Exploring the mechanism(s) of energy dissipation in the light harvesting complex of the photosynthetic algae Cyclotella meneghiniana

AbstractPhotosynthetic organisms have developed vital strategies which allow them to switch from a light-harvesting to an energy dissipative state at the level of the antenna system in order to survive the detrimental effects of excess light illumination. These mechanisms are particularly relevant in diatoms, which grow in highly fluctuating light environments and thus require fast and strong response to changing light conditions. We performed transient absorption spectroscopy on FCPa, the main light-harvesting antenna from the diatom Cyclotella meneghiniana, in the unquenched and quenched state. Our results show that in quenched FCPa two quenching channels are active and are characterized by differing rate constants and distinct spectroscopic signatures. One channel is associated with a faster quenching rate (16ns−1) and virtually no difference in spectral shape compared to the bulk unquenched chlorophylls, while a second channel is associated with a slower quenching rate (2.7ns−1) and exhibits an increased population of red-emitting states. We discuss the origin of the two processes in the context of the models proposed for the regulation of photosynthetic light-harvesting. This article is part of a Special Issue entitled: Photosynthesis Research for Sustainability: Keys to Produce Clean Energy

Reduced Intrinsic Non-Radiative Losses Allow Room-Temperature Triplet Emission from Purely Organic Emitters

Persistent luminescence from triplet excitons in organic molecules is rare, as fast non-radiative deactivation typically dominates over radiative transitions. This work demonstrates that the substitution of a hydrogen atom in a derivative of phenanthroimidazole with an N-phenyl ring can substantially stabilize the excited state. This stabilization converts an organic material without phosphorescence emission into a molecular system exhibiting efficient and ultralong afterglow phosphorescence at room temperature. Results from systematic photophysical investigations, kinetic modeling, excited-state dynamic modeling, and single-crystal structure analysis identify that the long-lived triplets originate from a reduction of intrinsic non-radiative molecular relaxations. Further modification of the N-phenyl ring with halogen atoms affects the afterglow lifetime and quantum yield. As a proof-of-concept, an anticounterfeiting device is demonstrated with a time-dependent Morse code feature for data encryption based on these emitters. A fundamental design principle is outlined to achieve long-lived and emissive triplet states by suppressing intrinsic non-radiative relaxations in the form of molecular vibrations or rotations

The role of exciton delocalization in the major photosynthetic light-harvesting antenna of plants

In the major peripheral plant light-harvesting complex LHCII, excitation energy is transferred between chlorophylls along an energetic cascade before it is transmitted further into the photosynthetic assembly to be converted into chemical energy. The efficiency of these energy transfer processes involves a complicated interplay of pigment-protein structural reorganization and protein dynamic disorder, and the system must stay robust within the fluctuating protein environment. The final, lowest energy site has been proposed to exist within a trimeric excitonically coupled chlorophyll (Chl) cluster, comprising Chls a610-a611-a612. We studied an LHCII monomer with a site-specific mutation resulting in the loss of Chls a611and a612, and find that this mutant exhibits two predominant overlapping fluorescence bands. From a combination of bulk measurements, single-molecule fluorescence characterization, and modeling, we propose the two fluorescence bands originate from differing conditions of exciton delocalization and localization realized in the mutant. Disruption of the excitonically coupled terminal emitter Chl trimer results in an increased sensitivity of the excited state energy landscape to the disorder induced by the protein conformations. Consequently, the mutant demonstrates a loss of energy transfer efficiency. On the contrary, in the wildtype complex, the strong resonance coupling and correspondingly high degree of excitation delocalization within the Chls a610- a611-a612 cluster dampens the influence of the environment and ensures optimal communication with neighboring pigments. These results indicate that the terminal emitter trimer is thus an essential design principle for maintaining the efficient light-harvesting function of LHCII in the presence of protein disorder.VU University and by an Advanced Investigator grant from the European Research Council (No. 267333, PHOTPROT). Nederlandse Organisatie voor Wetenschappelijk Onderzoek, Council of Chemical Sciences (NWO-CW) via a TOP-grant (700.58.305), and by the EU FP7 project PAPETS (GA 323901). Netherlands Royal Academy of Sciences (KNAW).Earth and Life Sciences Council of the NWO (NWO-ALW).Consolidator Investigator grant from the European Research Council (No. 281341 ASAP).Czech Science Foundation (GACR, No. 14-25752S) and an NWO visitor grant 040.11.423 and grant 040.11.428.http://www.cell.combiophysj2016-03-31hb201

