Polaritons in Living Systems: Modifying Energy Landscapes in Photosynthetic Organisms Using a Photonic Structure
David M Coles, Lucas C Flatten, Thomas Sydney, Emily Hounslow, Semion K Saikin, Alán Aspuru-Guzik, Vlatko Vedral, Joseph Kuo-Hsiang Tang, Robert A Taylor, Jason… 展开作者
David M Coles, Lucas C Flatten, Thomas Sydney, Emily Hounslow, Semion K Saikin, Alán Aspuru-Guzik, Vlatko Vedral, Joseph Kuo-Hsiang Tang, Robert A Taylor, Jason M Smith, David G Lidzey
Photosynthetic organisms rely on a series of self-assembled nanostructures with tuned electronic energy levels in order to transport energy from where it is collected by photon absorption, to reaction centers where the energy is used to drive chemical reactions. In the photosynthetic bacteria Chlorobaculum tepidum (Cba. tepidum), a member of the green sulphur bacteria (GSB) family, light is absorbed by large antenna complexes called chlorosomes. The exciton generated is transferred to a protein baseplate attached to the chlorosome, before traveling through the Fenna-Matthews-Olson (FMO) complex to the reaction center. The energy levels of these systems are generally defined by their chemical structure. Here we show that by placing bacteria within a photonic microcavity, we can access the strong exciton-photon coupling regime between a confined cavity mode and exciton states of the chlorosome, whereby a coherent exchange of energy between the bacteria and cavity mode results in the formation of polariton states. The polaritons have an energy distinct from that of the exciton and photon, and can be tuned in situ via the microcavity length. This results in real-time, non-invasive control over the relative energy levels within the bacteria. This demonstrates the ability to strongly influence living biological systems with photonic structures such as microcavities. We believe that by creating polariton states, that are in this case a superposition of a photon and excitons within a living bacteria, we can modify energy transfer pathways and therefore study the importance of energy level alignment on the efficiency of photosynthetic systems.
Photosynthesis transfers energy efficiently through a series of antenna complexes to the reaction center where charge separation occurs. Energy transfer in vivo is primarily monitored by measuring fluorescence signals from the small fraction of excitations that fail to result in charge separation. Here, we use two-dimensional electronic spectroscopy to follow the entire energy transfer process in a thriving culture of the purple bacteria, Rhodobacter sphaeroides. By removing contributions from scattered light, we extract the dynamics of energy transfer through the dense network of antenna comp…
Antenna systems serve to absorb light and to transmit excitation energy to the reaction center (RC) in photosynthetic organisms. As the emitted (bacterio)chlorophyll fluorescence competes with the photochemical utilization of the excitation, the measured fluorescence yield is informed by the migration of the excitation in the antenna. In this work, the fluorescence yield concomitant with the oxidized dimer (P+) of the RC were measured during light excitation (induction) and relaxation (in the dark) for whole cells of photosynthetic bacterium Rhodobacter sphaeroides lacking cytochrome c_2 as na…
Photosynthetic organisms use networks of chromophores to absorb sunlight and deliver the energy to reaction centres, where charge separation triggers a cascade of chemical steps to store the energy. We present a detailed model of the light-harvesting complexes in purple bacteria, including explicit interaction with sunlight; energy loss through radiative and non-radiative processes; and dephasing and thermalizing effects of coupling to a vibrational bath. An important feature of the model is that we capture the effect of slow vibrational modes by introducing time-dependent disorder. Our model …
The study of how photosynthetic organisms convert light offers insight not only into nature's evolutionary process, but may also give clues as to how best to design and manipulate artificial photosynthetic systems -- and also how far we can drive natural photosynthetic systems beyond normal operating conditions, so that they can harvest energy for us under otherwise extreme conditions. In addition to its interest from a basic scientific perspective, therefore, the goal to develop a deep quantitative understanding of photosynthesis offers the potential payoff of enhancing our current arsenal of…
Pennes' differential equation for bioheat transfer and the heat transfer equation are solved for the temperature distribution in a living tissue with spherical inclusions, irradiated by microwave power. It is shown that relative temperature excess in a small inclusion in the tissue in some cases is inversely proportional to its radius and does not depend on the applied power. In pulsing RF fields the effect is amplified proportionally to the ratio of the pulse period to the pulse duration. The local temperature rise significantly outpaces the averaged one and therefore the Watt to Weight SAR l…
For any system, whether physical or non-physical, knowledge of the form and strength of inter-individual interactions is a key-information. In an approach based on statistical physics one needs to know the interaction Hamiltonian. For non-physical systems, based on qualitative arguments similar to those used in physical chemistry, interaction strength gives useful clues about the macroscopic properties of the system. Even though our ultimate objective is the understanding of social phenomena, we found that systems composed of insects (or other living organisms) are of great convenience for inv…
