Light-harvesting by antenna-containing xanthorhodopsin from an Antarctic 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 primitive thylakoid-less cyanobacterium Gloeobacter violaceus , where they facilitate light-driven outward proton pumping and enhanced light-harvesting. However, their distribution, binding specificity, and ecological significance in cyanobacteria remain poorly understood. Here we report widespread xanthorhodopsin genes in cyanobacterial genomes and characterize a protein from an Antarctic filamentous cyanobacterium that uniquely binds hydroxylated lutein. Through bioinformatics, spectroscopic, functional and structural assays analyses, we determine the properties and ecological role of this cyanobacterial xanthorhodopsin. Our findings highlight xanthorhodopsins' role in modulating light-harvesting efficiency in cyanobacteria, particularly in extreme environments. The lutein binding and associated structural changes likely provide selective advantages for adapting to polar light conditions, contributing to cyanobacterial survival in harsh habitats.