Do photosynthetic complexes use quantum coherence to increase their efficiency?

Do photosynthetic complexes use quantum coherence to increase their efficiency?
Mechanisms of efficiency-driven evolution and environment-assisted quantum transport. (A) Schematic description of the evolutionary progress of photosynthetic complexes toward their current geometry, with efficiency being the evolutionary driving force. As evolution progresses, the structure of the photosynthetic complex evolves toward its current structure [the Fenna-Matthews-Olson (FMO) complex in this example] while increasing efficiency. Whether this is indeed the evolutionary pathway of photosynthetic complexes, and if so, whether quantum coherence is part of the efficiency enhancement is a central question in the field of quantum biology. (B) Schematic depiction of the population uniformization mechanism shown for a uniform chain of six sites (blue lines depict the sites in the chain; yellow arrows show the excitation of first site and extraction from fifth site). The density of the sites is described by blue bars for the quantum regime, ENAQT regime, and classical regime, along with a schematic form for the current versus dephasing curves. Credit: Science Advances, doi: 10.1126/sciadv.abc4631

In a new report now published on Science Advances, Elinor Zerah Harush and Yonatan Dubi in the departments of chemistry and nanoscale science and technology, at the Ben-Gurion University of the Negev, Israel, discussed a direct evaluation of the effects of quantum coherence on the efficiency of three natural photosynthetic complexes. The open quantum systems approach allowed the researchers to simultaneously identify the quantum-nature and efficiency under natural physiological conditions. These systems resided in a mixed quantum-classical regime, which they characterized using dephasing-assisted transport. The efficiency was minimal at best therefore the presence of quantum coherence did not play a substantial role in the process. The efficiency was also independent of any structural parameters, suggesting the role of evolution during structural design for other uses.

Investigating quantum effects in biology

During photosynthesis, energy can be transferred from an antenna to a reaction center to collect light and convert it to for use by the organism. Exciton-bound electron hole pairs formed the energy carriers in the photosynthetic process to carry harvested solar energy from the antenna to the reaction center via a network of bacteriochlorophylls (photosynthetic pigments that occur in bacteria), also known as the exciton-transfer complex (ETC). Interests on the ETC have expanded in the past decade where researchers used ultrafast nonlinear spectroscopy signals to demonstrate long-lived oscillations. The discovery of coherent oscillations in ETCs presented the hypothesis that quantum coherence occurred within natural photosynthetic complexes to assist energy transfer. Harush et al. sought to understand if quantum coherence could exist in the biological process of photosynthetic energy transfer. If so, was it used by the natural system for enhanced functional efficiency? While experimental and theoretical work have addressed these questions, they remain largely unanswered. In this work, the team addressed the questions using tools developed from the theory of open quantum systems. The findings suggest the unlikelihood for photosynthetic complexes to use quantum coherence to increase their efficiency.

Do photosynthetic complexes use quantum coherence to increase their efficiency?
Effect of environment on photosynthetic transfer efficiency in FMO and PC645. Calculated exciton current as a function of dephasing for the FMO (A) and PC-645 (B) complexes. The shaded green area indicates the estimated range of physiological dephasing rates. Insets show a schematic description of the exciton complexes. Credit: Science Advances, doi: 10.1126/sciadv.abc4631
The experiments

The team considered three different photosynthetic ETCs (exciton-transfer complexes) during the experiments. These include the Fenna-Matthews-Olson (FMO) complex—which appears in green sulfur bacteria, the cryptophyte phycocyanin-645 (PC-645) protein—a part of the photosynthetic apparatus in cryptophyte algae, and light harvesting 2 (LH2) – a part of the purple photosynthetic bacterium Rhodopseudomonas acidophila. All three complexes showed coherent energy transfer oscillations in nonlinear two-dimensional spectroscopy measurements. The team plotted the exciton current as a function of the dephasing rate for the FMO complex and the PC-645 complex. The similarity between the plots indicted relative insensitivity of the current to the internal structure Hamiltonian. Using the bacterial populations Harush et al. tested the level of "quantumness" of the system. They recognized this using a connection between the exciton population and dephasing rate through the mechanism of environment-assisted quantum transport (ENAQT). The ENAQT effect was clearly visible in the results since the current showed a maximum in the dephasing rate. However, the current enhancement was minute at approximately 0.0015% increase to indicate the unlikely nature of the complex to impose a meaningful evolutionary driving force.

