Enumerative Discovery of Noncanonical Polypeptide Secondary Structures.

Energetically favorable local interactions can overcome the entropic cost of chain ordering and cause otherwise flexible polymers to adopt regularly repeating backbone conformations. A prominent example is the α helix present in many protein structures, which is stabilized by , + 4 hydrogen bonds between backbone peptide units. With the increased chemical diversity offered by unnatural amino acids and backbones, it has been possible to identify regularly repeating structures not present in proteins, but to date, there has been no systematic approach for identifying new polymers likely to have such structures despite their considerable potential for molecular engineering.

De novo design of proteins housing excitonically coupled chlorophyll special pairs.

Natural photosystems couple light harvesting to charge separation using a 'special pair' of chlorophyll molecules that accepts excitation energy from the antenna and initiates an electron-transfer cascade. To investigate the photophysics of special pairs independently of the complexities of native photosynthetic proteins, and as a first step toward creating synthetic photosystems for new energy conversion technologies, we designed C-symmetric proteins that hold two chlorophyll molecules in closely juxtaposed arrangements. X-ray crystallography confirmed that one designed protein binds two chlorophylls in the same orientation as native special pairs, whereas a second designed protein positions them in a previously unseen geometry.

design of energy transfer proteins housing excitonically coupled chlorophyll special pairs.

Natural photosystems couple light harvesting to charge separation using a "special pair" of chlorophyll molecules that accepts excitation energy from the antenna and initiates an electron-transfer cascade. To investigate the photophysics of special pairs independent of complexities of native photosynthetic proteins, and as a first step towards synthetic photosystems for new energy conversion technologies, we designed C-symmetric proteins that precisely position chlorophyll dimers. X-ray crystallography shows that one designed protein binds two chlorophylls in a binding orientation matching native special pairs, while a second positions them in a previously unseen geometry.

Engineering excitonically coupled dimers in an artificial protein for light harvesting via computational modeling.

In photosynthesis, pigment-protein complexes achieve outstanding photoinduced charge separation efficiencies through a set of strategies in which excited states delocalization over multiple pigments ("excitons") and charge-transfer states play key roles. These concepts, and their implementation in bioinspired artificial systems, are attracting increasing attention due to the vast potential that could be tapped by realizing efficient photochemical reactions. In particular, de novo designed proteins provide a diverse structural toolbox that can be used to manipulate the geometric and electronic properties of bound chromophore molecules.

Surviving on low-energy light comes at a price.

Two species of photosynthetic cyanobacteria can thrive in far-red light but they either become less resilient to photodamage or less energy efficient.

Dynamics of diverse coherences in primary charge separation of bacterial reaction center at 77 K revealed by wavelet analysis.

To uncover the mechanism behind the high photo-electronic conversion efficiency in natural photosynthetic complexes it is essential to trace the dynamics of electronic and vibrational quantum coherences. Here we apply wavelet analysis to two-dimensional electronic spectroscopy data for three purple bacterial reaction centers with mutations that produce drastically different rates of primary charge separation. From the frequency distribution and dynamic evolution features of the quantum beating, electronic coherence with a dephasing lifetime of ~50 fs, vibronic coherence with a lifetime of ~150 fs and vibrational/vibronic coherences with a lifetime of 450 fs are distinguished.

Dynamic Stark Effect in Two-Dimensional Spectroscopy Revealing Modulation of Ultrafast Charge Separation in Bacterial Reaction Centers by an Inherent Electric Field.

Despite extensive study, mysteries remain regarding the highly efficient ultrafast charge separation processes in photosynthetic reaction centers (RCs). In this work, transient Stark signals were found to be present in ultrafast two-dimensional electronic spectra recorded for purple bacterial RCs at 77 K. These arose from the electric field that is inherent to the intradimer charge-transfer intermediate of the bacteriochlorophyll pair (P), PP.

Complete mapping of energy transfer pathways in the plant light-harvesting complex Lhca4.

The Lhca4 antenna complex of plant Photosystem I (PSI) is characterized by extremely red-shifted and broadened absorption and emission bands from its low-energy chlorophylls (Chls). The mixing of a charge-transfer (CT) state with the excited state manifold causing these so-called red forms results in highly complicated multi-component excited energy transfer (EET) kinetics within the complex. The two-dimensional electronic spectroscopy experiments presented here reveal that EET towards the CT state occurs on three timescales: fast from the red Chls (within 1 ps), slower (5-7 ps) from the stromal side Chls, and very slow (100-200 ps) from a newly discovered 690 nm luminal trap.