Oxidative Two-State Photoreactivity of a Manganese(IV) Complex using NIR Light

Highly reducing or oxidizing photocatalysts are a fundamental challenge in the field of inorganic and organic photochemistry. Only a few transition metal complexes with earth-abundant metal ions have so far advanced to excited state oxidants, including chromium, iron and cobalt. All these photocatalysts require high energy light for excitation and their oxidizing power has not been fully exploited due to significant energy dissipation before reaching the photoactive state. Herein we demonstrate that the complex [Mn(dgpy)2]4+ based on earth-abundant manganese can be excited with low-energy NIR light (850 nm, 1.46 eV) to yield a luminescent mixed 2LMCT/2MC excited state (1435 nm, 0.86 eV) with a lifetime of 1.6 ns. The dissipated energy amounts to 0.60 eV. In spite of this energy loss, *[Mn(dgpy)2]4+ with its excited state redox potential Ered* of 1.80 V vs SCE outcompetes the strongest reported precious metal photooxidant (iridium(III)). *[Mn(dgpy)2]4+ oxidizes naphthalene (Eox 1.31 1.54 V vs. SCE) to its radical cation giving the manganese(III) complex [Mn(dgpy)2]3+ in a clean outer-sphere electron transfer process. Unexpectedly, mesitylene, toluene, benzene and nitriles with even extremely high oxidation potentials up to Eox = 2.4 V provoke the [Mn(dgpy)2]4+/3+ reduction under photolysis. A higher energy short-lived 4LMCT excited state with a lifetime of 0.78 ps is made responsible for these demanding oxidations, which proceed by static rather than dynamic quenching. This dual excited state reactivity from 2LMCT/2MC and 4LMCT states is linked to the 4LMCT 2LMCT/2MC intersystem crossing process. These unique findings demonstrate how the design of manganese complexes (i) expands the absorption cross section to 400 850 nm, (ii) increases the 2LMCT/2MC state lifetime to the nanosecond range allowing luminescence and classical dynamic photoredox processes and (iii) enables non-classical static quenching of an extremely oxidizing 4LMCT excited state by the solvent. This conceptually novel approach of static quenching by the solvent minimizes free energy losses, harnesses the full photooxidizing power and thus allows even oxidation of nitriles and benzene using earth-abundant elements and low-energy light

In Situ Visualization and Quantification of Electrical Self‐Heating in Conjugated Polymer Diodes Using Raman Spectroscopy

Self-heating in organic electronics can lead to anomalous electrical performance and even accelerated degradation. However, in the case of disordered organic semiconductors, self-heating effects are difficult to quantify using electrical techniques alone due to complex transport properties. Therefore, more direct methods are needed to monitor the impact of self-heating on device performance. Here, self-heating in poly[2,6-(4,4-bis-(2-ethylhexyl)-4H-cyclopenta [2,1-b;3,4-b′] dithiophene)-alt-4,7(2,1,3-benzothiadiazole)] (PCPDTBT) diodes is visualized using Raman spectroscopy, and thermal effects due to self-heating are quantified by exploiting temperature-dependent shifts in the polymer vibrational modes. The temperature increases due to self-heating are quantified by correlating the Raman shifts observed in electrically biased diodes with temperature-dependent Raman measurements. Temperature elevations up to 75 K are demonstrated in the PCPDTBT diodes at moderate power of about 2.6–3.3 W cm−2. Numerical modeling rationalizes the significant role of Joule and recombination heating on the diode current–voltage characteristics. This work demonstrates a facile approach for in situ monitoring of self-heating in organic semiconductors for a range of applications, from fundamental transport studies to thermal management in devices

Evidence for coherent mixing of excited and charge-transfer states in the major plant light-harvesting antenna, LHCII

