Light-driven proton transfers and proton transport by microbial rhodopsins – A biophysical perspective

Brown, Leonid S.

doi:10.1016/j.bbamem.2022.183867

Cited by 25 publications

(21 citation statements)

References 121 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…However, direct tracing of intra-protein displacements of protons in energy converting enzymes and chemical models (see [199,200,[207][208][209][210][211][212][213][214][215][216][217][218][219] for reviews) showed that fast proton transfer over a distance of up to 20 Å can be mediated by water bridges, provided that the distance between the groups involved is ≤ 3.0 Å, in accordance with Eigen [200]. Thereby it does not matter that water molecules are equally poor proton acceptors (with pKb of 0.0) and proton donors (with pKa of 14.0) because protons pass water by so-called von Grotthuss mechanism [220][221][222].…”

Section: Is Asp Wb An Universal Trap For a Proton From Wcat?mentioning

confidence: 99%

“…Replacement of Thr46 by a valine decreased the apparent pK of Asp96 by approximately two pH units [242], which may characterize the contribution of the H-bond between Thr46 and Asp96 to the unusually high apparent pK of the latter. The photoisomerization of the retinal twists the α-helices and lets water molecules in the space between them, see the pink structure [209,218,219,[243][244][245][246]247. The pK value of Asp-96 shifts to 7.1, which allows its deprotonation and proton transfer, via a transiently formed water chain, to the Schiff base of retinal at about 10 Å, see {Luecke, 2000 #3390, 248,249].…”

Section: Is Asp Wb An Universal Trap For a Proton From Wcat?mentioning

confidence: 99%

See 1 more Smart Citation

Common mechanism of activated catalysis in P-loop fold nucleoside triphosphatases -in varietate concordia

Kozlova

Shalaeva

Dibrova

2022

Preprint

View full text Add to dashboard Cite

Although P-loop fold nucleoside triphosphatases (also known as Walker NTPases) are ubiquitous, their catalytic mechanism remains obscure. Based on a comparative structural analysis of 3136 Mg-NTP-containing catalytic sites, we propose a common scheme of activated catalysis for P-loop NTPases where a hydrogen bond (H-bond) between the strictly conserved, Mg-coordinating Ser/Thr of the Walker A motif ([Ser/Thr]WA) and the conserved aspartate of the Walker B motif (AspWB) plays the key role. We found that this H-bond is very short in the structures with bound transition state (TS) analogs. We suggest that the proton affinities of these two residues reverse in the TS so that the proton relocates from [Ser/Thr]WA to AspWB. The anionic [Ser/Thr]WA withdraws then a proton from the (catalytic) water molecule, and the nascent hydroxyl anion attacks gamma-phosphate. When the gamma-phosphate group breaks away, the trapped proton relays from AspWB, via [Ser/Thr]WA, to beta-phosphate and compensates for its developing negative charge.

show abstract

Section: Is Asp Wb An Universal Trap For a Proton From Wcat?mentioning

confidence: 99%

Section: Is Asp Wb An Universal Trap For a Proton From Wcat?mentioning

confidence: 99%

Common mechanism of activated catalysis in P-loop fold nucleoside triphosphatases -in varietate concordia

Kozlova

Shalaeva

Dibrova

2022

Preprint

View full text Add to dashboard Cite

show abstract

“…It can be countered that the [Ser/Thr] K+1 –Asp WB pair does not interact directly with W cat . However, direct tracing of intra-protein displacements of protons in energy converting enzymes and chemical models (see [ 181 , 182 , 197 , 198 , 199 , 200 , 201 , 202 , 203 , 204 , 205 , 206 , 207 , 208 , 209 ] for reviews) showed that fast proton transfer over a distance of up to 20 Å can be mediated by water bridges, provided that the distance between the groups involved is ≤3.0 Å, in accordance with Eigen [ 182 ]. Thereby it does not matter that water molecules are equally poor proton acceptors (with pK b of 0.0) and proton donors (with pK a of 14.0) because protons pass water by the so-called von Grotthuss mechanism [ 210 , 211 , 212 ].…”

