The study of quantum phenomena in biology has received significant attention in the last decade. One of the problems of most interest is the understanding of quantum effects during the first steps of photosynthesis. Ultrafast two-dimensional electronic spectroscopy has revealed that pigment-protein complexes responsible for light- harvesting and charge separation in photosynthetic organisms can support quantum coherent dynamics in the excited state, for up to few hundreds of femtoseconds. The leading hypothesis on the mechanisms supporting this coherent behaviour is quan- tum interactions between electronic and some specific vibrational motions in the excited state. This hypothesis, however, awaits unambiguous confirmation. Among the most powerful techniques to investigate the quantum behaviour of an emitter is the study of quantum optical properties of the light it emits. This thesis de- velops theoretical studies showing that frequency-filtered and time-resolved photon counting statistics of the light emitted by a prototype photosynthetic unit can give important insight into the quantum coherent nature and the mechanisms underlying excited state dynamics in single photosynthetic complexes. By developing a pertur- bative and efficient approach to the computation of frequency- and time- resolved photon correlation functions, we show that such correlations have the potential to give unambiguous signatures of coherence contributions to the steady state emis- sion. For a light-harvesting unit emitting in free space, the signatures of excited state coherence manifest themselves as non-trivial antibunching. This feature can- not be probed by measuring unfiltered photon correlations. We then consider the situation in which a prototype energy transfer unit is embedded in an optical cavity such that its emission rate is enhanced. In this case we observed a rich behaviour of the frequency-filtered, second-order photon correlations that allows a clear distinc- tion of coherence contributions, and their variation, depending of the electronic and vibrational interactions in the system of interest.
The study of quantum phenomena in biology has received significant attention in the last decade. One of the problems of most interest is the understanding of quantum effects during the first steps of photosynthesis. Ultrafast two-dimensional electronic spectroscopy has revealed that pigment-protein complexes responsible for light- harvesting and charge separation in photosynthetic organisms can support quantum coherent dynamics in the excited state, for up to few hundreds of femtoseconds. The leading hypothesis on the mechanisms supporting this coherent behaviour is quan- tum interactions between electronic and some specific vibrational motions in the excited state. This hypothesis, however, awaits unambiguous confirmation. Among the most powerful techniques to investigate the quantum behaviour of an emitter is the study of quantum optical properties of the light it emits. This thesis de- velops theoretical studies showing that frequency-filtered and time-resolved photon counting statistics of the light emitted by a prototype photosynthetic unit can give important insight into the quantum coherent nature and the mechanisms underlying excited state dynamics in single photosynthetic complexes. By developing a pertur- bative and efficient approach to the computation of frequency- and time- resolved photon correlation functions, we show that such correlations have the potential to give unambiguous signatures of coherence contributions to the steady state emis- sion. For a light-harvesting unit emitting in free space, the signatures of excited state coherence manifest themselves as non-trivial antibunching. This feature can- not be probed by measuring unfiltered photon correlations. We then consider the situation in which a prototype energy transfer unit is embedded in an optical cavity such that its emission rate is enhanced. In this case we observed a rich behaviour of the frequency-filtered, second-order photon correlations that allows a clear distinc- tion of coherence contributions, and their variation, depending of the electronic and vibrational interactions in the system of interest.
Identifying signatures of quantum coherent behaviour in photoactive systems that are maintained in stationary states away from thermal equilibrium is an open problem of wide interest in a variety of physical scenarios, including single photosynthetic complexes subjected to continuous incoherent illumination. Here we consider a prototype light-harvesting heterodimer exhibiting coherent and collective exciton-vibration interactions and show that the second-order frequency-filtered correlations of fluorescence photons provide insightful information on the influence of such coherent interactions for different transitions, thereby yielding fundamentally different photon-counting statistics. Furthermore, we show that coherent vibronic mechanisms strongly affect the asymmetries characteristic of time-resolved photon cross-correlations and manifest themselves in a time-dependent violation of the Cauchy-Schwarz inequality bounding cross-correlations for classically fluctuating fields. We finally discuss how such second-order correlation asymmetry establishes important connections between coherent vibronic interactions, directional exciton population transport, and violation of quantum detailed balance. Our work then indicates that measurement of two-colour photon correlation asymmetry can be an important avenue to investigate quantum behaviour of single photoactive biomolecular and chemical systems under incoherent illumination conditions.