In photosynthetic organisms, the energy of light during illumination is absorbed by the antenna complexes, which is transmitted by excitons and is either absorbed by the reaction centers (RCs), which have been closed in this way, or emitted by fluorescence. The basic components of the dynamics of light absorption have been integrated into a simple model of exciton migration, which contains two parameters: the exciton hopping probability and the exciton lifetime. During continuous radiation with light the fraction of closed RCs, $x$, continuously increases and at a critical threshold, $x_c$, a …
Metabolic energy consumption has long been thought to play a major role in the aging process ({\it 1}). Across species, a gram of tissue on average expends about the same amount of energy during life-span ({\it 2}). Energy restriction has also been shown that increases maximum life-span ({\it 3}) and retards age-associated changes ({\it 4}). However, there are significant exceptions to a universal energy consumption during life-span, mainly coming from the inter-class comparison ({\it 5, 6}). Here we present a unique relation for life-span energy consumption, valid for $\sim$300 species repres…
Trying to identify the entropy production within a cell has been part of debates and studies in the last century. First the idea was to make a resemblance of a cell with a Carnot engine, which is the most thermodynamically perfect machine. This approach was clearly not the best, since the yield achieved within a cell cannot be ideal, but can we even measure it? Several models approach the living cell, since the very simple one (e.g. Prigogine model) to more elaborated proposals. The concept of entropy has been the centre of discussions within several scientific fields. To interpret how entropy…
All organisms, fundamentally, are made from the same raw material, namely the elements of the periodic table. Biochemical diversity is achieved with how these elements are utilized, for what purpose and in which physical location. Determining elemental distributions, especially those of trace elements that facilitate metabolism as cofactors in the active centers of essential enzymes, can determine the state of metabolism, the nutritional status or the developmental stage of an organism. Photosynthetic eukaryotes, especially algae, are excellent subjects for quantitative analysis of elemental d…
Various Hamiltonian models have been derived for chemical structures belonging to living organisms while the Hamiltonian concept was not applied to life as a whole. However, Hamiltonian components were recently defined for living organisms on the condition to take in consideration their evolutionary implications (Bounias, 2001: CASYS'0l). This paper identifies differential elements of Spacetime, from which it delimits a probabilistic fuzzy-like invariance standing for conservativity of biological Hamiltonians. The distributions of potential and kinetic components in a individual bio-Hamiltonia…
Photosynthetic organisms harvest light energy, utilizing the absorption and energy transfer properties of protein-bound chromophores. Controlling the harvesting efficiency is critical for the optimal function of the photosynthetic apparatus. Here, we show that cyanobacterial light-harvesting antenna may be able to regulate the flow of energy in order to switch reversibly from efficient energy conversion to photo-protective quenching via a structural change. We isolated cyanobacterial light harvesting proteins, phycocyanin and allophycocyanin, and measured their optical properties in solution a…
Biological cells and many living organisms are mostly made of liquids and therefore, by analogy with liquid drops, they should exhibit a range of fundamental nonlinear phenomena such as the onset of standing surface waves. Here, we test four common species of earthworm to demonstrate that vertical vibration of living worms lying horizontally of a flat solid surface results in the onset of subharmonic Faraday-like body waves, which is possible because earthworms have a hydrostatic skeleton with a flexible skin and a liquid-filled body cavity. Our findings are supported by theoretical analysis b…
Physical Approaches to Metabolic Scaling in Living Systems
Aix-Marseille Université（艾克斯-马赛大学）；INSERM（法国国家健康与医学研究院）；DyNaMo（动态建模中心）；Turing Centre for Living Systems（图灵生命系统中心）；Max Planck Institute for the Physics of Complex Systems（马克斯·普朗克复杂系统物理研究所）；Case Western Reserve University（凯斯西储大学）；Cluster of Excellence Physics of Life (PoL)（生命物理学卓越集群）；Center for Systems Biology Dresden（德累斯顿系统生物学中心）
Active crystals are highly ordered structures that emerge from the self-organization of motile objects, and have been widely studied in synthetic and bacterial active matter. Whether collective crystallization phenomena can occur in groups of autonomously developing multicellular organisms is currently unknown. Here, we show that swimming starfish embryos spontaneously assemble into chiral crystals that span thousands of spinning organisms and persist for tens of hours. Combining experiments, theory, and simulations, we demonstrate that the formation, dynamics, and dissolution of these living …
Recent field investigations of photosynthetic bacteria living in geothermal hot spring environments have revealed surprisingly complex ecosystems, with an unexpected level of genetic diversity. One case of particular interest involves the distribution along hot spring thermal gradients of genetically distinct bacterial strains that differ in their preferred temperatures for reproduction and photosynthesis. In such systems, a single variable, temperature, defines the relevant environmental variation. In spite of this, each region along the thermal gradient exhibits multiple strains of photosynt…
