Ion-transporting mechanism in microbial rhodopsins: Mini-review relating to the session 5 at the 19th International Conference on Retinal Proteins

Yuji Furutani, Chii-Shen Yang
2023 Biophysics and Physicobiology  
Microbial rhodopsin is basically composed of seven transmembrane helices and binds an all-trans retinal as the chromophore through a protonated Schiff base linkage with a specific lysin residue on the seventh helix [1, 2] . Upon specific wavelength of light activation, isomerization of the retinal chromophore from all-trans to 13-cis configuration initiates the cyclic photoreaction (Figure 1a ). Initially, four kinds of microbial rhodopsins were found from an extremely halophilic archaeon,
more » ... acterium salinarum, and extensive studies were conducted; they are bacteriorhodpsin (BR), halorhodopsin (HR), sensory rhodopsin I (SRI), and sensory rhodopsin II (SRII). BR functions as an outward proton pump [3], while HR functions as inward chloride ion pump. They both are regarded as ion transporting rhodopsins. On the other hand, SRI and SRII each functions as light sensors regulating the positive and negative phototactic behavior of a bacterial cell, respectively. Since 2000, the metagenomic analysis opened new worlds of microbial rhodopsins in the ocean, fresh water, soils, etc. Nowadays, various kinds of functions, including but not limited to light-driven ion pump, light sensor, light-gated channel, light-regulated enzyme, and more are identified in new microbial rhodopsins (Figure 1b ) [2, 4] . In this brief review, ion-transporting rhodopsins are main focus. An outward proton-pumping rhodopsin generates proton gradient and forms electrochemical potential or proton mobile force (PMF) across the cell membrane, which is utilized by ATP synthase and flagellar motor for biological consumable energy generation. Thus, it is not so surprising that they were found from bacteria living in aquatic environments like salt lake and the ocean. One of the examples is proteorhodopsin (PR); it has been found from many ocean cyanobacteria and mainly contributes on the generation of bioenergy on the earth by harvesting light energy from the sun (~10 13 W) in addition to chlorophyll-based photosynthetic systems [2, 5] . Another interesting feature was found in xanthorhodopsin (XR), which binds a carotenoid as antenna capturing light energy and transferring the energy to the nearby retinal chromophore [6] . Although biological function remains elusive, a fungal pathogen (Leptosphaeria maculans) causing leaf disease of plant also possesses outward proton-pumping rhodopsin (LR) [7] . For unicellular organism, inward proton pump seems to be useless at first, because it dissipates the proton gradient and hence electrochemical potential or PMF utilized for living. When a single point mutation (D217E) of Anabaena sensory rhodopsin (ASR) produces inward proton-pumping activity [8, 9] , it was not anticipated that such inward proton pump exists in nature as ASR was considered a light sensor for regulating gene expression. But in 2016, the first inward proton pump in nature was found from a deep-ocean marine bacterium, Parvularcula oceani, and named as xenorhodopsin (XeR) [10] . Then in 2020, another inward proton pump, schizorhodopsin (SzR), was discovered from Asgard archaea, which is the archaeal group closest to eukaryotes [11] . It turns out those light-driven inward proton pump rhodopsins are widely distributed in nature. It had been widely believed that microbial rhodopsin possesses a single chromophore in monomer until XR, an outward proton pump, was found with a secondary chromophore, salinixanthine, which functions as antenna chromophore
doi:10.2142/biophysico.bppb-v20.s005 pmid:38362333 pmcid:PMC10865854 fatcat:4fu7lq2drjecrnoeck32pyocy4