Ultrafast spectroscopy experiments show that photosynthetic systems can preserve quantum beats in the process of electronic energy transfer between pigments, even at room temperature. But what does this discovery imply for biology - and for quantum mechanics? This dissertation examines photosynthesis through the tools of quantum information science. We evaluate to what extent photosynthesis can be thought of as a type of quantum technology, and consider how we can apply experimental tools widely used for quantum technologies (state tomography and coherent control) to photosynthesis. Throughout, we use the Fenna-Matthews-Olson (FMO) complex of greens sulfur bacteria as a model photosynthetic pigment-protein complex.In Part I, we evaluate two mechanisms for the possible biological relevance of quantum coherent motion. First, we consider the extent to which dynamics in light-harvesting systems exhibit the quantum speedups characteristic of quantum algorithms and quantum walks. Second, we demonstrate a ratchet effect in electronic energy transfer enabled by partially coherent dynamics. To do so, we build a new model of energy transfer between weakly coupled light-harvesting complexes to understand how electronic coherence arises under natural conditions.In Part II, we present proposals for experimental probes of light harvesting dynamics with ultrafast spectroscopy. We show how the signal from pump-probe spectroscopy can be formally inverted to determine the excited state electronic density matrix. Finally, we examine the feasiblity of coherent control experiments on light-harvesting systems, and provide two realistic targets feasible with present-day technology.
We investigate how optical second-order cross correlations witness the quantum features of a prototype donor-acceptor light-harvesting unit. By considering a pair of detuned two-level emitters electronically coupled and incoherently driven to a non-equilibrium steady-state, we gain insight into how electronic quantum properties such as exciton eigenstate delocalization, coherent energy transfer and steady-state electronic coherence, are manifested in the joint probability of emission or optical second-order cross correlation. Specifically, we show that the frequency associated with oscillations present in time-resolved second-order cross correlation functions quantifies not only the time scale of coherent energy transfer but also the degree of delocalization of the exciton eigenstates. Furthermore, we show that time-resolved cross correlations directly witness steady-state electronic coherence. Our work strengthens the idea that measurements of the intensity quantum cross correlations can provide distinctive signatures of the quantum behavior of biophysical emitters.
For many years, the fields of quantum optics and biology have rarely shared a common path. In quantum optics, most of the concepts and techniques developed over the years stand for systems where only a few degrees of freedom are considered and, more importantly, where the systems under study are assumed to be completely isolated from their surrounding environment. This situation is far from what we can find in nature. Biological complexes are, by definition, warm, wet and noisy systems subjected to environmental fluctuations, where quantum phenomena are unlikely to be observed. Notwithstanding, in recent years, this paradigm has begun to be questioned by several works where quantum-mechanical concepts have been introduced in order to describe the dynamics of important biological processes, such as energy transport in photosynthetic light-harvesting complexes. The goal of this thesis is twofold. Firstly, we will investigate how ideas and techniques routinely used in quantum optics can be exploited in order to develop new quantum-based spectroscopy techniques and, secondly, we will examine to what extent microscopic quantum phenomena could impact on the efficient transport behavior of photosynthetic light-havesting complexes. This problem is particularly relevant, because the understanding of the fundamental mechanisms that enable the highly efficient transport of energy in photosynthetic systems could lead us to the design of future quantum-inspired light-harvesting technologies, such as high-efficiency organic solar cells.
