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

Forward and reverse primary (<10 ns) and secondary (>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 15ZPo dark-adapted state instead of the typical red-absorbing 15ZPr dark-adapted state characteristic of this subfamily. The green-absorbing 15EPg photoproduct of NpF2164g7 is unstable, allowing this CBCR domain to function as a power sensor. Photoexcitation of the 15ZPo state triggers inhomogeneous excited-state dynamics with three spectrally and temporally distinguishable pathways to generate the light-adapted 15EPg 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 15EPg. In the reverse direction, the primary dynamics after photoexcitation of 15EPg are qualitatively similar to those of other red/green CBCRs, but secondary dynamics involve a "pre-equilibrium" step before regenerating 15ZPo. The anomalous photodynamics of NpF2164g7 may reflect an evolutionary adaptation of CBCR sensors that function as broadband light intensity sensors.