Cavity-Modified Exciton Dynamics in Photosynthetic Units.

Recently, exciton-photon strong coupling has been proposed as a means to control and enhance energy transfer in ensembles of organic molecules. Here, we demonstrate that the exciton dynamics in an archetypal purple bacterial photosynthetic unit, composed of six LH2 antennas surrounding a single LH1 complex, is greatly modified by its interaction with an optical cavity. We develop a Bloch-Redfield master equation approach that accounts for the interplay between the B800 and B850 bacteriochlorophyll molecules within each LH2 antenna, as well as their interactions with the central LH1 complex.

Both electronic and vibrational coherences are involved in primary electron transfer in bacterial reaction center.

Understanding the mechanism behind the near-unity efficiency of primary electron transfer in reaction centers is essential for designing performance-enhanced artificial solar conversion systems to fulfill mankind's growing demands for energy. One of the most important challenges is distinguishing electronic and vibrational coherence and establishing their respective roles during charge separation. In this work we apply two-dimensional electronic spectroscopy to three structurally-modified reaction centers from the purple bacterium Rhodobacter sphaeroides with different primary electron transfer rates.

Vibronic Coherence in the Charge Separation Process of the Rhodobacter sphaeroides Reaction Center.

Two-dimensional electronic spectroscopy was applied to a variant of the reaction center (RC) of purple bacterium Rhodobacter sphaeroides lacking the primary acceptor ubiquinone in order to understand the ultrafast separation and transfer of charge between the bacteriochlorin cofactors. For the first time, characteristic 2D spectra were obtained for the participating excited and charge-transfer states, and the electron-transfer cascade (including two different channels, the P* and B* channels) was fully mapped. By analyzing quantum beats using 2D frequency maps, excited-state vibrational modes at 153 and 33 cm were identified.

Quantum - coherent dynamics in photosynthetic charge separation revealed by wavelet analysis.

Experimental/theoretical evidence for sustained vibration-assisted electronic (vibronic) coherence in the Photosystem II Reaction Center (PSII RC) indicates that photosynthetic solar-energy conversion might be optimized through the interplay of electronic and vibrational quantum dynamics. This evidence has been obtained by investigating the primary charge separation process in the PSII RC by two-dimensional electronic spectroscopy (2DES) and Redfield modeling of the experimental data. However, while conventional Fourier transform analysis of the 2DES data allows oscillatory signatures of vibronic coherence to be identified in the frequency domain in the form of static 2D frequency maps, the real-time evolution of the coherences is lost.

Quantum design of photosynthesis for bio-inspired solar-energy conversion.

Photosynthesis is the natural process that converts solar photons into energy-rich products that are needed to drive the biochemistry of life. Two ultrafast processes form the basis of photosynthesis: excitation energy transfer and charge separation. Under optimal conditions, every photon that is absorbed is used by the photosynthetic organism.

Achieving Exciton Delocalization in Quantum Dot Aggregates Using Organic Linker Molecules.

The design of new complex structures containing semiconductor quantum dots offers a means to create a variety of new meso-solids and molecules. The control of the coupling properties between the dots, accompanied by the energetic tunability of the dots themselves, paves the way toward the application and use of novel quantum properties. Here we present our approach to alteration of interdot coupling using organic linking molecules in a system of covalently bonded, aggregated quantum dots.

Exciton-vibrational resonance and dynamics of charge separation in the photosystem II reaction center.

The dynamics of charge separation in the photosystem II reaction center (PSII-RC) in the presence of intramolecular vibrations with their frequency matching the energy gap between the exciton state acting as the primary electron donor and the first charge-transfer (CT) state are investigated. A reduced PSII-RC 4-state model explicitly including a CT state is analyzed within Redfield relaxation theory in the multidimensional exciton-vibrational (vibronic) basis. This model is used to study coherent energy/electron transfers and their spectral signatures obtained by two-dimensional electronic spectroscopy (2DES).

Competing charge transfer pathways at the photosystem II-electrode interface.

The integration of the water-oxidation enzyme photosystem II (PSII) into electrodes allows the electrons extracted from water oxidation to be harnessed for enzyme characterization and to drive novel endergonic reactions. However, PSII continues to underperform in integrated photoelectrochemical systems despite extensive optimization efforts. Here we carried out protein-film photoelectrochemistry using spinach and Thermosynechococcus elongatus PSII, and we identified a competing charge transfer pathway at the enzyme-electrode interface that short-circuits the known water-oxidation pathway.

