Light-harvesting by antenna-containing xanthorhodopsin from an Antarctic Pseudanabaenaceae cyanobacterium

Microbial rhodopsins are light-sensitive proteins vital to various phototrophic and sensory processes in microorganisms. Xanthorhodopsins, with their dual chromophore system involving retinal and carotenoids, have been predominantly studied in the extreme halophilic bacterium Salinibacter ruber and in the early-branching thylakoid-less cyanobacterium Gloeobacter violaceus, where they facilitate light-driven outward proton pumping. However, their distribution, binding specificity, and ecological significance in cyanobacteria remain poorly understood. Here we report the incidence of xanthorhodopsin genes in cyanobacterial genomes and characterize psXR, a xanthorhodopsin from an uncultured Antarctic cyanobacterium from the filamentous family of Pseudanabaenaceae that binds a hydroxylated carotenoid antenna. Through bioinformatic, spectroscopic, functional and structural analyses, we determine the properties of psXR and potential physiological roles of cyanobacterial xanthorhodopsins. Our findings suggest xanthorhodopsins' role in modulating light-harvesting efficiency in cyanobacteria, particularly in extreme environments. The antenna binding and associated structural changes likely provide selective advantages for adapting to polar light conditions such as prolonged low light intensities and spectral shifts, contributing to cyanobacterial survival in harsh habitats.