Rhodopsin-bestrophin fusion proteins from unicellular algae form gigantic pentameric ion channels

Rozenberg, Andrey; Kaczmarczyk, Igor; Matzov, Donna; Vierock, Johannes; Nagata, Takashi; Sugiura, Masahiro; Katayama, Kota; Kawasaki, Yuma; Konno, Masae; Nagasaka, Yujiro; Aoyama, Mako; Das, Ishita; Pahima, Efrat; Church, Jonathan R.; Adam, Suliman; Borin, Veniamin; Chazan, Ariel; Augustin, Sandra; Wietek, Jonas; Dine, Julien; Peleg, Yoav; Kawanabe, Akira; Fujiwara, Yuichiro; Sheves, Mordechai; Schapiro, Igor; Furutani, Yuji; Kandori, Hideki; Inoue, Kazuhide; Hegemann, Peter; Béjà, Oded; Shalev-Benami, Moran

doi:10.1038/s41594-022-00783-x

Cited by 30 publications

(41 citation statements)

References 111 publications

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“…Microbial rhodopsins are categorized into different functional subgroups, including light-driven ion pumps, light-gated ion channels, light sensors, and light-activated enzymes, − while animal rhodopsins are G protein-coupled receptors. , Microbial and animal rhodopsins possess retinal chromophores that capture light and isomerize from all- trans to 13- cis and from 11 -cis to all- trans -retinal, respectively . Although this selection has been unique for each class, a recently discovered microbial rhodopsin, bestrhodopsin, offered two surprising photochemical properties . Bestrhodopsin is a novel microbial rhodopsin subfamily from marine unicellular algae, in which one or two rhodopsin domains are fused to a bestrophin channel (also called RB or RRB, respectively) and function as light-gated ion channels.…”

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confidence: 99%

“…Bestrhodopsin is a novel microbial rhodopsin subfamily from marine unicellular algae, in which one or two rhodopsin domains are fused to a bestrophin channel (also called RB or RRB, respectively) and function as light-gated ion channels. The first surprise was that bestrhodopsin performs an all- trans to 11- cis photoisomerization . The second surprise in its photochemistry was the lack of photoreaction at low temperatures.…”

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confidence: 99%

“…Light-induced formation of the 11- cis form in bestrhodopsin is unique for microbial rhodopsins, whereas it is not surprising for animal rhodopsins, as retinochrome performs all- trans to 11- cis photoisomerization. , In contrast, 7- cis retinal is not known in nature . How is photoisomerization from all- trans to 7- cis form possible?…”

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confidence: 99%

“…Primary intermediates of rhodopsins can normally be trapped at 77 K in a frozen protein environment . Barrierless or very low barrier photoisomerization in the excited states of animal and microbial rhodopsins, respectively, explain these experimental observations well. , In contrast, the lack of photoreaction in bestrhodopsin at <170 K raised a question about the origin of the potential barrier . Selective isomerization into the 11- cis form, and not into 13- cis form, in bestrhodopsin suggests a very high potential barrier along the C 13 C 14 bond rotation coordinate, while that along the C 11 C 12 bond rotation must be lower but still high enough to produce the observed temperature dependence.…”

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confidence: 99%

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Unusual Photoisomerization Pathway in a Near-Infrared Light Absorbing Enzymerhodopsin

Sugiura

Ishikawa

Katayama

et al. 2022

J. Phys. Chem. Lett.

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Microbial and animal rhodopsins possess retinal chromophores which capture light and normally photoisomerize from all-trans to 13-cis and from 11-cis to all-trans-retinal, respectively. Here, we show that a near-infrared light-absorbing enzymerhodopsin from Obelidium mucronatum (OmNeoR) contains the all-trans form in the dark but isomerizes into the 7-cis form upon illumination. The photoproduct (λmax = 372 nm; P372) possesses a deprotonated Schiff base, and the system exhibits a bistable nature. The photochemistry of OmNeoR was arrested at <270 K, indicating the presence of a potential barrier in the excited state. Formation of P372 is accompanied by protonation changes of protonated carboxylic acids and peptide backbone changes of an α-helix. Photoisomerization from the all-trans to 7-cis retinal conformation rarely occurs in any solvent and protein environments; thus, the present study reports on a novel photochemistry mediated by a microbial rhodopsin, leading from the all-trans to 7-cis form selectively.