Mixing of exciton and charge-transfer states in light-harvesting complex Lhca4.

Lhca4 is one of the peripheral antennae of higher plant photosystem I and it is characterized by the presence of chlorophyll a with absorption and emission bands around 30 nm red-shifted compared to those of the other chlorophylls associated with plant complexes. In this work we have investigated the origin of this red shift by using the recent structure of Lhca4 (Qin et al., Science, 2015, 348, 989) to build an exciton model that includes a charge-transfer (CT) state mixed with the excited-state manifold.

Dark States in the Light-Harvesting complex 2 Revealed by Two-dimensional Electronic Spectroscopy.

Energy transfer and trapping in the light harvesting antennae of purple photosynthetic bacteria is an ultrafast process, which occurs with a quantum efficiency close to unity. However the mechanisms behind this process have not yet been fully understood. Recently it was proposed that low-lying energy dark states, such as charge transfer states and polaron pairs, play an important role in the dynamics and directionality of energy transfer.

How exciton-vibrational coherences control charge separation in the photosystem II reaction center.

In photosynthesis absorbed sun light produces collective excitations (excitons) that form a coherent superposition of electronic and vibrational states of the individual pigments. Two-dimensional (2D) electronic spectroscopy allows a visualization of how these coherences are involved in the primary processes of energy and charge transfer. Based on quantitative modeling we identify the exciton-vibrational coherences observed in 2D photon echo of the photosystem II reaction center (PSII-RC).

Identification of common motifs in the regulation of light harvesting: The case of cyanobacteria IsiA.

When cyanobacteria are grown under iron-limited or other oxidative stress conditions the iron stress inducible pigment-protein IsiA is synthesized in variable amounts. IsiA accumulates in aggregates inside the photosynthetic membrane that strongly dissipate chlorophyll excited state energy. In this paper we applied Stark fluorescence (SF) spectroscopy at 77K to IsiA aggregates to gain insight into the nature of the emitting and energy dissipating state(s).

Quantum Coherence in Photosynthesis for Efficient Solar Energy Conversion.

The crucial step in the conversion of solar to chemical energy in Photosynthesis takes place in the reaction center where the absorbed excitation energy is converted into a stable charge separated state by ultrafast electron transfer events. However, the fundamental mechanism responsible for the near unity quantum efficiency of this process is unknown. Here we elucidate the role of coherence in determining the efficiency of charge separation in the plant photosystem II reaction centre (PSII RC) by comprehensively combining experiment (two-dimensional electronic spectroscopy) and theory (Redfield theory).

The nature of coherences in the B820 bacteriochlorophyll dimer revealed by two-dimensional electronic spectroscopy.

Light-harvesting in photosynthesis is determined by the excitonic interactions in disordered antennae and the coupling of collective electronic excitations to fast nuclear motions, producing efficient energy transfer with a complicated interplay between exciton and vibrational coherences. Two-dimensional electronic spectroscopy (2DES) is a powerful tool to study the presence of these coherences in photosynthetic complexes. However, the unambiguous assignment of the nature of the observed coherences is still under debate.

Mixed exciton-charge-transfer states in photosystem II: Stark spectroscopy on site-directed mutants.

We investigated the electronic structure of the photosystem II reaction center (PSII RC) in relation to the light-induced charge separation process using Stark spectroscopy on a series of site-directed PSII RC mutants from the cyanobacterium Synechocystis sp. PCC 6803. The site-directed mutations modify the protein environment of the cofactors involved in charge separation (P(D1), P(D2), Chl(D1), and Phe(D1)).

Identification of two emitting sites in the dissipative state of the major light harvesting antenna.

In order to cope with the deleterious effects of excess light, photosynthetic organisms have developed remarkable strategies where the excess energy is dissipated as heat by the antenna system. In higher plants one main player in the process is the major light harvesting antenna of Photosystem II (PSII), LHCII. In this paper we applied Stark fluorescence spectroscopy to LHCII in different quenching states to investigate the possible contribution of charge-transfer states to the quenching.

Investigating the early stages of photosystem II assembly in Synechocystis sp. PCC 6803: isolation of CP47 and CP43 complexes.

Biochemical characterization of intermediates involved in the assembly of the oxygen-evolving Photosystem II (PSII) complex is hampered by their low abundance in the membrane. Using the cyanobacterium Synechocystis sp. PCC 6803, we describe here the isolation of the CP47 and CP43 subunits, which, during biogenesis, attach to a reaction center assembly complex containing D1, D2, and cytochrome b(559), with CP47 binding first.