The multitalented microbial sensory rhodopsins

doi:10.1016/j.tim.2006.09.005

Trends in Microbiology

Volume 14, Issue 11, November 2006, Pages 480-487

https://doi.org/10.1016/j.tim.2006.09.005 Get rights and content

Sensory rhodopsins are photoactive, membrane-embedded seven-transmembrane helix receptors that use retinal as a chromophore. They are widespread in the microbial world in each of the three domains of life: Archaea, Bacteria and Eukarya. A striking characteristic of these photoreceptors is their different modes of signaling in different organisms, including interaction with other membrane proteins, interaction with cytoplasmic transducers and light-controlled Ca²⁺ channel activity. More than two decades since the discovery of the first sensory rhodopsins in the archaeon Halobacterium salinarum, genome projects have revealed a widespread presence of homologous photosensors. New work on cyanobacteria, algae, fungi and marine proteobacteria is revealing how evolution has modified the common design of these proteins to produce a remarkably rich diversity in their signaling biochemistry.

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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Protein motions visualized by femtosecond time-resolved crystallography: The case of photosensory vs photosynthetic proteins
2022, Current Opinion in Structural Biology
Proteins are dynamic objects and undergo conformational changes when functioning. These changes range from interconversion between states in equilibrium to ultrafast and coherent structural motions within one perturbed state. Time-resolved serial femtosecond crystallography at free-electron X-ray lasers can unravel structural changes with atomic resolution and down to femtosecond time scales. In this review, we summarize recent advances on detecting structural changes for phytochrome photosensor proteins and a bacterial photosynthetic reaction center. In the phytochrome structural changes are extensive and involve major rearrangements of many amino acids and water molecules, accompanying the regulation of its biochemical activity, whereas in the photosynthetic reaction center protein the structural changes are smaller, more localized, and are optimized to facilitate electron transfer along the chromophores. The detected structural motions underpin the proteins’ function, providing a showcase for the importance of detecting ultrafast protein structural dynamics.
Coregulation of gene expression by White collar 1 and phytochrome in Ustilago maydis
2021, Fungal Genetics and Biology
Ustilago maydis encodes ten predicted light-sensing proteins. The biological functions of only a few of them are elucidated. Among the characterized ones are two DNA-photolyases and two rhodopsins that act as DNA-repair enzymes or green light-driven proton pumps, respectively. Here we report on the role of two other photoreceptors in U. maydis, namely White collar 1 (Wco1) and Phytochrome 1 (Phy1). We show that they bind flavins or biliverdin as chromophores, respectively. Both photoreceptors undergo a photocycle in vitro. Wco1 is the dominant blue light receptor in the saprophytic phase, controlling all of the 324 differentially expressed genes in blue light. U. maydis also responds to red and far-red light. However, the number of red or far-red light-controlled genes is less compared to blue light-regulated ones. Moreover, most of the red and far-red light-controlled genes not only depend on Phy1 but also on Wco1, indicating partial coregulation of gene expression by both photoreceptors. GFP-fused Wco1 is preferentially located in the nucleus, Phy1 in the cytosol, thus providing no hint that these photoreceptors directly interact or operate within the same complex. This is the first report on a functional characterization and coaction of White collar 1 and phytochrome orthologs in basidiomycetes.
Expression of Anabaena sensory rhodopsin is influenced by different codons of seven residues at the N-terminal region
2018, Protein Expression and Purification
Microbial rhodopsins are well-known seven-transmembrane proteins that have been extensively studied for their structure and function. These retinal-binding proteins can be divided into two types. Type I is microbial rhodopsin, and type II (visual pigment) is expressed mostly in mammalian eyes. The two primary functions of type I rhodopsin are ion pumping activity and sensory transduction. Anabaena sensory rhodopsin (ASR) is a microbial rhodopsin with a specific function of photosensory transduction. ASR is expressed at moderate levels in Escherichia coli, but its expression level is lower compared to the general green light absorbing proteorhodopsin (GPR). In this study, full-length ASR was used to test the influence of codon usage on expression E. coli. Seven amino acids at the N-terminal region of ASR after the Met start codon were changed randomly using designed primers, which allowed for 8192 different nucleotide combinations. The codon changes were screened for the preferable codons that resulted in higher expression yield. Among the 57 selected mutations, 24 color-enhanced E. coli colonies contained ASR proteins, and they expressed ASR at a higher level than the bacteria with wild-type ASR codon usage. This result strongly suggests that the specific codon usage of only the N-terminal portion of a protein can increase the expression level of the entire protein.
A Guide to Optogenetic Applications, With Special Focus on Behavioral and In Vivo Electrophysiological Experiments
2018, Handbook of Behavioral Neuroscience
This chapter gives detailed instructions for setting up and running optogenetic experiments. It starts with a comprehensive overview of optogenetic methods and their constraints and advantages as a methodological approach. Different optogenetic tools, such as microbial opsins and light-activated G protein–coupled receptors, are introduced and discussed in terms of their feasibility. At the end of this section, state-of-the-art optogenetic stimulation devices are reviewed. This is followed by a detailed description of all necessary prerequisites to plan and execute optogenetic behavioral and electrophysiological experiments in mice. On this basis, the subsequent section gives concrete advice on troubleshooting and execution of optogenetic experiments. At the end of the chapter, a research perspective on optogenetic applications in neuroscience is provided.
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Optogenetics is a fast developing science that combines gene biology and optics to new research fields in neuroscience and cell biology. In the introduction a short literature update of optogenetic tools is given with some emphasis on rhodopsin and flavin based optogenetic tools. Then the BLUF coupled photoactivated adenylyl cyclases (PACs) are discussed (BLUF = Blue Light sensor Using FAD). The primary photo-dynamics of the BLUF domains is described. A BLUF domain photocycle scheme and a BLUF domain reaction coordinate scheme are presented. The adenylyl cyclase action of catalytic ATP to cAMP (a cellular second messenger) conversion is described. Light-induced cyclase activity of BLUF coupled photoactivated adenylyl cyclases (BLUF-PACs) is analyzed. Optogenetic BLUF-PAC applications are shortly reviewed.
A Proteorhodopsin-Related Photosensor Expands the Repertoire of Structural Motifs Employed by Sensory Rhodopsins
2023, Journal of Physical Chemistry B

