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Diatoms are a major group of algae, responsible for a quarter of the global primary production on our planet. Their adaptation to marine environments is ensured by their light-harvesting antenna - the fucoxanthin-chlorophyll protein (FCP) complex, which absorbs strongly in the blue-green spectral region. Although these essential proteins have been the subject of many studies, for a long time their comprehensive description was not possible in the absence of structural data. Last year, the 3D structures of several FCP complexes were revealed. The structure of an FCP dimer was resolved by crystallography for the pennate diatom Phaeodactylum tricornutum [W. Wang et al., Science, 2019, 363, 6427] and the structure of the PSII supercomplex from the centric diatom Chaetoceros gracilis, containing several FCPs, was obtained by electron microscopy [X. Pi et al., Science, 2019, 365, 6452; R. Nagao et al., Nat. Plants, 2019, 5, 890]. In this Perspective article, we evaluate how precisely these structures may account for previously published ultrafast spectroscopy results, describing the excitation energy transfer in the FCP from another centric diatom Cyclotella meneghiniana. Surprisingly, we find that the published FCP structures cannot explain several observations obtained from ultrafast spectroscopy. Using the available structures, and results from electron microscopy, we construct a trimer-based FCP model for Cyclotella meneghiniana, consistent with ultrafast experimental data. As a whole, our observations suggest that the structures from the proteins belonging to the FCP family display larger variations than the equivalent LHC proteins in plants, which may reflect species-specific adaptations or original strategies for adapting to rapidly changing marine environments.

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Detailed studies of the excitation dynamics in photosynthetic pigment-proteins require an application of a wide range of spectroscopic methods. From the later part of the previous century, pump-probe and time-resolved fluorescence spectroscopy provided an impressive amount of information. Being simple to grasp, these methods are well-understood and widely used by the photosynthesis research community. In the last fifteen years, two-dimensional (2D) spectroscopy was developed. It has significant advantages over other methods, in particular higher temporal resolution available and higher signal-to-noise ratio. Even though it provides considerable opportunities in research, both its experimental realization and theoretical description are rather complicated, making it somewhat difficult to understand and apply. This makes an unfortunate gap in the community, with spectroscopy experts being able to use the technique, but sometimes lacking the relevant biological knowledge, while biologists having that knowledge are dubious about 2D spectroscopy due to the complexity of the approach. This publication is an attempt to fill this gap by providing an accessible introduction to the concepts, principles and possible applications of the 2D spectroscopy, aimed at the biologically trained members of the photosynthesis research community.

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The photosynthetic apparatus of green plants is well known for its extremely high efficiency that allows them to operate under dim light conditions. On the other hand, intense sunlight may result in overexcitation of the light-harvesting antenna and the formation of reactive compounds capable of 'burning out' the whole photosynthetic unit. Non-photochemical quenching is a self-regulatory mechanism utilized by green plants on a molecular level that allows them to safely dissipate the detrimental excess excitation energy as heat. Although it is believed to take place in the plant's major light-harvesting complexes (LHC) II, there is still no consensus regarding its molecular nature. To get more insight into its physical origin, we performed high-resolution time-resolved fluorescence measurements of LHCII trimers and their aggregates across a wide temperature range. Based on simulations of the excitation energy transfer in the LHCII aggregate, we associate the red-emitting state, having fluorescence maximum at ∼700 nm, with the partial mixing of excitonic and chlorophyll-chlorophyll charge transfer states. On the other hand, the quenched state has a totally different nature and is related to the incoherent excitation transfer to the short-lived carotenoid excited states. Our results also show that the required level of photoprotection in vivo can be achieved by a very subtle change in the number of LHCIIs switched to the quenched state.

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Energy transfer processes and coherent phenomena in the fucoxanthin-chlorophyll protein complex, which is responsible for the light harvesting function in marine algae diatoms, were investigated at 77 K by using two-dimensional electronic spectroscopy. Experiments performed on femtosecond and picosecond timescales led to separation of spectral dynamics, witnessing evolutions of coherence and population states of the system in the spectral region of Qy transitions of chlorophylls a and c. Analysis of the coherence dynamics allowed us to identify chlorophyll (Chl) a and fucoxanthin intramolecular vibrations dominating over the first few picoseconds. Closer inspection of the spectral region of the Qy transition of Chl c revealed previously not identified, mutually non-interacting chlorophyll c states participating in femtosecond or picosecond energy transfer to the Chl a molecules. Consideration of separated coherent and incoherent dynamics allowed us to hypothesize the vibrations-assisted coherent energy transfer between Chl c and Chl a and the overall spatial arrangement of chlorophyll molecules.

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Fucoxanthin-chlorophyll protein (FCP) is the key molecular complex performing the light-harvesting function in diatoms, which, being a major group of algae, are responsible for up to one quarter of the total primary production on Earth. These photosynthetic organisms contain an unusually large amount of the carotenoid fucoxanthin, which absorbs the light in the blue-green spectral region and transfers the captured excitation energy to the FCP-bound chlorophylls. Due to the large number of fucoxanthins, the excitation energy transfer cascades in these complexes are particularly tangled. In this work we present the two-color two-dimensional electronic spectroscopy experiments on FCP. Analysis of the data using the modified decay associated spectra permits a detailed mapping of the excitation frequency dependent energy transfer flow with a femtosecond time resolution.

