Eukaryotic G protein-coupled receptors as descendants of prokaryotic sodium-translocating rhodopsins

Shalaeva, Daria N.; Galperin, Michael Y.

doi:10.1186/s13062-015-0091-4

Cited by 45 publications

(46 citation statements)

References 98 publications

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“…Biologists have been seeking evidence to solve the long‐standing question of the common ancestry of these two highly diverged superfamilies of seven transmembrane sensory proteins, rhodopsins, and bacteriorhodopsins. Shalaeva et al () propose a common ancestry for sodium‐translocating bacteriorhodopsins and various sodium ion‐binding GPCRs, given their common ability to bind sodium ions (Shalaeva et al ). Depending on how limited the functionality of rhodopsin‐like GPCRs in dinoflagellates is, the prevalence of proteorhodopsins may point toward their complementary function as energy generators.…”

Section: Discussionmentioning

confidence: 99%

Comparative transcriptomics supports the presence of G protein‐coupled receptor‐based signaling in unicellular marine eukaryotes

Mojib

Kubanek

2019

Limnology & Oceanography

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Being abundant primary producers, single-celled eukaryotic diatoms and dinoflagellates dominate marine food webs and significantly impact the ecology of the oceans. These organisms face competition and predation which have contributed to the evolution of chemical defenses and their ability to sense chemical cues. Elucidating how these chemical cues are perceived by organisms requires identification of proteins involved in relaying chemical information to cells. The functions of G protein-coupled receptor (GPCR) signaling diversified over evolutionary time in multicellular organisms, but the role that GPCR signaling plays in unicellular eukaryotes remains largely unknown. Using comparative transcriptomic analysis, we identified repertoires of GPCR signaling proteins from 81 diatom and 36 dinoflagellate transcriptomes. Diatoms and dinoflagellates express putative GPCRs that are highly diverged from known metazoan GPCRs along with well-conserved core components of GPCR signaling pathways. Unlike other eukaryotes that express multiple classes of GPCRs, diatoms and dinoflagellates were each found to express a single, major class of putative GPCRs with greatest similarity to class C and rhodopsin-like GPCRs, respectively. Furthermore, only 4.2% of the GPCR-like transcripts from dinoflagellates were predicted to be true GPCRs compared to 48% in diatoms. These results suggest that further expansion of GPCRs did not take place within each of these two major phytoplankton groups, and that dinoflagellate GPCRs are more divergent from known GPCRs than are diatom GPCRs. Our results provide additional evidence for the global existence of relatively ancestral GPCR signaling machinery in marine phytoplankton.

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Section: Discussionmentioning

confidence: 99%

Comparative transcriptomics supports the presence of G protein‐coupled receptor‐based signaling in unicellular marine eukaryotes

Mojib

Kubanek

2019

Limnology & Oceanography

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“…Moreover, in 2015 the evolutional relationship of microbial light-driven Na + pumps and class A G protein-coupled receptors (GPCRs) was studied, based on the existing structures of the ground state of KR2 55 . Presented here structure of the O-state with Na + bound inside the protein supports the high similarity of the Na + binding sites in KR2 and GPCRs.…”

Section: Supplementary Textmentioning

confidence: 99%

Molecular mechanism of light-driven sodium pumping

Kovalev

Astashkin

Gushchin

et al. 2020

Preprint

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ABSTRACTMicrobial rhodopsins appeared to be the most abundant light-harvesting proteins on the Earth and are the major contributes to the solar energy captured in the sea. They possess highly diverse biological functions. Explosion of research on microbial rhodopsins led to breakthroughs in their applications, in particular, in neuroscience.An unexpected new discovery was a Na+-pumping KR2 rhodopsin from Krokinobacter eikastus, the first light-driven non-proton cation pump. A fundamental difference between proton and other cation pumps is that non-proton pumps cannot use tunneling or Grotthuss mechanism for the ion translocation and, therefore, Na+ pumping cannot be understood in the framework of classical proton pump, like bacteriorhodopsin. Extensive studies on the molecular mechanism of KR2 failed to reveal mechanism of pumping. The existing high-resolution structures relate only to the ground state of the protein and revealed no Na+ inside the protein, which is unusual for active ion transporters.KR2 is only known non proton cation transporter with demonstrated remarkable potential for optogenetic applications and, therefore, elucidation of the mechanism of cation transport is important. To understand conception of cation pumping we solved crystal structures of the functionally key O-intermediate state of physiologically relevant pentameric form of KR2 and its D116N and H30A key mutants at high resolution and performed additional functional studies.The structure of the O-state reveals a sodium ion near the retinal Schiff base coordinated by N112 and D116 residues of the characteristic (for the whole family) NDQ triad. The structural and functional data show that cation uptake and release are driven by a switching mechanism. Surprisely, Na+ pathway in KR2 is lined with the chain of polar pores/cavities, similarly to the channelrhodopsin-2. Using Parinello fast molecular dynamics approach we obtained a molecular movie of a probable ion release.Our data provides insight into the mechanism of a non-proton cation light-driven pumping, strongly suggest close relation of sodium pumps to channel rhodopsins and, we believe, expand the present knowledge of rhodopsin world. Certainly they might be used for engineering of cation pumps and ion channels for optogenetics.

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“…4 In addition, NpSRII is distantly related to G-protein coupled receptors (GPCRs) including visual rhodopsins. 5 Similar to other rhodopsins, NpSRII comprises seven transmembrane helices (A-G) with a retinal chromophore covalently bound to a conserved lysine residue of helix G via a protonated Schiff base. In membranes, NpSRII interacts with its cognate transducer (NpHtrII), which consists of a membrane-embedded N-terminal domain with two transmembrane a-helices, TM1 and TM2, and an elongated ahelical coiled-coil cytoplasmic signalling domain that protrudes into the cytoplasm by $26 nm.…”

Section: Introductionmentioning

confidence: 99%

Characterization of an archaeal photoreceptor/transducer complex from Natronomonas pharaonis assembled within styrene–maleic acid lipid particles

et al. 2017

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Eukaryotic G protein-coupled receptors as descendants of prokaryotic sodium-translocating rhodopsins

Cited by 45 publications

References 98 publications

Comparative transcriptomics supports the presence of G protein‐coupled receptor‐based signaling in unicellular marine eukaryotes

Comparative transcriptomics supports the presence of G protein‐coupled receptor‐based signaling in unicellular marine eukaryotes

Molecular mechanism of light-driven sodium pumping

Characterization of an archaeal photoreceptor/transducer complex from Natronomonas pharaonis assembled within styrene–maleic acid lipid particles

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