Do photosynthetic complexes use quantum coherence to increase their efficiency?
Exciton density arrangement in the formation of ENAQT. (A) Density configuration (i.e., exciton occupation at different sites) of the FMO complex for three different regimes: quantum limit (blue line, γdeph = 10−4 μs−1), biological condition (yellow line, γdeph = 106 μs−1), and classic limit (green line, γdeph = 1012 μs−1). The transition from the quantum regime toward the classical regime is accompanied by a shift in the density configuration, from a wave function–determined configuration to a uniform gradient between the source and the sink, with a uniform configuration in between. To more clearly see this, (B), (C) and (D) present the schematic structure of FMO, where each sphere represents a BChl site, and the color brightness reflects its density. Credit: Science Advances, doi: 10.1126/sciadv.abc4631

Effect of environment on photosynthetic transfer efficiency

The team next investigated the LH2 (light harvesting-2) complex to understand the connection between ENAQT (environment-assisted quantum transport) and the population. This was difficult due to the lack of spatial separation between the antenna and reaction center in the construct. The LH2 complex contained two rings of bacteriophyll pigments; B800 (yellow ring) and B850 (blue ring) named after their energy absorption resonance in nanometers and absorbing energy in the visible region of the spectrum. Each part of the complex could absorb light to excite an exciton, which transferred from one of the rings to the reaction center allowing many exciton transfer-paths to occur. However, a current versus dephasing curve for LH2 revealed the importance of coherence during transport. The team then plotted current as a function of dephasing rate of the LH2 system and noted a very small increase in current approximating 0.05 percent.

  • Do photosynthetic complexes use quantum coherence to increase their efficiency?
    Effect of environment on photosynthetic transfer efficiency in LH2. Average LH2 exciton current as a function of dephasing rate (black line), calculated for ≈900 possible paths. Pink curves show the current of arbitrary chosen realizations (i.e., entry and exit sites) in LH2. Shaded green area marks the natural dephasing rate. Inset: Schematic description of LH2 transfer network. Credit: Science Advances, doi: 10.1126/sciadv.abc4631
  • Do photosynthetic complexes use quantum coherence to increase their efficiency?
    Current versus dephasing rate for 5000 realizations of FMO-like networks. Energies were kept fixed, while hopping matrix elements were picked from a range of ±200 cm−1. ENAQT is obtained for almost the same range for all realizations, indicating the independence of efficiency in the ENAQT regime (and the regime itself) on the structure of the system. Credit: Science Advances, doi: 10.1126/sciadv.abc4631

Current, coherence and classicality.

The results of the study established the absence of a substantial increase in the exciton current when comparing the fully quantum case with the physiologically realistic dephasing rates. They also took classical systems in to account, which were not defined by the lack of any , although their coherences could be fully determined from the populations without additional information. Researchers had previously quantified the distinction between quantum and classical systems. In a classical system, the two currents will be the same, implying that quantum coherences do not carry additional information across the classical dynamics.

The outcome of this study indicated how the structures of interest relative to FMO, PC-645 and LH2 did not evolve to enhance the efficiency of the complexes. In the future, Elinor Zerah Harush and Yonatan Dubi intend to assess the origin of the observed dephasing time to acknowledge if the values calculated in the study are unique. The team also intend to understand other potential evolutionary advantages of the photosynthetic transfer complexes, which will guide biophysicists to broadly understand the possible role of quantum effects in complexes.

Explore further

Purple bacteria shine path to super-efficient light harvesting

More information: Harush E. Z. and Dubi Y. Do photosynthetic complexes use quantum coherence to increase their efficiency? Probably not. Science Advances, 10.1126/sciadv.abc4631

Engel G. S. et al. Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems. Nature, doi:

Panitchayangkoon G. et al. Long-lived quantum coherence in photosynthetic complexes at physiological temperature. PNAS, doi:

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