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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. In this paper we apply 2DES to an excitonically coupled bacteriochlorophyll dimer, the B820 subunit of the light harvesting complex 1 (LH1-RC) of R. rubrum G9. Fourier analysis of the measured kinetics and modeling of the spectral responses in a complete basis of electronic and vibrational states allow us to distinguish between pure vibrational, mixed exciton-vibrational (vibronic), and predominantly exciton coherences. The mixed coherences have been found in a wide range of oscillation frequencies, whereas exciton coherences give the biggest contributions for the frequencies in the 400-550 cm(-1) range, corresponding to the exciton splitting energy of the B820 dimer. Significant exciton coherences are also present at higher frequencies, i.e., up to 800 cm(-1), which are determined by realizations of the disorder with a large energy gap between the two pigments (which increases the apparent value of the exciton splitting). Although the B820 dimer is a model system, the approach presented here represents a basis for further analyses of more complicated systems, providing a tool for studying the interplay between electronic and vibrational coherences in disordered photosynthetic antennae and reaction centres.

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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). We reveal the presence of electronic coherence between excitons as well as between exciton and charge transfer states which we argue to be maintained by vibrational modes. Furthermore, we present evidence for the strong correlation between the degree of electronic coherence and efficient and ultrafast charge separation. We propose that this coherent mechanism will inspire the development of new energy technologies.

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Chlorosomes are light-harvesting antennae that enable exceptionally efficient light energy capture and excitation transfer. They are found in certain photosynthetic bacteria, some of which live in extremely low-light environments. In this work, chlorosomes from the green sulfur bacterium Chlorobaculum tepidum were studied by coherent electronic two-dimensional (2D) spectroscopy. Previously uncharacterized ultrafast energy transfer dynamics were followed, appearing as evolution of the 2D spectral line-shape during the first 200 fs after excitation. Observed initial energy flow through the chlorosome is well explained by effective exciton diffusion on a sub-100 fs time scale, which assures efficiency and robustness of the process. The ultrafast incoherent diffusion-like behavior of the excitons points to a disordered energy landscape in the chlorosome, which leads to a rapid loss of excitonic coherences between its structural subunits. This disorder prevents observation of excitonic coherences in the experimental data and implies that the chlorosome as a whole does not function as a coherent light-harvester.

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In many potential applications of two-dimensional (2D) electronic spectroscopy the excitation energies per pulse are strictly limited, while the samples are strongly scattering. We demonstrate a technique, based on double-modulation of incident laser beams with mechanical choppers, which can be implemented in almost any non-collinear four wave mixing scheme including 2D spectroscopy setup. The technique virtually eliminates artifacts or "ghost" signals in 2D spectra, which arise due to scattering and accumulation of long-lived species. To illustrate the advantages of the technique, we show a comparison of porphyrin J-aggregate 2D spectra obtained with different methods following by discussion.

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The femto- and picosecond time resolved spectroscopy of (eta(6)-cis-stilbene)Cr(CO)(3) provides evidence for three optically accessible excited states one leading to cis-trans isomerisation of the coordinated stilbene ligand and another which results in a slow release of CO.

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Energy transfer properties of novel coumarin-perylene bisimide dendrimer are studied by means of steady state and time-resolved UV/vis spectroscopy. At low donor excitation density fast (transfer rate approximately 10 ps(-1)) and efficient (quantum yield approximately 99.5%) donor-acceptor energy transfer is observed. The random distributions of donor-acceptor orientations and distances result in nonexponential energy transfer kinetics. The energy transfer remains independent of excitation density up to densities corresponding to one absorbed photon per 10 dendrimer molecules. At higher excitation densities the transfer rate is found to increase due to excitation of multiple donors per dendrimer. Control of the donor-acceptor energy transfer rate is achieved by pre-excitation of the acceptor and monitored by prepump-pump-probe experiments, which show that the energy transfer rate can be decreased by a factor of 2. The relative orientations of transition dipole moments in the donor and acceptor molecules are found to be one of the key factors determining the energy transfer dynamics at high excitation densities.

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The synthesis and characterisation of a novel coumarin donor-perylene bisimide acceptor light-harvesting system is reported, in which an energy-transfer efficiency of >99% is achieved. Comparison of the excited-state properties of the donor-acceptor system with model compounds revealed that although the photophysical properties of the perylene bisimide acceptor unit are affected considerably by the nature of the substituent at the imide positions and the solvent employed, through-bond interaction between the donor and acceptor units is negligible. Energy transfer in the present system can be described as occurring via a through-space energy-transfer mechanism. Careful consideration of the redox properties of the donor relative to the acceptor units allows for avoidance of potentially deleterious excited-state electron-transfer processes.