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The evolutionary path of the epithelial sodium channel delta-subunit in Cetartiodactyla points to a role in sodium sensing

  • The epithelial sodium channel (ENaC) plays a key role in osmoregulation in tetrapod vertebrates and is a candidate receptor for salt taste sensation. There are four ENaC subunits (alpha, beta, gamma, & delta) which form alpha beta gamma or delta beta gamma-ENaCs. While alpha beta gamma-ENaC is a maintenance protein controlling sodium and potassium homeostasis, delta beta gamma-ENaC might represent a stress protein monitoring high sodium concentrations. The delta-subunit emerged with water-to-land transition of tetrapod vertebrate ancestors. We investigated the evolutionary path of ENaC-coding genes in Cetartiodactyla, a group comprising even-toed ungulates and the cetaceans (whales/dolphins) which transitioned from terrestrial to marine environments in the Eocene. The genes SCNN1A (alpha-ENaC), SCNN1B (beta-ENaC) and SCNN1G (gamma-ENaC) are intact in all 22 investigated cetartiodactylan families. While SCNN1D (delta-ENaC) is intact in terrestrial Artiodactyla, it is a pseudogene in 12 cetacean families. A fusion of SCNN1D exons 11 and 12 under preservation of the open reading frame was observed in the Antilopinae, representing a new feature of this clade. Transcripts of SCNN1A, SCNN1B and SCNN1G were present in kidney and lung tissues of Bottlenose dolphins, highlighting alpha beta gamma-ENaC's role as a maintenance protein. Consistent with SCNN1D loss, Bottlenose dolphins and Beluga whales did not show behavioural differences to stimuli with or without sodium in seawater-equivalent concentrations. These data suggest a function of delta-ENaC as a sodium sensing protein which might have become obsolete in cetaceans after the migration to high-salinity marine environments. Consistently, there is reduced selection pressure or pseudogenisation of SCNN1D in other marine mammals, including sirenians, pinnipeds and sea otter.

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Metadaten
Document Type:Preprint
Language:English
Author:Fynn Zahnow, Chiara Jaeger, Yassmin Mohamed, Gianluca Vogelhuber, Fabian May, Alexandra Maria Ciocan, Arianna Manieri, Stephan Maxeiner, Gabriela Krasteva-Christ, Matthew R.D. Cobain, Lars Podsiadlowski, Jose Luis Crespo-Picazo, Daniel Garcia-Parraga, Mike Althaus
Parent Title (English):bioRxiv
DOI:https://doi.org/10.1101/2024.11.18.623996
Date of first publication:2024/11/19
Copyright:The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
Funding:MA is supported by grants from the Ministry of Science and Education of the State of North Rhine-Westphalia (project no. 005-2101-0144 and 005-2211-0043). This work is further funded by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation), Project-ID 514177501 and Project-lD 528562393 - FIP 26. GV was supported by an ERASMUS+ scholarship.
Departments, institutes and facilities:Fachbereich Angewandte Naturwissenschaften
Institut für funktionale Gen-Analytik (IFGA)
Projects:Automatisierte funktionale Analytik von Ionenkanälen und Transportern (NRW/MKW/005-2101-0144)
AStaBaK - Atomare Strukturaufklärung von Biomolekülen durch automatisierte Kristallisation (NRW/MKW/005-2211-0043)
Analyseplattform für molekulare Mechanismen und zelluläre Funktionen (DE/DFG/514177501)
CytoTransport - Mechanismen und Modulation zellulärer Transportprozesse (DE/DFG/528562393)
Dewey Decimal Classification (DDC):5 Naturwissenschaften und Mathematik / 57 Biowissenschaften; Biologie / 576 Genetik und Evolution
Entry in this database:2024/11/21