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Trends in Microbiology

ReviewThe multitalented microbial sensory rhodopsins

Section snippets

The expanding family of rhodopsins in microorganisms

Prokaryotic phototaxis receptors: signaling to membrane-embedded transducers

Signal relay in the SRII–HtrII complex from Natronomonas pharaonis

Anabaena sensory rhodopsin: signaling to a soluble cytoplasmic transducer

Chlamydomonas photomotility receptors: signaling by ion-channel activation

Marine sensory proteorhodopsins: the oceans are a cauldron for microbial rhodopsin genes

Concluding remarks and future perspectives

Update

Acknowledgements

Glossary

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FEBS Lett.

J. Biol. Chem.

J. Biol. Chem.

Curr. Opin. Struct. Biol.

Biochim. Biophys. Acta

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J. Biol. Chem.

Biophys. J.

Trends Plant Sci.

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Biophys. J.

Curr. Biol.

Neuron

J. Biol. Chem.

Curr. Opin. Struct. Biol.

Control of transmembrane ion fluxes to select halorhodopsin-deficient and other energy transduction mutants of Halobacterium halobium

Proc. Natl. Acad. Sci. U. S. A.

Identification of a third rhodopsin-like pigment in phototactic Halobacterium halobium

Proc. Natl. Acad. Sci. U. S. A.

Functions of a new photoreceptor membrane

Proc. Natl. Acad. Sci. U. S. A.

Retinylidene proteins: structures and functions from Archaea to humans

Annu. Rev. Cell Dev. Biol.

New insights into the evolutionary history of type 1 rhodopsins

J. Mol. Evol.

Microbial rhodopsins: phylogenetic and functional diversity

Fungal rhodopsins and opsin-related proteins: eukaryotic homologues of bacteriorhodopsin with unknown functions

Photochem. Photobiol. Sci.

Molecular mechanism of photosignaling by archaeal sensory rhodopsins

Annu. Rev. Biophys. Biomol. Struct.

Photochemistry and photoinduced proton-transfer by pharaonis phoborhodopsin

Biochemistry (Mosc.)

The mechanism of colour discrimination by a bacterial sensory rhodopsin

Nature

The genome of Salinibacter ruber: convergence and gene exchange among hyperhalophilic bacteria and archaea

Proc. Natl. Acad. Sci. U. S. A.

Xanthorhodopsin: a proton pump with a light-harvesting carotenoid antenna

Science

Crystal structure of sensory rhodopsin II at 2.4 Å: insights into color tuning and transducer interaction

Science

X-ray structure of sensory rhodopsin II at 2.1-Å resolution

Proc. Natl. Acad. Sci. U. S. A.

Review
The multitalented microbial sensory rhodopsins