Abstract
Microbial rhodopsin is a photoreceptor protein found in various bacteria and archaea, and it is considered to be a light-utilization device unique to heterotrophs. Recent studies have shown that several cyanobacterial genomes also include genes that encode rhodopsins, indicating that these auxiliary light-utilizing proteins may have evolved within photoautotroph lineages. To explore this possibility, we performed a large-scale genomic survey to clarify the distribution of rhodopsin and its phylogeny. Our surveys revealed a novel rhodopsin clade, cyanorhodopsin (CyR), that is unique to cyanobacteria. Genomic analysis revealed that rhodopsin genes show a habitat-biased distribution in cyanobacterial taxa, and that the CyR clade is composed exclusively of non-marine cyanobacterial strains. Functional analysis using a heterologous expression system revealed that CyRs function as light-driven outward H+ pumps. Examination of the photochemical properties and crystal structure (2.65 Å resolution) of a representative CyR protein, N2098R from Calothrix sp. NIES-2098, revealed that the structure of the protein is very similar to that of other rhodopsins such as bacteriorhodopsin, but that its retinal configuration and spectroscopic characteristics (absorption maximum and photocycle) are distinct from those of bacteriorhodopsin. These results suggest that the CyR clade proteins evolved together with chlorophyll-based photosynthesis systems and may have been optimized for the cyanobacterial environment.
Highlights
Microbial rhodopsin is a photoreceptor protein found in various bacteria and archaea, and it is considered to be a light-utilization device unique to heterotrophs
Various functions of rhodopsins have been found in prokaryotes, but they can be broadly separated into two types: (i) light sensors that work as phototaxis receptors and enzymes and (ii) ion pumps that use light energy to create an ion-motive force that can be used by cells as a type of intracellular
This fragmented evidence implies that rhodopsin-mediated photosystems may have evolved in the cyanobacterial lineage together with chlorophyll-based photosynthesis systems to allow for more efficient utilization of solar energy, the distribution of rhodopsin genes in the cyanobacterial lineage remains to be c larified[20]
Summary
Microbial rhodopsin is a photoreceptor protein found in various bacteria and archaea, and it is considered to be a light-utilization device unique to heterotrophs. Recent culture-independent surveys have shown that a diverse range of bacterial taxa, including several strains of cyanobacteria, have microbial rhodopsin (hereafter rhodopsin), which is a light-energy-harvesting device distinct from chlorophyll-based photosystems. This raises the possibility that rhodopsin-mediated photosystems have evolved in the cyanobacterial lineage. Most of the genes in the CyHR clade are possessed only by cyanobacteria; they have been found in a few marine b acteria[19] Together, this fragmented evidence implies that rhodopsin-mediated photosystems may have evolved in the cyanobacterial lineage together with chlorophyll-based photosynthesis systems to allow for more efficient utilization of solar energy, the distribution of rhodopsin genes in the cyanobacterial lineage remains to be c larified[20]
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