Elisabetta Collini

Coherently wired light-harvesting in photosynthetic marine algae at ambient temperature

Photosynthesis makes use of sunlight to convert carbon dioxide into useful biomass and is vital for life on Earth. Crucial components for the photosynthetic process are antenna proteins, which absorb light and transmit the resultant excitation energy between molecules to a reaction centre. The efficiency of these electronic energy transfers has inspired much work on antenna proteins isolated from photosynthetic organisms to uncover the basic mechanisms at play. Intriguingly, recent work has documented that light-absorbing molecules in some photosynthetic proteins capture and transfer energy according to quantum-mechanical probability laws instead of classical laws at temperatures up to 180 K. This contrasts with the long-held view that long-range quantum coherence between molecules cannot be sustained in complex biological systems, even at low temperatures. Here we present two-dimensional photon echo spectroscopy measurements on two evolutionarily related light-harvesting proteins isolated from marine cryptophyte algae, which reveal exceptionally long-lasting excitation oscillations with distinct correlations and anti-correlations even at ambient temperature. These observations provide compelling evidence for quantum-coherent sharing of electronic excitation across the 5-nm-wide proteins under biologically relevant conditions, suggesting that distant molecules within the photosynthetic proteins are ‘wired’ together by quantum coherence for more efficient light-harvesting in cryptophyte marine algae.

Coherent Intrachain Energy Migration in a Conjugated Polymer at Room Temperature

The intermediate coupling regime for electronic energy transfer is of particular interest because excitation moves in space, as in a classical hopping mechanism, but quantum phase information is conserved. We conducted an ultrafast polarization experiment specifically designed to observe quantum coherent dynamics in this regime. Conjugated polymer samples with different chain conformations were examined as model multichromophoric systems. The data, recorded at room temperature, reveal coherent intrachain (but not interchain) electronic energy transfer. Our results suggest that quantum transport effects occur at room temperature when chemical donor-acceptor bonds help to correlate dephasing perturbations.

Assessment of Water-Soluble π-Extended Squaraines as One- and Two-Photon Singlet Oxygen Photosensitizers: Design, Synthesis, and Characterization

Singlet oxygen sensitization by organic molecules is a topic of major interest in the development of both efficient photodynamic therapy (PDT) and aerobic oxidations under complete green chemistry conditions. We report on the design, synthesis, biology, and complete spectroscopic characterization (vis-NIR linear and two-photon absorption spectroscopy, singlet oxygen generation efficiencies for both one- and two-photon excitation, electrochemistry, intrinsic dark toxicity, cellular uptake, and subcellular localization) of three classes of innovative singlet oxygen sensitizers pertaining to the family of symmetric squaraine derivatives originating from pi-excessive heterocycles. The main advantage of pi-extended squaraine photosensitizers over the large number of other known photosensitizers is their exceedingly strong two-photon absorption enabling, together with sizable singlet oxygen sensitization capabilities, for their use at the clinical application relevant wavelength of 806 nm. We finally show encouraging results about the dark toxicity and cellular uptake capabilities of water-soluble squaraine photosensitizers, opening the way for clinical small animal PDT trials.

Spectroscopic signatures of quantum-coherent energy transfer

One of the most surprising and significant advances in the study of the photosynthetic light-harvesting process is the discovery that the electronic energy transfer might involve long-lived electronic coherences, under physiologically relevant conditions. This means that the transfer of energy among different chromophores does not follow the expected classical incoherent hopping mechanism, but that quantum-mechanical laws can steer the migration of energy. The implications of such a quantum transport regime, although currently under debate, might have a tremendous impact on our way of thinking about natural and artificial light-harvesting. Central to these discoveries has been the development of new ultrafast spectroscopic techniques, in particular two-dimensional electronic spectroscopy, which is now the primary tool to obtain clear and definitive experimental proof of such effects. This review aims to provide an overview of the experimental techniques developed with the purpose of attaining a more detailed picture of the coherent and incoherent quantum dynamics relevant to energy transfer processes, not limited to the two-dimensional electronic spectroscopy. With the idea of summarizing the experimental and theoretical basic notions necessary to introduce the field, the connection between experimental observables and coherence dynamics will be analysed in detail for each technique, highlighting how electronic coherences could be manifested in different experimental signatures. Similarities and differences among coherent signals as well as advantages and disadvantages of each approach will be critically discussed. Current opinions and debated issues will be emphasised and some possible future directions to address still open questions will be suggested.