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confidence: 99%

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confidence: 99%

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confidence: 99%

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confidence: 99%

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Unusual Photoisomerization Pathway in a Near-Infrared Light Absorbing Enzymerhodopsin

Sugiura

Ishikawa

Katayama

et al. 2022

J. Phys. Chem. Lett.

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“…Only a small fraction of protist rhodopsins have been characterized at any level beyond their primary structure, and further characterization will likely bring many striking discoveries. A recent example are algal rhodopsins that act as photosensitive domains to regulate a pentameric bestrophin channel (42).…”

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confidence: 99%

Structural foundations of potassium selectivity in channelrhodopsins

Govorunova

Sineshchekov

Brown

et al. 2022

Preprint

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Kalium channelrhodopsins (KCRs) are light-gated K+ channels recently found in the stramenopile protist Hyphochytrium catenoides. When expressed in neurons, KCRs enable high-precision optical inhibition of spiking (optogenetic silencing). KCRs are capable of discriminating K+ from Na+ without the conventional K+-selectivity filter found in classical K+ channels. The genome of H. catenoides also encodes a third paralog that is more permeable for Na+ than for K+. To identify structural motifs responsible for the unusual K+ selectivity of KCRs, we systematically analyzed a series of chimeras and mutants of this protein. We found that mutations of three critical residues in the paralog convert its Na+ selective channel into a K+ selective one. Our characterization of homologous proteins from other protists (Colponema vietnamica, Cafeteria burkhardae and Chromera velia) and metagenomic samples confirmed the importance of these residues for K+ selectivity. We also show that Trp102 and Asp116, conserved in all three H. catenoides orthologs, are necessary, although not sufficient, for K+ selectivity. Our results provide the foundation for further engineering of KCRs for optogenetic needs.

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Angstrom‐Scale 2D Channels Designed For Osmotic Energy Harvesting

Ding,

Gu,

Zhang

et al. 2024

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Confronting the impending exhaustion of traditional energy, it is urgent to devise and deploy sustainable clean energy alternatives. Osmotic energy contained in the salinity gradient of the sea‐river interface is an innovative, abundant, clean, and renewable osmotic energy that has garnered considerable attention in recent years. Inspired by the impressively intelligent ion channels in nature, the developed angstrom‐scale 2D channels with simple fabrication process, outstanding design flexibility, and substantial charge density exhibit excellent energy conversion performance, opening up a new era for osmotic energy harvesting. However, this attractive research field remains fraught with numerous challenges, particularly due to the complexities associated with the regulation at angstrom scale. In this review, the latest advancements in the design of angstrom‐scale 2D channels are primarily outlined for harvesting osmotic energy. Drawing upon the analytical framework of osmotic power generation mechanisms and the insights gleaned from the biomimetic intelligent devices, the design strategies are highlighted for high‐performance angstrom channels in terms of structure, functionalization, and application, with a particular emphasis on ion selectivity and ion transport resistance. Finally, current challenges and future prospects are discussed to anticipate the emergence of more anomalous properties and disruptive technologies that can promote large‐scale power generation.

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Rhodopsin-bestrophin fusion proteins from unicellular algae form gigantic pentameric ion channels

Cited by 30 publications

References 111 publications

Unusual Photoisomerization Pathway in a Near-Infrared Light Absorbing Enzymerhodopsin

Unusual Photoisomerization Pathway in a Near-Infrared Light Absorbing Enzymerhodopsin

Structural foundations of potassium selectivity in channelrhodopsins

Angstrom‐Scale 2D Channels Designed For Osmotic Energy Harvesting

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