Quantum phase synchronization via exciton-vibrational energy dissipation sustains long-lived coherence in photosynthetic antennas

Coherent energy transfer is a highly efficient energy transfer pathway in photosynthesis. Matching of long-lived quantum coherence to the time scale of energy transfer is a prerequisite. In contrast to short-lived electronic coherence, the presence of exciton-vibrational coherence in photosynthetic systems5,6 can account for the observed long-lasting quantum coherence. However, uncovering the mechanism of such coherence within a biological environment is challenging because of the presence of noise typically encountered at room temperature. This paper presents conclusive evidence of the existence of long-lasting electronic vibronic coherence in the allophycocyanin trimer, in which pigment pairs behave as excitonic dimers with weak exciton-vibrational coupling. Employing ultrafast two-dimensional electronic spectroscopy, our study demonstrates an extension of the exciton-vibrational coherence time within the trimer compared with the isolated pigments. The prolonged quantum coherences were identified as arising from the quantum phase synchronization of the resonant vibrational collective modes for the pigment pair. The anti-symmetric resonant collective modes undergo fast energy dissipation when coupled to the delocalized electronic states of fast dephasing, while the decoupled symmetric resonant collective modes survive. The nuclear motion of the symmetric resonant collective modes leads to the correlated energy fluctuation of the excitonic energy levels on the two individual pigment molecules in the dimer, resulting in significantly lowered energy dissipation and supporting long-lasting quantum coherences. The presence of the quantum phase synchronization was confirmed by two experimental indicators consistent with the expectation, i.e., about half reduction in the vibrational intensities of the resonant modes and their almost zero intensites in dynamical Stokes shift spectrum. This paper provides direct evidence revealing how biological systems effectively employ a quantum synchronization strategy to uphold persistent coherences, and our findings pave the way for protecting coherences against the noisy environment in quantum biology.