Large third-order nonlinear optical response of porphyrin J-aggregates oriented in self-assembled thin films

The preparation and characterization of a self-assembled material showing a high nonlinear response and good photostability to ultrashort laser pulses is presented. The material is built by alternate deposition of tetrakis(4-sulfonatophenyl)porphyrin diacid (H4TPPS2−) and poly(diallyldimethylammonium chloride) (PDDA) forming electrostatically self-assembled multilayers (ESAMs). UV-visible absorption and emission experiments show that in this matrix H4TPPS2− is present mainly in its J-aggregated form. Furthermore, linear dichroism experiments on a 3 bilayer film show a preferential alignment of the porphyrin aggregate with the J-band transition dipole moment parallel to the film surface. The two photon absorption (TPA) properties of these films are investigated with the Z-scan technique at 806 nm, employing 130 fs pulses. The samples exhibit strong nonlinearities with a very large two-photon absorption coefficient βTPA of 50 cm GW−1. The origin of this large response is investigated. It has been already demonstrated that aggregation enhances the molecular TPA cross section of H4TPPS2− from 30 to 1000 GM in water solution thanks to cooperative effects. In a 20 bilayer film a further increase by a factor of 1.7 is observed and explained in terms of preferential alignment of J-aggregates in the multilayers.

Effective two-photon absorption cross section of heteroaromatic quadrupolar dyes: dependence on measurement technique and laser pulse characteristics.

The linear and nonlinear optical properties of the heteroaromatic push-pull-push two-photon absorbing dye N-methyl-2,5-bis[1-(N-methylpyrid-4-yl)ethen-2-yl]-pyrrole ditriflate (PEPEP) are reported. The determination of the two-photon absorption (TPA) cross-section spectrum has been performed with different techniques: femtosecond TPA-white light continuum probe experiments, two-photon-induced fluorescence, and open aperture Z-scan measurements using both nanosecond and femtosecond laser pulses. The measured TPA cross sections and their wavelength dispersion show a marked dependence on the parameters of the laser pulses and on the measurement technique employed. These properties are discussed in terms of the different microscopic mechanisms that can contribute to the multiphoton absorption processes, with different weight depending on the measurement conditions and on the photophysical parameters of the dye.

Single-residue insertion switches the quaternary structure and exciton states of cryptophyte light-harvesting proteins.

Significance There is intense interest in determining whether coherent quantum processes play a nontrivial role in biology. This interest was sparked by the discovery of long-lived oscillations in 2D electronic spectra of photosynthetic proteins, including the phycobiliproteins (PBPs) from cryptophyte algae. Using X-ray crystallography, we show that cryptophyte PBPs adopt one of two quaternary structures, open or closed. The key feature of the closed form is the juxtaposition of two central chromophores resulting in excitonic coupling. The switch between forms is ascribed to the insertion of a single amino acid in the open-form proteins. Thus, PBP quaternary structure controls excitonic coupling and the mechanism of light harvesting. Comparing organisms with these two distinct proteins will reveal the role of quantum coherence in photosynthesis. Observation of coherent oscillations in the 2D electronic spectra (2D ES) of photosynthetic proteins has led researchers to ask whether nontrivial quantum phenomena are biologically significant. Coherent oscillations have been reported for the soluble light-harvesting phycobiliprotein (PBP) antenna isolated from cryptophyte algae. To probe the link between spectral properties and protein structure, we determined crystal structures of three PBP light-harvesting complexes isolated from different species. Each PBP is a dimer of αβ subunits in which the structure of the αβ monomer is conserved. However, we discovered two dramatically distinct quaternary conformations, one of which is specific to the genus Hemiselmis. Because of steric effects emerging from the insertion of a single amino acid, the two αβ monomers are rotated by ∼73° to an “open” configuration in contrast to the “closed” configuration of other cryptophyte PBPs. This structural change is significant for the light-harvesting function because it disrupts the strong excitonic coupling between two central chromophores in the closed form. The 2D ES show marked cross-peak oscillations assigned to electronic and vibrational coherences in the closed-form PC645. However, such features appear to be reduced, or perhaps absent, in the open structures. Thus cryptophytes have evolved a structural switch controlled by an amino acid insertion to modulate excitonic interactions and therefore the mechanisms used for light harvesting.

