Structural Mechanism for Light-driven Transport by a New Type of Chloride Ion Pump, Nonlabens marinus Rhodopsin-3

Hosaka, Toshiaki; Yoshizawa, Susumu; Nakajima, Yu; Ohsawa, Noboru; Hato, Masakatsu; DeLong, Edward F.; Kogure, Kazuhiro; Yokoyama, Shigeyuki; Kimura‐Someya, Tomomi; Iwasaki, Wataru; Shirouzu, Mikako

doi:10.1074/jbc.m116.728220

Cited by 34 publications

(63 citation statements)

References 36 publications

(58 reference statements)

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“…25 Two X-ray structures of a representative of this group show that, similar to HRs, a chloride ion is coordinated by the first two members of the motif, Asn and Thr, and that the latter is more critical for chloride binding. 41,42 The detailed mechanism of chloride transport is not known, and the HR-like sequence of chloride uptake and release was suggested for some members of this group but not for the others. 40,43 Finally, the most recent addition to the ranks of anion transporting microbial rhodopsins is a distinct group of cyanobacterial light-driven anion pumps with the TSD motif.…”

Section: Introductionmentioning

confidence: 99%

Molecular details of the unique mechanism of chloride transport by a cyanobacterial rhodopsin

Harris

Saita

Resler

et al. 2018

Phys. Chem. Chem. Phys.

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Microbial rhodopsins are well known as versatile and ubiquitous light-driven ion transporters and photosensors. While the proton transport mechanism has been studied in great detail, much less is known about various modes of anion transport. Until recently, only two main groups of light-driven anion pumps were known, archaeal halorhodopsins (HRs) and bacterial chloride pumps (known as ClRs or NTQs). Last year, another group of cyanobacterial anion pumps with a very distinct primary structure was reported. Here, we studied the chloride-transporting photocycle of a representative of this new group, Mastigocladopsis repens rhodopsin (MastR), using time-resolved spectroscopy in the infrared and visible ranges and site-directed mutagenesis. We found that, in accordance with its unique amino acid sequence containing many polar residues in the transmembrane region of the protein, its photocycle features a number of unusual molecular events not known for other anion-pumping rhodopsins. It appears that light-driven chloride ion transfers by MastR are coupled with translocation of protons and water molecules as well as perturbation of several polar sidechains. Of particular interest is transient deprotonation of Asp-85, homologous to the cytoplasmic proton donor of light-driven proton pumps (such as Asp-96 of bacteriorhodopsin), which may serve as a regulatory mechanism.

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Section: Introductionmentioning

confidence: 99%

Molecular details of the unique mechanism of chloride transport by a cyanobacterial rhodopsin

Harris

Saita

Resler

et al. 2018

Phys. Chem. Chem. Phys.

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“…2A and SI Appendix, Fig. S1), which is conserved among H + -pumping microbial rhodopsins (7,19,20) and is also found in the Cl − pump Nonlabens marinus rhodopsin 3 (NM-R3) (21,22). The hydrated cavity on the intracellular side contains Gln123 of the NDQ motif, as well as Asn61, which plays a role in the ion selectivity (7,23).…”

