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Fleming, Graham R.

Publications and source records attributed to Fleming, Graham R..

13 records
All sourcesNASA NTRSDOE OSTI
DOE OSTI2024

The development and applications of multidimensional biomolecular spectroscopy illustrated by photosynthetic light harvesting

The parallel and synergistic developments of atomic resolution structural information, new spectroscopic methods, their underpinning formalism, and the application of sophisticated theoretical methods have led to a step function change in our understanding of photosynthetic light harvesting, the process by which photosynthetic organisms collect solar energy and supply it to their reaction centers to initiate the chemistry of photosynthesis. The new spectroscopic methods, in particular multidimensional spectroscopies, have enabled a transition from recording rates of processes to focusing on mechanism. We discuss two ultrafast spectroscopies – two-dimensional electronic spectroscopy and two-dimensional electronic-vibrational spectroscopy – and illustrate their development through the lens of photosynthetic light harvesting. Both spectroscopies provide enhanced spectral resolution and, in different ways, reveal pathways of energy flow and coherent oscillations which relate to the quantum mechanical mixing of, for example, electronic excitations (excitons) and nuclear motions. The new types of information present in these spectra provoked the application of sophisticated quantum dynamical theories to describe the temporal evolution of the spectra and provide new questions for experimental investigation. While multidimensional spectroscopies have applications in many other areas of science, we feel that the investigation of photosynthetic light harvesting has had the largest influence on the development of spectroscopic and theoretical methods for the study of quantum dynamics in biology, hence the focus of this review. We conclude with key questions for the next decade of this review.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2024

Design principles for energy transfer in the photosystem II supercomplex from kinetic transition networks

Photosystem II (PSII) has the unique ability to perform water-splitting. With light-harvesting complexes, it forms the PSII supercomplex (PSII-SC) which is a functional unit that can perform efficient energy conversion, as well as photoprotection, allowing photosynthetic organisms to adapt to the naturally fluctuating sunlight intensity. Achieving these functions requires a collaborative energy transfer network between all subunits of the PSII-SC. In this work, we perform kinetic analyses and characterise the energy landscape of the PSII-SC with a structure-based energy transfer model. With first passage time analyses and kinetic Monte Carlo simulations, we are able to map out the overall energy transfer network. We also investigate how energy transfer pathways are affected when individual protein complexes are removed from the network, revealing the functional roles of the subunits of the PSII-SC. In addition, we provide a quantitative description of the flat energy landscape of the PSII-SC. We show that it is a unique landscape that produces multiple kinetically relevant pathways, corresponding to a high pathway entropy. These design principles are crucial for balancing efficient energy conversion and photoprotection.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2024

Chlorophyll to zeaxanthin energy transfer in nonphotochemical quenching: An exciton annihilation-free transient absorption study

Zeaxanthin (Zea) is a key component in the energy-dependent, rapidly reversible, nonphotochemical quenching process (qE) that regulates photosynthetic light harvesting. Previous transient absorption (TA) studies suggested that Zea can participate in direct quenching via chlorophyll (Chl) to Zea energy transfer. However, the contamination of intrinsic exciton–exciton annihilation (EEA) makes the assignment of TA signal ambiguous. In this study, we present EEA-free TA data using Nicotiana benthamiana thylakoid membranes, including the wild type and three NPQ mutants (npq1, npq4, and lut2) generated by CRISPR/Cas9 mutagenesis. The results show a strong correlation between excitation energy transfer from excited Chl Q y to Zea S 1 and the xanthophyll cycle during qE activation. Notably, a Lut S 1 signal is absent in the npq1 thylakoids which lack zeaxanthin. Additionally, the fifth-order response analysis shows a reduction in the exciton diffusion length (L D ) from 62 ± 6 nm to 43 ± 3 nm under high light illumination, consistent with the reduced range of exciton motion being a key aspect of plants’ response to excess light.

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CH↗
DOE OSTI2023

Kinetics of the xanthophyll cycle and its role in photoprotective memory and response

Efficiently balancing photochemistry and photoprotection is crucial for survival and productivity of photosynthetic organisms in the rapidly fluctuating light levels found in natural environments. The ability to respond quickly to sudden changes in light level is clearly advantageous. In the alga Nannochloropsis oceanica we observed an ability to respond rapidly to sudden increases in light level which occur soon after a previous high-light exposure. This ability implies a kind of memory. In this work, we explore the xanthophyll cycle in N. oceanica as a short-term photoprotective memory system. By combining snapshot fluorescence lifetime measurements with a biochemistry-based quantitative model, we show that short-term memory arises from the xanthophyll cycle. In addition, the model enables us to characterize the relative quenching abilities of the three xanthophyll cycle components. Given the ubiquity of the xanthophyll cycle in photosynthetic organisms the model described here will be of utility in improving our understanding of vascular plant and algal photoprotection with important implications for crop productivity.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2023

Single-photon absorption and emission from a natural photosynthetic complex

Photosynthesis is generally assumed to be initiated by a single photon from the Sun, which, as a weak light source, delivers at most a few tens of photons per nanometre squared per second within a chlorophyll absorption band1. Yet much experimental and theoretical work over the past 40 years has explored the events during photosynthesis subsequent to absorption of light from intense, ultrashort laser pulses. Here, we use single photons to excite under ambient conditions the light-harvesting 2 (LH2) complex of the purple bacterium Rhodobacter sphaeroides, comprising B800 and B850 rings that contain 9 and 18 bacteriochlorophyll molecules, respectively. Excitation of the B800 ring leads to electronic energy transfer to the B850 ring in approximately 0.7 ps, followed by rapid B850-to-B850 energy transfer on an approximately 100-fs timescale and light emission at 850–875 nm. Using a heralded single photon source20,21 along with coincidence counting, we establish time correlation functions for B800 excitation and B850 fluorescence emission and demonstrate that both events involve single photons. We also find that the probability distribution of the number of heralds per detected fluorescence photon supports the view that a single photon can upon absorption drive the subsequent energy transfer and fluorescence emission and hence, by extension, the primary charge separation of photosynthesis. An analytical stochastic model and a Monte Carlo numerical model capture the data, further confirming that absorption of single photons is correlated with emission of single photons in a natural light-harvesting complex.