LHCII, the major light harvesting antenna from plants, plays a dual role in photosynthesis. In low light it is a light-harvester, while in high light it is a quencher that protects the organism from photodamage. The switching mechanism between these two orthogonal conditions is mediated by protein dynamic disorder and photoprotective energy dissipation. The latter in particular is thought to occur in part via spectroscopically 'dark' states. We searched for such states in LHCII trimers from spinach, at both room temperature and at 77 K. Using 2D electronic spectroscopy, we explored coherent interactions between chlorophylls absorbing on the low-energy side of LHCII, which is the region that is responsible for both light-harvesting and photoprotection. 2D beating frequency maps allow us to identify four frequencies with strong excitonic character. In particular, our results show the presence of a low-lying state that is coupled to a low-energy excitonic state. We assign this to a mixed excitonic-charge transfer state involving the state with charge separation within the Chl a603-b609 heterodimer, borrowing some dipole strength from the Chl a602-a603 excited states. Such a state may play a role in photoprotection, in conjunction with specific and environmentally controlled realizations of protein dynamic disorder. Our identification and assignment of the coherences observed in the 2D frequency maps suggests that the structure of exciton states as well as a mixing of the excited and charge-transfer states is affected by coupling of these states to resonant vibrations in LHCII

Exploring the mechanism(s) of energy dissipation in the light harvesting complex of the photosynthetic algae Cyclotella meneghiniana ☆

Photosynthetic organisms have developed vital strategies which allow them to switch from a light-harvesting to an energy dissipative state at the level of the antenna system in order to survive the detrimental effects of excess light illumination. These mechanisms are particularly relevant in diatoms, which grow in highly fluctuating light environments and thus require fast and strong response to changing light conditions. We performed transient absorption spectroscopy on FCPa, the main light-harvesting antenna from the diatom Cyclotella meneghiniana, in the unquenched and quenched state. Our results show that in quenched FCPa two quenching channels are active and are characterized by differing rate constants and distinct spectroscopic signatures. One channel is associated with a faster quenching rate (16 ns ) and virtually no difference in spectral shape compared to the bulk unquenched chlorophylls, while a second channel is associated with a slower quenching rate (2.7 ns ) and exhibits an increased population of red-emitting states. We discuss the origin of the two processes in the context of the models proposed for the regulation of photosynthetic light-harvesting. This article is part of a Special Issue entitled: Photosynthesis Research for Sustainability: Keys to Produce Clean Energy

Energy dissipation mechanisms in the FCPb light-harvesting complex of the diatom Cyclotella meneghiniana

Transient absorption spectroscopy has been applied to investigate the energy dissipation mechanisms in the nonameric fucoxanthin-chlorophyll-a,c-binding protein FCPb of the centric diatom Cyclotella meneghiniana. FCPb complexes in their unquenched state were compared with those in two types of quenching environments, namely aggregation-induced quenching by detergent removal, and clustering via incorporation into liposomes. Applying global and target analysis, in combination with a fluorescence lifetime study and annihilation calculations, we were able to resolve two quenching channels in FCPb that involve chlorophyll-a pigments for FCPb exposed to both quenching environments. The fast quenching channel operates on a timescale of tens of picoseconds and exhibits similar spectral signatures as the unquenched state. The slower quenching channel operates on a timescale of tens to hundreds of picoseconds, depending on the degree of quenching, and is characterized by enhanced population of low-energy states between 680 and 710 nm. The results indicate that FCPb is, in principle, able to function as a dissipater of excess energy and can do this in vitro even more efficiently than the homologous FCPa complex, the sole complex involved in fast photoprotection in these organisms. This indicates that when a complex displays photoprotection-related spectral signatures in vitro it does not imply that the complex participates in photoprotection in vivo. We suggest that FCPa is favored over FCPb as the sole energy-regulating complex in diatoms because its composition can more easily establish the balance between light-harvesting and quenching required for efficient photoprotection

Symmetry-breaking charge transfer and intersystem crossing in copper phthalocyanine thin films

Intermolecular interactions in π-stacked chromophores strongly influence their photophysical properties, and thereby also their function in photonic applications. Mixed electronic and vibrational coupling interactions lead to complex potential energy landscapes with competitive photophysical pathways. Here, we characterize the photoexcited dynamics of the small molecule semiconductor copper pthalocyanine (CuPc) in solution and in thin film, the latter comprising two different π-stacked architectures, α-CuPc and β-CuPc. In solution, CuPc undergoes ultrafast intersytem crossing (ISC) to the triplet excited state. In the solid state, both α-CuPc and β-CuPc morphologies exhibit a mixing between Frenkel and charge-transfer excitons (Frenkel-CT mixing). We find that this mixing influences the photophysical properties differently, based on morphology. In addition to ISC, α-CuPc demonstrates symmetry-breaking charge transfer, which furthermore depends on excitation wavelength. This mechanism is not observed in β-CuPc. These results elucidate how molecular organization mediates the balance of competitive photexcited decay mechanisms in organic semiconductors