Section: Significancementioning

confidence: 99%

Energetics and dynamics of a light-driven sodium-pumping rhodopsin

Suomivuori

Gámiz‐Hernández

Sundholm

et al. 2017

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

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The conversion of light energy into ion gradients across biological membranes is one of the most fundamental reactions in primary biological energy transduction. Recently, the structure of the first light-activated Na + pump, Krokinobacter eikastus rhodopsin 2 (KR2), was resolved at atomic resolution [Kato HE, et al. (2015) Nature 521: [48][49][50][51][52][53]. To elucidate its molecular mechanism for Na + pumping, we perform here extensive classical and quantum molecular dynamics (MD) simulations of transient photocycle states. Our simulations show how the dynamics of key residues regulate water and ion access between the bulk and the buried light-triggered retinal site. We identify putative Na + binding sites and show how protonation and conformational changes gate the ion through these sites toward the extracellular side. We further show by correlated ab initio quantum chemical calculations that the obtained putative photocycle intermediates are in close agreement with experimental transient optical spectroscopic data. The combined results of the ion translocation and gating mechanisms in KR2 may provide a basis for the rational design of novel light-driven ion pumps with optogenetic applications.bacterial ion pumps | bioenergetics | QM/MM | optogenetics | retinal P rimary biological energy conversion is based on the efficient capture and conversion of light and chemical energy into ion gradients across biological membranes (1, 2). The established gradients are used to thermodynamically drive energy-requiring processes, such as active transport and synthesis of adenosine triphosphate (ATP) (3, 4). The rhodopsin family of proteins catalyzes such reactions by harnessing the energy from retinal photoisomerization and deprotonation reactions, followed by conformational changes that further trigger the pumping of ions across the membrane (5). All previously known ion-pumping rhodopsins function either as inward chloride or outward proton pumps, but the structure of the first Na + pumping rhodopsin, Krokinobacter eikastus rhodopsin 2 (KR2) (6), was recently resolved (7,8). In the absence of Na + ions, KR2 functions as an outward proton pump, similarly to bacteriorhodopsin (bR), but under physiological conditions, KR2 pumps Na + out of the cell (6, 9).KR2 shares the heptahelical transmembrane (7TM) structure common to all microbial rhodopsins (Fig. 1A) (5,7,8). In contrast to bR, however, where a highly conserved Asp-Thr-Asp (DTD) motif is used to pump protons, KR2 employs a unique NDQ motif comprising residues Asn112, Asp116, and Gln123 (6). In bR, Asp85 and Asp96 function as proton acceptors and donors for the protonated Schiff base (PSB), respectively, whereas in KR2, Asn112 and Gln123 occupy these positions, and Asp116 replaces Thr89. In analogy to bR, it has been suggested that Gln123 aids in capturing ions from the solvent and that Asn112 might be part of a Na + binding site (6,10).Similarly to other microbial rhodopsins, four photocycle intermediates have been spectroscopically identified in KR2 (Fig. 1B) (6)...

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“…The common feature of CIR and HR is that the Schiff base remains protonated throughout the pumping cycle whereas Cl − uptake kinetics differs (31). A crystal structure of the CIR from Nonlabens marinus shows greater similarity to the structure of the light-driven Na + pump KR2 (32) than to those of archaeal ion pumps, consistent with convergent evolution of Cl − -pumping within the archaeal and eubacterial type 1 rhodopsin subfamilies.…”

Section: The Known Molecular Functions Of Microbial Rhodopsinsmentioning

confidence: 82%

Microbial Rhodopsins: Diversity, Mechanisms, and Optogenetic Applications

Govorunova

Sineshchekov

et al. 2017

Annu. Rev. Biochem.

283

294

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Microbial rhodopsins are a family of photoactive retinylidene proteins widespread throughout the microbial world. They are notable for their diversity of function, using variations of a shared seven-transmembrane helix design and similar photochemical reactions to carry out distinctly different light-driven energy and sensory transduction processes. Their study has contributed to our understanding of how evolution modifies protein scaffolds to create new protein chemistry, and their use as tools to control membrane potential with light is fundamental to the transformative technology of optogenetics. We review the currently known functions, and present more in-depth assessment of three functionally and structurally distinct types discovered over the past two years: (i) anion-conducting channelrhodopsins (ACRs) from cryptophyte algae, enabling efficient optogenetic neural suppression, (ii) cryptophyte cation-conducting channelrhodopsins (CCRs), structurally distinct from the green algae CCRs used extensively for neural activation, and (iii) enzymerhodopsins, with light-gated guanylylcyclase or kinase activity promising for optogenetic control of signal transduction.

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Structural Mechanism for Light-driven Transport by a New Type of Chloride Ion Pump, Nonlabens marinus Rhodopsin-3

Cited by 34 publications

References 36 publications

Molecular details of the unique mechanism of chloride transport by a cyanobacterial rhodopsin

Molecular details of the unique mechanism of chloride transport by a cyanobacterial rhodopsin

Energetics and dynamics of a light-driven sodium-pumping rhodopsin

Microbial Rhodopsins: Diversity, Mechanisms, and Optogenetic Applications

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