Upper-state-assisted uphill energy transfer in a far-red light-harvesting antenna from an Antarctic alga

Abstract

Photosynthetic organisms thrive across remarkably diverse light environments, from dim, spectrally filtered habitats to high-irradiance niches. Their antenna complexes have evolved structural and excitonic features that tailor energy capture and delivery to local conditions, making comparative studies of noncanonical antennas essential for understanding the diversity of evolved designs. Here, we investigate the far-red light-harvesting complex from an Antarctic alga, Prasiola crispa (Pc-frLHC), whose ring-shaped undecameric (11-subunit) antenna absorbs strongly near ∼710 nm yet still drives photosystem II. Using femtosecond transient absorption with selective excitation of chlorophyll (Chl) b (645 nm), Chl a (675 nm), and far-red Chls (740 nm), we resolve a rapid, directional energy transfer cascade that funnels population into the lowest excitonic level of the far-red Chl trimer. Transient absorption anisotropy directly resolves a characteristic hopping time between the far-red Chl trimers of ∼11.5 ps, while exciton–exciton annihilation kinetics under increased fluence at far-red excitation provide independent corroboration. Spectral dynamics and anisotropy further reveal the existence of a higher-lying excitonic state near ∼670 nm within the far-red Chls. Thermal access to this ∼670 nm state enables repeated cycling that facilitates the uphill transfer toward Chl a despite a sizable energy gap of ∼580 cm−1. These findings clarify how Pc-frLHC exploits the excitonic coupling and the ring-mediated transport to harvest redshifted light for photosystem II excitation, offering general principles for engineering photofunctional systems adapted to spectrally limited environments.