Metazoan evolution of glutamate receptors reveals unreported phylogenetic groups and divergent lineage-specific events

Abstract
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Abstract

Glutamate receptors are divided in two unrelated families: ionotropic (iGluR), driving synaptic transmission, and metabotropic (mGluR), which modulate synaptic strength. The present classification of GluRs is based on vertebrate proteins and has remained unchanged for over two decades. Here we report an exhaustive phylogenetic study of GluRs in metazoans. Importantly, we demonstrate that GluRs have followed different evolutionary histories in separated animal lineages. Our analysis reveals that the present organization of iGluRs into six classes does not capture the full complexity of their evolution. Instead, we propose an organization into four subfamilies and ten classes, four of which have never been previously described. Furthermore, we report a sister class to mGluR classes I-III, class IV. We show that many unreported proteins are expressed in the nervous system, and that new Epsilon receptors form functional ligand-gated ion channels. We propose an updated classification of glutamate receptors that includes our findings.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for Figures 1, Figure 1 - figure supplement 1, Figure 1 - figure supplement 3, Figure 1 - figure supplement 4, Figure2, Figure 4, Figure 4 - figure supplement 1 and Figure 4 - figure supplement 3.

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Article and author information

Author details

David Ramos-Vicente

Molecular Physiology of the Synapse Laboratory, Biomedical Research Institute Sant Pau, Barcelona, Spain

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-2730-0850
Jie Ji

Institute of Biotechnology and Biomedicine, Universitat Autònoma de Barcelona, Bellaterra (Cerdanyola del Vallès), Spain

Competing interests
The authors declare that no competing interests exist.
Esther Gratacòs-Batlle

Department of Biomedicine, Medical School, University of Barcelona, Barcelona, Spain

Competing interests
The authors declare that no competing interests exist.
Gemma Gou

Molecular Physiology of the Synapse Laboratory, Biomedical Research Institute Sant Pau, Barcelona, Spain

Competing interests
The authors declare that no competing interests exist.
Rita Reig-Viader

Molecular Physiology of the Synapse Laboratory, Biomedical Research Institute Sant Pau, Barcelona, Spain

Competing interests
The authors declare that no competing interests exist.
Javier Luís

Molecular Physiology of the Synapse Laboratory, Biomedical Research Institute Sant Pau, Barcelona, Spain

Competing interests
The authors declare that no competing interests exist.
Demian Burguera

Department of Genetics, University of Barcelona, Barcelona, Spain

Competing interests
The authors declare that no competing interests exist.
Enrique Navas-Perez

Department of Genetics, University of Barcelona, Barcelona, Spain

Competing interests
The authors declare that no competing interests exist.
Jordi García-Fernández

Department of Genetics, University of Barcelona, Barcelona, Spain

Competing interests
The authors declare that no competing interests exist.
Pablo Fuentes-Prior

Molecular Bases of Disease, Biomedical Research Institute Sant Pau, Barcelona, Spain

Competing interests
The authors declare that no competing interests exist.
Hector Escriva

Biologie Intégrative des Organismes Marins, Sorbonne Université, CNRS, Banyuls-sur-Mer, France

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The authors declare that no competing interests exist.
Nerea Roher

Institute of Biotechnology and Biomedicine, Universitat Autònoma de Barcelona, Bellaterra (Cerdanyola del Vallès), Spain

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The authors declare that no competing interests exist.
David Soto

Department of Biomedicine, Medical School, University of Barcelona, Barcelona, Spain

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The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-7995-3805
Àlex Bayés

Molecular Physiology of the Synapse Laboratory, Biomedical Research Institute Sant Pau, Barcelona, Spain

For correspondence
abayesp@santpau.cat

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-5265-6306

Funding

Ministerio de Economía y Competitividad (BFU2012-34398)

David Ramos-Vicente
Gemma Gou
Rita Reig-Viader
Javier Luís
Àlex Bayés

Ministerio de Economía y Competitividad (BFU2014-57562-P)

David Soto

Centre National de la Recherche Scientifique (ANR-16-CE12-0008-01)

Hector Escriva

Ministerio de Economía y Competitividad (BFU2017-83317-P)

David Soto

Ministerio de Economía y Competitividad (RD16/0008/0014)

David Soto

Ministerio de Economía y Competitividad (BFU2015-69717-P)

David Ramos-Vicente
Gemma Gou
Rita Reig-Viader
Javier Luís
Àlex Bayés

Seventh Framework Programme (304111)

David Ramos-Vicente
Gemma Gou
Rita Reig-Viader
Javier Luís
Àlex Bayés

Ministerio de Economía y Competitividad (RYC-2011-08391)

Àlex Bayés

Ministerio de Economía y Competitividad (RYC-2010-06210)

Nerea Roher

China Scholarship Council (CSC-2013-06300075)

Jie Ji

Ministerio de Economía y Competitividad (SAF2014-57994-R)

Pablo Fuentes-Prior

Ministerio de Economía y Competitividad (AGL2015-65129-R)

Jie Ji
Nerea Roher

Generalitat de Catalunya (SGR-345-2014)

David Ramos-Vicente
Gemma Gou
Rita Reig-Viader
Javier Luís
Àlex Bayés

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

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