The theory of evolution by natural selection cannot be used to evaluate the truth value of the following proposition: Through evolution, there exists at least one species that can adapt to any one given environment. To address this issue, this study attempted to define natural selection from the perspective of mathematical and physical laws. This study roughly classified biological activities into molecular, cellular, individual, ecological, and biogeochemical (atomic) levels according to scale and complexity, and selected typical phenomena from each level to analyze the relationship between a…
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Natural organisms such as photosynthetic bacteria, algae, and plants employ complex molecular machinery to convert solar energy into biochemical fuel. An important common feature shared by most of these photosynthetic organisms is that they capture photons in the form of excitons typically delocalized over a few to tens of pigment molecules embedded in protein environments of light harvesting complexes (LHCs). Delocalized excitons created in such LHCs remain well protected despite being swayed by environmental fluctuations, and are delivered successfully to their destinations over hundred nano…
Living organisms are inherently out-of-equilibrium systems. We employ new developments in stochastic energetics and rely on a minimal microscopic model to predict the amount of mechanical energy dissipated by such dynamics. Our model includes complex rheological effects and nonequilibrium stochastic forces. By performing active microrheology and tracking micron-sized vesicles in the cytoplasm of living oocytes, we provide unprecedented measurements of the spectrum of dissipated energy. We show that our model is fully consistent with the experimental data, and we use it to offer predictions for…
The sense of smell is an important part of living organisms. It assists with the interaction of the living organism with its environment. The mechanism by which smell is detected and identified is not fully known. Earlier, shape theory was proposed as an explanation for odor perception mechanism. This theory posits that the shape of the odorant must fit in its complementary olfactory receptor for an odor to be identified -- just like key fits in a lock. This theory turns out to have some limitations, thus leading to the proposition of new theory called the vibrational theory of olfaction. In v…
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For more than 50 years we have known that photosynthetic systems harvest solar energy with almost unit {\it quantum efficiency}. However, recent experimental evidence of {\it quantum coherence} during the excitonic energy transport in photosynthetic organisms challenges our understanding of this fundamental biological function. Currently, and despite numerous efforts, the causal connection between coherence and efficiency is still a matter of debate. We show, through the study of extensive simulations of quantum coherent transport on networks, that three dimensional structures characterized by…
The metabolic processes complexity is at the heart of energy conversion in living organisms and forms a huge obstacle to develop tractable thermodynamic metabolism models. By raising our analysis to a higher level of abstraction, we develop a compact -- i.e. relying on a reduced set of parameters -- thermodynamic model of metabolism, in order to analyze the chemical-to-mechanical energy conversion under muscle load, and give a thermodynamic ground to Hill's seminal muscular operational response model. Living organisms are viewed as dynamical systems experiencing a feedback loop in the sense th…
Phototrophic organisms such as plants, photosynthetic bacteria and algae use microscopic complexes of pigment molecules to absorb sunlight. Within the light-harvesting complexes, which frequently have several functional and structural subunits, the energy is transferred in the form of molecular excitations with very high efficiency. Green sulfur bacteria are considered to be amongst the most efficient light-harvesting organisms. Despite multiple experimental and theoretical studies of these bacteria the physical origin of the efficient and robust energy transfer in their light-harvesting compl…
Collective motion of self-propelled organisms or synthetic particles often termed active fluid has attracted enormous attention in broad scientific community because of it fundamentally non-equilibrium nature. Energy input and interactions among the moving units and the medium lead to complex dynamics. Here we introduce a new class of active matter, living liquid crystals (LLCs) that combine living swimming bacteria with a lyotropic liquid crystal. The physical properties of LLCs can be controlled by the amount of oxygen available to bacteria, by concentration of ingredients, or by temperature…
We extend the concept that life is an informational phenomenon, at every level of organisation, from molecules to the global ecological system. According to this thesis: (a) living is information processing, in which memory is maintained by both molecular states and ecological states as well as the more obvious nucleic acid coding; (b) this information processing has one overall function - to perpetuate itself; and (c) the processing method is filtration (cognition) of, and synthesis of, information at lower levels to appear at higher levels in complex systems (emergence). We show how informat…
