Retinal to Retinal Energy Transfer in a Bistable Microbial Rhodopsin Dimer.

Neorhodopsin (NeoR) is a newly discovered fungal bistable rhodopsin that reversibly photoswitches between UV- and near-IR absorbing states denoted NeoR and NeoR, respectively. NeoR represents a deprotonated retinal Schiff base (RSB), while NeoR represents a protonated RSB. Cryo-EM studies indicate that NeoR forms homodimers with 29 Å center-to-center distance between the retinal chromophores. UV excitation of NeoR takes place to an optically allowed S3 state of 1B symmetry, which rapidly converts to a low-lying optically forbidden S1 state of 2A symmetry in 39 fs, followed by a multiexponential decay to the ground state on the 1-100 ps time scale. A theoretically predicted nπ* (S2) state does not get populated in any appreciable transient concentration during the excited-state relaxation cascade. We observe an intradimer retinal to retinal excitation energy transfer (EET) process from the NeoR S1 state to NeoR, in competition with photoproduct formation. To quantitatively assess the EET mechanism and rate, we experimentally addressed and modeled the EET process under varying NeoR-NeoR photoequilibrium conditions and determined the EET rate at (200 ps). The NeoR S1 state shows a weak stimulated emission band in the near-IR around 700 nm, which may result from mixing with an intramolecular charge-transfer (ICT) state, enhancing the transition dipole moment of the S1-S0 transition and possibly facilitating the EET process. We suggest that EET may bear general relevance to the function of bistable multiwavelength rhodopsin oligomers.