We review recent theoretical calculations of quantum entanglement in photosynthetic light harvesting complexes. These works establish, for the first time, a manifestation of this characteristically quantum mechanical phenomenon in biologically functional structures. We begin by summarizing calculations on model biomolecular systems that aim to reveal non-trivial characteristics of quantum entanglement in non-equilibrium biological environments. We then discuss and compare several calculations performed recently of excitonic dynamics in the Fenna-Matthews-Olson light harvesting complex and of the electronic entanglement present in this widely studied pigment-protein structure. We point out the commonalities between the derived results and also identify and explain the differences. We also discuss recent work that examines entanglement in the structurally more intricate light harvesting complex II (LHCII). During this overview, we take the opportunity to clarify several subtle issues relating to entanglement in such biomolecular systems, including the role of entanglement in biological function, the complexity of dynamical modeling that is required to capture the salient features of entanglement in such biomolecular systems, and the relationship between entanglement and other quantum mechanical features that are observed and predicted in light harvesting complexes. Finally, we suggest possible extensions of the current work and also review the options for experimental confirmation of the predicted entanglement phenomena in light harvesting complexes.
Ultrafast pulses allow observation of molecular dynamics with femtosecond time resolution through pump probe experiments. However, averaging over an ensemble of molecules tends to wash out phase sensitive information, necessary to probe quantum effects, due to the intrinsic inhomogeneity in molecular conformations, orientations and interactions that lead to unique potential energy landscapes for each molecule. It is therefore important to go beyond the ensemble average when looking at quantum dynamics of organic systems at room temperature, and resolve the behaviour of specific molecules on an individual basis. In this thesis, we show the creation, manipulation and observation of ultrafast coherent effects in single molecules at room temperature, and resolve a certain measure of environmental influence on the specific dynamics of each molecule. Moreover, we apply this insight to investigate a functional light harvesting biosystem, and lay the basis for a technique that has the time and space resolution required to observe these systems in vivo. In chapter 1, we introduce the concepts and techniques the research in this thesis is built on. In chapter 2, we treat the possibility of controlling ultrafast pulses at the high-NA diffraction limit, and come to conclusions about the procedure to follow there that hold for all pulse-shaping experiments. We show in proof of principle experiments that we can control the ultrafast characteristics of optical pulses in nanometric excitation volumes. In chapters 3 and 4 we report the creation, detection and control of ultrafast quantum dynamics in single organic molecules at room temperature. We show that manipulation of superposition states is possible in these systems within a coherence dephasing time of ~50 fs. This leads to the first observation of rabi-oscillations in room temperature single molecules, to ultrafast operation of an organic qubit, and to the creation of non-stationary superposition states (vibrational wavepackets). We probe the influence of the local environment on the composition and dynamics of these wavepackets and show we can optimize the state preparation protocol for each individual molecule in its own nanoenvironment, leading to high fidelity coherent control. In these chapters we lay out the proof of principle work of detecting the quantumdynamics of a complex system in interaction with its environment at room temperature. In chapter 5 we discuss application of these techniques to the investigation of long lived coherence in photosynthetic systems. We show that electronic coherence between different rings of the LH2 system persists to time scales of 100s of femtoseconds at room temperature. Moreover we show that the energy transfer pathways in LH2 adapt to environmentally induced changes in the molecule and that the nature of the transfer remains coherent for each pathway, providing strong evidence that coherent energy transfer is the optimum process for energy transfer in photosynthesis. Finally, in chapter 6 we take the technical development one step further and report on the creation of a framework based on plasmonic antennas that allows for control of the amplitude-phase characteristics in nanometric sized hotspot fields. We show for the first time that the ultrafast characteristics of plasmonic hotspots can directly be engineered through design of the plasmonic system and experimentally demonstrate two much-anticipated examples: a sub-diffraction resolution phase shaper and an ultrafast plasmonic switch for pump probe experiments. The results presented in this thesis form the first creation and observation of ultrafast coherent dynamics in individual molecular systems at room temperature. This is a necessary step to be able to do true quantum tomography in complex systems, resolve the influence of the environment on molecular dynamics, and investigate the physics that determines evolutionary optimization and functionality in biomolecules.