Trends in Microbiology
ReviewThe multitalented microbial sensory rhodopsins
Section snippets
The expanding family of rhodopsins in microorganisms
Photoactive membrane-embedded retinylidene proteins (rhodopsins) are used throughout the animal and microbial kingdoms as receptors for light. In the late 1930s, the first rhodopsin photosensors were characterized in photosensitive membranes in bovine eyes and were demonstrated to be ubiquitous in animal visual systems. Half a century later, the first microbial sensory rhodopsin, a protein now called sensory rhodopsin I (SRI; see Glossary), was discovered in a search for receptors that mediated
Prokaryotic phototaxis receptors: signaling to membrane-embedded transducers
Sensory rhodopsins I and II (Figure 1) form 2:2 complexes in haloarchaeal membranes with their cognate transducers, HtrI and HtrII, respectively (Figure 2) 9, 10, 11. The transducers, which are homologous to bacterial chemotaxis receptors, contain two transmembrane helices and a large cytoplasmic domain that, at its distal end, binds to the histidine kinase CheA. The SR–Htr complexes modulate the CheA kinase activity, thereby controlling the extent of phosphorylation of a cytoplasmic
Signal relay in the SRII–HtrII complex from Natronomonas pharaonis
From atomic-resolution structures of dark SRII 15, 16 and time-resolved Fourier transform infrared spectroscopy (FTIR) of the photoproducts 17, 18, 19, 20, 21, 22, the photoactivation of the Natronomonas pharaonis SRII–HtrII repellent receptor is the best characterized among sensory rhodopsins in terms of the chemical events induced by retinal photoisomerization 23, 24, 25. Much current research is focused on the next step, namely how the receptor signal is relayed to the transducer. The signal
Anabaena sensory rhodopsin: signaling to a soluble cytoplasmic transducer
The first eubacterial sensory rhodopsin to be identified was Anabaena sensory rhodopsin (ASR) from the freshwater cyanobacterium Anabaena sp. PCC7120. ASR interacts with a partner protein that is very different from the haloarchaeal phototaxis transducers [38]. The receptor is encoded in an operon along with a second gene that encodes a small soluble cytoplasmic protein, recently named ASR transducer (ASRT) [39]. The co-expression of ASR and ASRT in Escherichia coli accelerates the ASR
Chlamydomonas photomotility receptors: signaling by ion-channel activation
The Chlamydomonas photomotility receptors are the only identified eukaryotic microbial rhodopsins for which a function in the cell has been established [45], although strong evidence from heterologously expressed protein indicates that another eukaryotic microbial rhodopsin also functions as a light-driven proton pump in the fungus Leptosphaeria maculans [46]. (Proton-pumping activity has also been observed in Acetabularia rhodopsin expressed in Xenopus oocytes but the authors note that the
Marine sensory proteorhodopsins: the oceans are a cauldron for microbial rhodopsin genes
The largest number of microbial rhodopsin genes have been found by environmental sequencing of ocean samples. The first microbial rhodopsin-encoding gene in the ocean was discovered on a genome fragment derived from an uncultured marine γ-proteobacterium of the SAR86 group and was shown to be a light-driven proton pump 58, 59. The encoded protein was named proteorhodopsin (PR). Subsequently, homologous PR-encoding genes have been detected in marine plankton by the use of PCR-based gene surveys
Concluding remarks and future perspectives
Microbial rhodopsins are present in all three domains of life and, therefore, progenitors of these proteins could have existed in early evolution before the divergence of the Archaea, Bacteria and Eukarya (for a discussion, see Refs 4, 8). Light-driven ion transport as a means of obtaining cellular energy might well have predated the development of photosynthesis, and could represent one of the earliest means by which organisms tapped solar radiation as an energy source. Microbial sensory
Update
A recent article by Sudo and Spudich [69] reports that when three residues in bacteriorhodopsin (BR) are replaced by the corresponding residues in SRII, BR efficiently relays the retinal photoisomerization signal to the SRII integral membrane transducer HtrII and induces robust phototaxis responses. A single replacement (Ala215Thr), which bridges the retinal and membrane-embedded surface residues, confers weak phototaxis signaling activity, and two additional replacements (surface substitutions
Acknowledgements
The author is grateful to Elena Spudich and Oleg Sineshchekov for discussion and critical reading of the manuscript. Ranga Partha and the author carried out the analysis of proteorhodopsin sequences to identify sensory proteorhodopsins. Work referenced from the author's laboratory was supported by the National Institutes of Health, the National Science Foundation, the Human Frontiers in Science Program and the Robert A. Welch Foundation.
Glossary
- ASR
- sensory rhodopsin in the cyanobacterium Anabaena sp. PCC7120.
- ASRT
- putative transducer for ASR signals.
- BR
- bacteriorhodopsin, a light-driven proton pump in haloarchaea; the first-discovered transport rhodopsin.
- CSRA
- Chlamydomonas reinhardtii sensory rhodopsin A, a phototaxis–photophobic response receptor also known as channelrhodopsin-1.
- CSRB
- Chlamydomonas reinhardtii sensory rhodopsin B, a phototaxis–photophobic response receptor also known as channelrhodopsin-2.
- HR
- halorhodopsin, a light-driven
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