Noncanonical Photodynamics of the Orange/Green Cyanobacteriochrome Power Sensor NpF2164g7 from the PtxD Phototaxis Regulator of Nostoc punctiforme

Forward and reverse primary (10 ns) photodynamics of cyanobacteriochrome (CBCR) NpF2164g7 were characterized by global analysis of ultrafast broadband transient absorption measurements. NpF2164g7 is the most C-terminal bilin-binding GAF domain in the Nostoc punctiforme phototaxis sensor PtxD (locus Npun_F2164). Although a member of the canonical red/green CBCR subfamily phylogenetically, NpF2164g7 exhibits an orange-absorbing 15Z Po dark-adapted state instead of the typical red-absorbing 15Z Pr dark-adapted state characteristic of this subfamily. The green-absorbing 15E Pg photoproduct of NpF2164g7 is unstable, allowing this CBCR domain to function as a power sensor. Photoexcitation of the 15Z Po state triggers inhomogeneous excited-state dynamics with three spectrally and temporally distinguishable pathways to generate the light-adapted 15E Pg state in high yield (estimated at 25–30%). Although observed in other CBCR domains, the inhomogeneity in NpF2164g7 extends far into secondary relaxation dynamics (10 ns −1 ms) through to formation of 15E Pg. In the reverse direction, the primary dynamics after photoexcitation of 15E Pg are qualitatively similar to those of other red/green CBCRs, but secondary dynamics involve a “pre-equilibrium” step before regenerating 15Z Po. The anomalous photodynamics of NpF2164g7 may reflect an evolutionary adaptation of CBCR sensors that function as broadband light intensity sensors.