrollic ring plane. We calculated molecularorbitals and electronic transition energies to S1 and S2 statesfor the four molecules interacting with the point charge byusing TD-DFT method. The transition energies calculatedby the same computational method in the absence of thecharge are in reasonably good correlation to experimentaldata and then we examined the quantum chemical charac-teristics of electronic transitions of the porphyrin derivativesinfluenced by the external point charge. The transition energies of non-metallic derivatives arefound to be generally blue-shifted by the interaction with anexternal positive charge due to stabilization of occupiedmolecular orbitals. In metal-containing derivatives, Mg-chlorin and Chl a, the atomic orbital of the central Mg atomhas been found to play an important role in electronictransition in the presence of an external charge. Due to thestrong interaction of the atomic orbital with the charge, themolecular orbital in mixing with the atomic orbital is muchstabilized by the presence of nearby positive charges andthen the transition energy to S1 state can be red-shifted orblue-shifted from that of isolated molecules depending onthe detailed location of the external charge. Furthermore, afew new transition bands have been shown to emerge as aresult of the interaction with the charge. This may lead to abroadening mechanism of absorption line shape of chloro-phyll molecules in biological environments where variousdistributions of external charges are often found. Acknowledgments. This work was supported by a researchgrant from Chungbuk National University in 2011.References

Long-Lived Electronic Coherence in Dissipative Exciton Dynamics of Light-Harvesting Complexes

The observed prevalence of oscillatory signals in the spectroscopy of biological light-harvesting complexes at ambient temperatures has led to a search for mechanisms supporting coherent transport through larger molecules in noisy environments. We demonstrate a generic mechanism supporting long-lasting electronic coherence up to 0.3 ps at a temperature of 277 K. The mechanism relies on two properties of the spectral density: (i) a large dissipative coupling to a continuum of higher-frequency vibrations required for efficient transport and (ii) a small slope of the spectral density at zero frequency.

Functionalized Nanoporous Gold Leaf Electrode Films for the Immobilization of Photosystem I

Plants and some types of bacteria demonstrate an elegant means to capitalize on the superabundance of solar energy that reaches our planet with their energy conversion process called photosynthesis. Seeking to harness Nature's optimization of this process, we have devised a biomimetic photonic energy conversion system that makes use of the photoactive protein complex Photosystem I, immobilized on the surface of nanoporous gold leaf (NPGL) electrodes, to drive a photoinduced electric current through an electrochemical cell. The intent of this study is to further the understanding of how the useful functionality of these naturally mass-produced, biological light-harvesting complexes can be integrated with nonbiological materials. Here, we show that the protein complexes retain their photonic energy conversion functionality after attachment to the nanoporous electrode surface and, further, that the additional PSI/electrode interfacial area provided by the NPGL allows for an increase in PSI-mediated electron transfer with respect to an analogous 2D system if the pores are sufficiently enlarged by dealloying. This increase of interfacial area is pertinent for other applications involving electron transfer between phases; thus, we also report on the widely accessible and scalable method by which the NPGL electrode films used in this study are fabricated and attached to glass and Au/Si supports and demonstrate their adaptability by modification with various self-assembled monolayers. Finally, we demonstrate that the magnitude of the PSI-catalyzed photocurrents provided by the NPGL electrode films is dependent upon the intensity of the light used to irradiate the electrodes.