Carotenoids bind rhodopsins and act as photocycle-accelerating pigments in marine Bacteroidota

Abstract

Microbial rhodopsins are photoreceptor proteins widely distributed in marine microorganisms that harness light energy and support marine ecosystems. While retinal is typically the sole chromophore in microbial rhodopsins, some proteorhodopsins, which are proton-pumping rhodopsins abundant in the ocean, use carotenoid antennae to transfer light energy to retinal. However, the mechanism by which carotenoids enhance rhodopsin functions remains unclear. Here, using the marine Bacteroidota isolate Nonlabens marinus S1-08T, we reconstituted complexes of rhodopsins with the carotenoid myxol and detected energy transfer to retinal in both proteorhodopsin and chloride ion-pumping rhodopsin. Carotenoid binding facilitated light harvesting and accelerated the photocycle, thereby improving the light utilization efficiency of proteorhodopsin. Cryogenic electron microscopy structural analysis further revealed the molecular architecture of the carotenoid–rhodopsin complexes. The ability to bind carotenoids is conserved in rhodopsins of the marine-dominant phylum Bacteroidota, which are widely transcribed in the photic zone. These findings reveal how carotenoids enhance rhodopsin functions in marine Bacteroidota. In marine bacteria, carotenoids enhance rhodopsin function by acting as light-harvesting antennae and photocycle-accelerating pigments, a dual mechanism that enhances light energy capture and expands the known strategies of microbial phototrophy.