Section: Discussionmentioning

confidence: 99%

Common Mechanism of Activated Catalysis in P-loop Fold Nucleoside Triphosphatases—United in Diversity

et al. 2022

View full text Add to dashboard Cite

To clarify the obscure hydrolysis mechanism of ubiquitous P-loop-fold nucleoside triphosphatases (Walker NTPases), we analysed the structures of 3136 catalytic sites with bound Mg-NTP complexes or their analogues. Our results are presented in two articles; here, in the second of them, we elucidated whether the Walker A and Walker B sequence motifs—common to all P-loop NTPases—could be directly involved in catalysis. We found that the hydrogen bonds (H-bonds) between the strictly conserved, Mg-coordinating Ser/Thr of the Walker A motif ([Ser/Thr]WA) and aspartate of the Walker B motif (AspWB) are particularly short (even as short as 2.4 ångströms) in the structures with bound transition state (TS) analogues. Given that a short H-bond implies parity in the pKa values of the H-bond partners, we suggest that, in response to the interactions of a P-loop NTPase with its cognate activating partner (which are analysed in the first article, reference, Biomolecules-1832854), a proton relocates from [Ser/Thr]WA to AspWB. The resulting anionic [Ser/Thr]WA alkoxide withdraws a proton from the catalytic water molecule, and the nascent hydroxyl attacks the gamma phosphate of NTP. When the gamma-phosphate breaks away, the trapped proton at AspWB passes by the Grotthuss relay via [Ser/Thr]WA to beta-phosphate and compensates for its developing negative charge that is thought to be responsible for the activation barrier of hydrolysis.

show abstract

“…Most of these pigments function as light-driven ion transporters or ion channels ( Figure 7 ). The newly discovered xenorhodopsins and schizorhodopsins are exceptional as they perform inward-directed proton transport ( Inoue et al, 2018 ; Inoue et al, 2020 ; Weissbecker et al, 2021 ; Brown, 2022 ). However, some type-1 rhodopsins display a photosensory function (sensory rhodopsins) and signal via a cognate transducer protein, which is totally different functionally and structurally from the animal G-proteins ( Bogomolni and Spudich, 1991 ; Krah et al, 1994 ; Deininger et al, 1995 ).…”

Section: Functional Diversity Phylogenymentioning

confidence: 99%

“…A large number of excellent reviews on the rhodopsin families have been published, many of which we have referred to where appropriate, along with the most relevant early and recent papers. We refrain from presenting many molecular details, and therefore we refer to the following more recent reviews ( DeGrip and Rothschild, 2000 ; Hofmann, 2000 ; Spudich et al, 2000 ; Hofmann et al, 2009 ; Yizhar et al, 2011 ; Palczewski and Orban, 2013 ; Ernst et al, 2014 ; Imamoto and Shichida, 2014 ; Inoue et al, 2014 ; Deisseroth, 2015 ; Hofmann and Palczewski, 2015 ; Brown and Ernst, 2017 ; Bando et al, 2019 ; El Khatib and Atamian, 2019 ; Dowling, 2020 ; Kandori, 2020 ; Kwon et al, 2020 ; Baillie et al, 2021 ; Moraes et al, 2021 ; Rozenberg et al, 2021 ; Bondar, 2022 ; Broser, 2022 ; Brown, 2022 ; Khelashvili and Menon, 2022 ; Nagata and Inoue, 2022 ).…”

Section: Introductionmentioning

confidence: 99%

Rhodopsins: An Excitingly Versatile Protein Species for Research, Development and Creative Engineering

Grip

Ganapathy

2022

Front. Chem.

View full text Add to dashboard Cite

The first member and eponym of the rhodopsin family was identified in the 1930s as the visual pigment of the rod photoreceptor cell in the animal retina. It was found to be a membrane protein, owing its photosensitivity to the presence of a covalently bound chromophoric group. This group, derived from vitamin A, was appropriately dubbed retinal. In the 1970s a microbial counterpart of this species was discovered in an archaeon, being a membrane protein also harbouring retinal as a chromophore, and named bacteriorhodopsin. Since their discovery a photogenic panorama unfolded, where up to date new members and subspecies with a variety of light-driven functionality have been added to this family. The animal branch, meanwhile categorized as type-2 rhodopsins, turned out to form a large subclass in the superfamily of G protein-coupled receptors and are essential to multiple elements of light-dependent animal sensory physiology. The microbial branch, the type-1 rhodopsins, largely function as light-driven ion pumps or channels, but also contain sensory-active and enzyme-sustaining subspecies. In this review we will follow the development of this exciting membrane protein panorama in a representative number of highlights and will present a prospect of their extraordinary future potential.

show abstract

Light-driven proton transfers and proton transport by microbial rhodopsins – A biophysical perspective

Cited by 25 publications

References 121 publications

Common mechanism of activated catalysis in P-loop fold nucleoside triphosphatases -in varietate concordia

Common mechanism of activated catalysis in P-loop fold nucleoside triphosphatases -in varietate concordia

Common Mechanism of Activated Catalysis in P-loop Fold Nucleoside Triphosphatases—United in Diversity

Rhodopsins: An Excitingly Versatile Protein Species for Research, Development and Creative Engineering

Contact Info

Product

Resources

About