Evolution of Pentameric Ligand-Gated Ion Channels: Pro-Loop Receptors.
Pentameric ligand-gated ion channels (pLGICs) are ubiquitous neurotransmitter receptors in Bilateria, with a small number of known prokaryotic homologues. Here we describe a new inventory and phylogenetic analysis of pLGIC genes across all kingdoms of life. Our main finding is a set of pLGIC genes i...
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doaj-fc621c958b0a475dad7a4170b2d4be6d2020-11-25T01:25:10ZengPublic Library of Science (PLoS)PLoS ONE1932-62032016-01-01113e015193410.1371/journal.pone.0151934Evolution of Pentameric Ligand-Gated Ion Channels: Pro-Loop Receptors.Mariama JaitehAntoine TalyJérôme HéninPentameric ligand-gated ion channels (pLGICs) are ubiquitous neurotransmitter receptors in Bilateria, with a small number of known prokaryotic homologues. Here we describe a new inventory and phylogenetic analysis of pLGIC genes across all kingdoms of life. Our main finding is a set of pLGIC genes in unicellular eukaryotes, some of which are metazoan-like Cys-loop receptors, and others devoid of Cys-loop cysteines, like their prokaryotic relatives. A number of such "Cys-less" receptors also appears in invertebrate metazoans. Together, those findings draw a new distribution of pLGICs in eukaryotes. A broader distribution of prokaryotic channels also emerges, including a major new archaeal taxon, Thaumarchaeota. More generally, pLGICs now appear nearly ubiquitous in major taxonomic groups except multicellular plants and fungi. However, pLGICs are sparsely present in unicellular taxa, suggesting a high rate of gene loss and a non-essential character, contrasting with their essential role as synaptic receptors of the bilaterian nervous system. Multiple alignments of these highly divergent sequences reveal a small number of conserved residues clustered at the interface between the extracellular and transmembrane domains. Only the "Cys-loop" proline is absolutely conserved, suggesting the more fitting name "Pro loop" for that motif, and "Pro-loop receptors" for the superfamily. The infered molecular phylogeny shows a Cys-loop and a Cys-less clade in eukaryotes, both containing metazoans and unicellular members. This suggests new hypotheses on the evolutionary history of the superfamily, such as a possible origin of the Cys-loop cysteines in an ancient unicellular eukaryote. Deeper phylogenetic relationships remain uncertain, particularly around the split between bacteria, archaea, and eukaryotes.http://europepmc.org/articles/PMC4795631?pdf=render |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Mariama Jaiteh Antoine Taly Jérôme Hénin |
spellingShingle |
Mariama Jaiteh Antoine Taly Jérôme Hénin Evolution of Pentameric Ligand-Gated Ion Channels: Pro-Loop Receptors. PLoS ONE |
author_facet |
Mariama Jaiteh Antoine Taly Jérôme Hénin |
author_sort |
Mariama Jaiteh |
title |
Evolution of Pentameric Ligand-Gated Ion Channels: Pro-Loop Receptors. |
title_short |
Evolution of Pentameric Ligand-Gated Ion Channels: Pro-Loop Receptors. |
title_full |
Evolution of Pentameric Ligand-Gated Ion Channels: Pro-Loop Receptors. |
title_fullStr |
Evolution of Pentameric Ligand-Gated Ion Channels: Pro-Loop Receptors. |
title_full_unstemmed |
Evolution of Pentameric Ligand-Gated Ion Channels: Pro-Loop Receptors. |
title_sort |
evolution of pentameric ligand-gated ion channels: pro-loop receptors. |
publisher |
Public Library of Science (PLoS) |
series |
PLoS ONE |
issn |
1932-6203 |
publishDate |
2016-01-01 |
description |
Pentameric ligand-gated ion channels (pLGICs) are ubiquitous neurotransmitter receptors in Bilateria, with a small number of known prokaryotic homologues. Here we describe a new inventory and phylogenetic analysis of pLGIC genes across all kingdoms of life. Our main finding is a set of pLGIC genes in unicellular eukaryotes, some of which are metazoan-like Cys-loop receptors, and others devoid of Cys-loop cysteines, like their prokaryotic relatives. A number of such "Cys-less" receptors also appears in invertebrate metazoans. Together, those findings draw a new distribution of pLGICs in eukaryotes. A broader distribution of prokaryotic channels also emerges, including a major new archaeal taxon, Thaumarchaeota. More generally, pLGICs now appear nearly ubiquitous in major taxonomic groups except multicellular plants and fungi. However, pLGICs are sparsely present in unicellular taxa, suggesting a high rate of gene loss and a non-essential character, contrasting with their essential role as synaptic receptors of the bilaterian nervous system. Multiple alignments of these highly divergent sequences reveal a small number of conserved residues clustered at the interface between the extracellular and transmembrane domains. Only the "Cys-loop" proline is absolutely conserved, suggesting the more fitting name "Pro loop" for that motif, and "Pro-loop receptors" for the superfamily. The infered molecular phylogeny shows a Cys-loop and a Cys-less clade in eukaryotes, both containing metazoans and unicellular members. This suggests new hypotheses on the evolutionary history of the superfamily, such as a possible origin of the Cys-loop cysteines in an ancient unicellular eukaryote. Deeper phylogenetic relationships remain uncertain, particularly around the split between bacteria, archaea, and eukaryotes. |
url |
http://europepmc.org/articles/PMC4795631?pdf=render |
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