Time-frequency methods for coherent spectroscopy

Time-frequency decomposition techniques, borrowed from the signal-processing field, have been adapted and applied to the analysis of 2D oscillating signals. While the Fourier-analysis techniques available so far are able to interpret the information content of the oscillating signal only in terms of its frequency components, the time-frequency transforms (TFT) proposed in this work can instead provide simultaneously frequency and time resolution, unveiling the dynamics of the relevant beating components, and supplying a valuable help in their interpretation. In order to fully exploit the potentiality of this method, several TFTs have been tested in the analysis of sample 2D data. Possible artifacts and sources of misinterpretation have been identified and discussed.

Molecular decision trees realized by ultrafast electronic spectroscopy

Significance One possible way to reduce the physical dimensions of a computing node is to instruct a molecule to evaluate a complicated logic function. This is even more so if several such functions are processed in parallel. The interaction between light and matter is a suitable route because it is bilinear, depending on both the properties of the laser and of the molecule; the outcome depends on the initial state of the molecule and there can be more than one distinct path leading to the readout signal. Two-dimensional photon spectroscopy is shown to have four paths originating from each interaction, thereby enabling, as shown in SI Text, quaternary logic. In the main text, we discuss the simpler case of binary logic. The outcome of a light–matter interaction depends on both the state of matter and the state of light. It is thus a natural setting for implementing bilinear classical logic. A description of the state of a time-varying system requires measuring an (ideally complete) set of time-dependent observables. Typically, this is prohibitive, but in weak-field spectroscopy we can move toward this goal because only a finite number of levels are accessible. Recent progress in nonlinear spectroscopies means that nontrivial measurements can be implemented and thereby give rise to interesting logic schemes where the outputs are functions of the observables. Lie algebra offers a natural tool for generating the outcome of the bilinear light–matter interaction. We show how to synthesize these ideas by explicitly discussing three-photon spectroscopy of a bichromophoric molecule for which there are four accessible states. Switching logic would use the on–off occupancies of these four states as outcomes. Here, we explore the use of all 16 observables that define the time-evolving state of the bichromophoric system. The bilinear laser–system interaction with the three pulses of the setup of a 2D photon echo spectroscopy experiment can be used to generate a rich parallel logic that corresponds to the implementation of a molecular decision tree. Our simulations allow relaxation by weak coupling to the environment, which adds to the complexity of the logic operations.

Photophysics and Dynamics of Surface Plasmon Polaritons-Mediated Energy Transfer in the Presence of an Applied Electric Field

The possibility to transfer energy between molecular excitons across a metal film up to 150 nm thick represents a very attractive solution to control and improve the performances of thin optoeletronic devices. This process involves the presence of coupled surface plasmon polaritons (SPPs) at the two dielectric-metal interfaces, capable of mediating the interactions between donor and acceptor, located on opposite sides of the metal film. In this Article, the photophysics and the dynamics of an efficient SPP-mediated energy transfer between a suitable dye and a conjugated polymer is characterized by means of steady-state and time-resolved photoluminescence techniques. The process is studied in model multilayer structures (donor/metal/acceptor) as well as in electrically pumped heterostructures (donor/metal cathode/acceptor/anode), to verify the effects of applied electric fields on the efficiency and the dynamics of SPP-mediated energy transfer. A striking enhancement of the overall luminescence was recorded in a particular range of applied bias, suggesting the presence of cooperative effects between optical and electrical stimulations.