Function and phylogeny support the independent evolution of an ASIC-like Deg/ENaC channel in the Placozoa
Function and phylogeny support the independent evolution of an ASIC-like Deg/ENaC channel in the Placozoa
ASIC channels are bilaterian proton-gated sodium channels belonging to the large and functionally-diverse Deg/ENaC family that also includes peptide- and mechanically-gated channels. Here, we report that the non-bilaterian invertebrate Trichoplax adhaerens possesses a proton-activated Deg/ENaC channel, TadNaC2, with a unique combination of biophysical features including tachyphylaxis like ASIC1a, reduced proton sensitivity like ASIC2a, biphasic macroscopic currents like ASIC3, as well as low sensitivity to the Deg/ENaC channel blocker amiloride and Ca2+ ions. Structural modeling and mutation analyses reveal that TadNaC2 proton gating is different from ASIC channels, lacking key molecular determinants, and involving unique residues within the palm and finger regions. Phylogenetic analysis reveals that a monophyletic clade of T. adhaerens Deg/ENaC channels, which includes TadNaC2, is phylogenetically distinct from ASIC channels, instead forming a clade with BASIC channels. Altogether, this work suggests that ASIC-like channels evolved independently in T. adhaerens and its phylum Placozoa. Our phylogenetic analysis also identifies several clades of uncharacterized metazoan Deg/ENaC channels, and provides phylogenetic evidence for the existence of Deg/ENaC channels outside of Metazoa, present in the gene data of select unicellular heterokont and filasterea-related species.
Animals, Placozoa/genetics, Phylogeny, Protons, Acid Sensing Ion Channels/genetics, Amiloride
Elkhatib, Wassim
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Yanez-Guerra, Luis A.
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Mayorova, Tatiana D.
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Currie, Mark A.
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Singh, Anhadvir
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Perera, Maria
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Gauberg, Julia
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Senatore, Adriano
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18 September 2023
Elkhatib, Wassim
e9a6a3ab-c74f-482d-9eff-3c7b2dd14466
Yanez-Guerra, Luis A.
cbca947b-bbf0-4b91-96b0-4a126e3b94b6
Mayorova, Tatiana D.
834a79ba-5daf-4388-9655-045d1eaadfea
Currie, Mark A.
d9d740aa-4cf4-4863-ba55-57d2c2f375e6
Singh, Anhadvir
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Perera, Maria
9eac73ef-d267-4090-8516-2717a5cb08f8
Gauberg, Julia
96c8a0a2-438c-44cc-bd62-74d9c435766a
Senatore, Adriano
0b2719e2-564d-4c37-abe4-6a4f82bbba31
Elkhatib, Wassim, Yanez-Guerra, Luis A., Mayorova, Tatiana D., Currie, Mark A., Singh, Anhadvir, Perera, Maria, Gauberg, Julia and Senatore, Adriano
(2023)
Function and phylogeny support the independent evolution of an ASIC-like Deg/ENaC channel in the Placozoa.
Communications Biology, 6 (1), [951].
(doi:10.1038/s42003-023-05312-0).
Abstract
ASIC channels are bilaterian proton-gated sodium channels belonging to the large and functionally-diverse Deg/ENaC family that also includes peptide- and mechanically-gated channels. Here, we report that the non-bilaterian invertebrate Trichoplax adhaerens possesses a proton-activated Deg/ENaC channel, TadNaC2, with a unique combination of biophysical features including tachyphylaxis like ASIC1a, reduced proton sensitivity like ASIC2a, biphasic macroscopic currents like ASIC3, as well as low sensitivity to the Deg/ENaC channel blocker amiloride and Ca2+ ions. Structural modeling and mutation analyses reveal that TadNaC2 proton gating is different from ASIC channels, lacking key molecular determinants, and involving unique residues within the palm and finger regions. Phylogenetic analysis reveals that a monophyletic clade of T. adhaerens Deg/ENaC channels, which includes TadNaC2, is phylogenetically distinct from ASIC channels, instead forming a clade with BASIC channels. Altogether, this work suggests that ASIC-like channels evolved independently in T. adhaerens and its phylum Placozoa. Our phylogenetic analysis also identifies several clades of uncharacterized metazoan Deg/ENaC channels, and provides phylogenetic evidence for the existence of Deg/ENaC channels outside of Metazoa, present in the gene data of select unicellular heterokont and filasterea-related species.
Text
s42003-023-05312-0
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Accepted/In Press date: 1 September 2023
Published date: 18 September 2023
Additional Information:
Funding Information:
This research was funded by an NSERC Discovery Grant (RGPIN-2021-03557), an NSERC Discovery Accelerator Supplement (RGPAS-2021-00002), an Ontario Early Researcher Award (ER17-13-247), and a Canadian Foundation for Innovation Grant (35297) to A. Senatore, An Ontario Graduate Scholarship to W.E., a Biotechnology and Biological Sciences Research Council Grant (BBSRC; BB/W010305/1) to L.A.Y.-G., and an NSERC Discovery Grant (RGPIN-2023-05615) and a Canadian Foundation for Innovation Grant (40684) to M.A.C. We would like to thank Dr. Carolyn Smith for early discussions about putative pH sensing behavior by T. adhaerens.
Keywords:
Animals, Placozoa/genetics, Phylogeny, Protons, Acid Sensing Ion Channels/genetics, Amiloride
Identifiers
Local EPrints ID: 483232
URI: http://eprints.soton.ac.uk/id/eprint/483232
ISSN: 2399-3642
PURE UUID: 5d8e0450-932f-49db-88a0-a864a7c2ad20
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Date deposited: 26 Oct 2023 16:51
Last modified: 18 Mar 2024 04:15
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Contributors
Author:
Wassim Elkhatib
Author:
Luis A. Yanez-Guerra
Author:
Tatiana D. Mayorova
Author:
Mark A. Currie
Author:
Anhadvir Singh
Author:
Maria Perera
Author:
Julia Gauberg
Author:
Adriano Senatore
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