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CH↗
DOE OSTI2022

Room-temperature polariton quantum fluids in halide perovskites

Abstract Quantum fluids exhibit quantum mechanical effects at the macroscopic level, which contrast strongly with classical fluids. Gain-dissipative solid-state exciton-polaritons systems are promising emulation platforms for complex quantum fluid studies at elevated temperatures. Recently, halide perovskite polariton systems have emerged as materials with distinctive advantages over other room-temperature systems for future studies of topological physics, non-Abelian gauge fields, and spin-orbit interactions. However, the demonstration of nonlinear quantum hydrodynamics, such as superfluidity and Čerenkov flow, which is a consequence of the renormalized elementary excitation spectrum, remains elusive in halide perovskites. Here, using homogenous halide perovskites single crystals, we report, in both one- and two-dimensional cases, the complete set of quantum fluid phase transitions from normal classical fluids to scatterless polariton superfluids and supersonic fluids—all at room temperature, clear consequences of the Landau criterion. Specifically, the supersonic Čerenkov wave pattern was observed at room temperature. The experimental results are also in quantitative agreement with theoretical predictions from the dissipative Gross-Pitaevskii equation. Our results set the stage for exploring the rich non-equilibrium quantum fluid many-body physics at room temperature and also pave the way for important polaritonic device applications.

42 ENGINEERING↗
DOE OSTI2022

From antenna to reaction center: Pathways of ultrafast energy and charge transfer in photosystem II

The photosystem II core complex (PSII-CC) is the smallest subunit of the oxygenic photosynthetic apparatus that contains core antennas and a reaction center, which together allow for rapid energy transfer and charge separation, ultimately leading to efficient solar energy conversion. However, there is a lack of consensus on the interplay between the energy transfer and charge separation dynamics of the core complex. Here, we report the application of two-dimensional electronic-vibrational (2DEV) spectroscopy to the spinach PSII-CC at 77 K. The simultaneous temporal and spectral resolution afforded by 2DEV spectroscopy facilitates the separation and direct assignment of coexisting dynamical processes. Our results show that the dominant dynamics of the PSII-CC are distinct in different excitation energy regions. By separating the excitation regions, we are able to distinguish the intraprotein dynamics and interprotein energy transfer. Additionally, with the improved resolution, we are able to identify the key pigments involved in the pathways, allowing for a direct connection between dynamical and structural information. Specifically, we show that C505 in CP43 and the peripheral chlorophyll Chlz D1 in the reaction center are most likely responsible for energy transfer from CP43 to the reaction center.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2022

The major trimeric antenna complexes serve as a site for qH-energy dissipation in plants

Plants and algae are faced with a conundrum: harvesting sufficient light to drive their metabolic needs while dissipating light in excess to prevent photodamage, a process known as nonphotochemical quenching. A slowly relaxing form of energy dissipation, termed qH, is critical for plants’ survival under abiotic stress; however, qH location in the photosynthetic membrane is unresolved. Here, we tested whether we could isolate subcomplexes from plants in which qH was induced that would remain in an energy-dissipative state. Interestingly, we found that chlorophyll (Chl) fluorescence lifetimes were decreased by qH in isolated major trimeric antenna complexes, indicating that they serve as a site for qH-energy dissipation and providing a natively quenched complex with physiological relevance to natural conditions. Next, we monitored the changes in thylakoid pigment, protein, and lipid contents of antenna with active or inactive qH but did not detect any evident differences. Finally, we investigated whether specific subunits of the major antenna complexes were required for qH but found that qH was insensitive to trimer composition. Because we previously observed that qH can occur in the absence of specific xanthophylls, and no evident changes in pigments, proteins, or lipids were detected, we tentatively propose that the energy-dissipative state reported here may stem from Chl–Chl excitonic interaction.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2022

Interference between Franck–Condon and Herzberg–Teller Terms in the Condensed-Phase Molecular Spectra of Metal-Based Tetrapyrrole Derivatives

The commonly used Franck-Condon (FC) approximation is inadequate for explaining the electronic spectra of compounds that possess vibrations with substantial Herzberg-Teller (HT) couplings. Metal-based tetrapyrrole derivatives, which are ubiquitous natural pigments, often exhibit prominent HT activity. In this paper, we compare the condensed phase spectra of zinc-tetraphenylporphyrin (ZnTPP) and zinc-phthalocyanine (ZnPc), which exhibit vastly different spectral features in spite of sharing a common tetrapyrrole backbone. The absorption and emission spectra of ZnTPP are characterized by a lack of mirror symmetry and nontrivial temperature dependence. In contrast, mirror symmetry is restored, and the nontrivial temperature-dependent features disappear in ZnPc. We attribute these differences to FC-HT interference, which is less pronounced in ZnPc because of a larger FC component in the dipole moment that leads to FC-dominated transitions. A single minimalistic FC-HT vibronic model reproduces all the experimental spectral features of these molecules. These observations suggest that FC-HT interference is highly susceptible to chemical modification.

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CH↗