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Teleostean fishes may have developed an efficient Na(+) uptake for adaptation to the freshwater system

Understanding Na(+) uptake mechanisms in vertebrates has been a research priority since vertebrate ancestors were thought to originate from hyperosmotic marine habitats to the hypoosmotic freshwater system. Given the evolutionary success of osmoregulator teleosts, these freshwater conquerors from th...

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Autores principales: Tseng, Yung-Che, Yan, Jia-Jiun, Furukawa, Fumiya, Chen, Ruo-Dong, Lee, Jay-Ron, Tsou, Yi-Ling, Liu, Tzu-Yen, Tang, Yu-Hsin, Hwang, Pung-Pung
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9581171/
https://www.ncbi.nlm.nih.gov/pubmed/36277196
http://dx.doi.org/10.3389/fphys.2022.947958
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author Tseng, Yung-Che
Yan, Jia-Jiun
Furukawa, Fumiya
Chen, Ruo-Dong
Lee, Jay-Ron
Tsou, Yi-Ling
Liu, Tzu-Yen
Tang, Yu-Hsin
Hwang, Pung-Pung
author_facet Tseng, Yung-Che
Yan, Jia-Jiun
Furukawa, Fumiya
Chen, Ruo-Dong
Lee, Jay-Ron
Tsou, Yi-Ling
Liu, Tzu-Yen
Tang, Yu-Hsin
Hwang, Pung-Pung
author_sort Tseng, Yung-Che
collection PubMed
description Understanding Na(+) uptake mechanisms in vertebrates has been a research priority since vertebrate ancestors were thought to originate from hyperosmotic marine habitats to the hypoosmotic freshwater system. Given the evolutionary success of osmoregulator teleosts, these freshwater conquerors from the marine habitats are reasonably considered to develop the traits of absorbing Na(+) from the Na(+)-poor circumstances for ionic homeostasis. However, in teleosts, the loss of epithelial Na(+) channel (ENaC) has long been a mystery and an issue under debate in the evolution of vertebrates. In this study, we evaluate the idea that energetic efficiency in teleosts may have been improved by selection for ENaC loss and an evolved energy-saving alternative, the Na(+)/H(+) exchangers (NHE3)-mediated Na(+) uptake/NH(4) (+) excretion machinery. The present study approaches this question from the lamprey, a pioneer invader of freshwater habitats, initially developed ENaC-mediated Na(+) uptake driven by energy-consuming apical H(+)-ATPase (VHA) in the gills, similar to amphibian skin and external gills. Later, teleosts may have intensified ammonotelism to generate larger NH(4) (+) outward gradients that facilitate NHE3-mediated Na(+) uptake against an unfavorable Na(+) gradient in freshwater without consuming additional ATP. Therefore, this study provides a fresh starting point for expanding our understanding of vertebrate ion regulation and environmental adaptation within the framework of the energy constraint concept.
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spelling pubmed-95811712022-10-20 Teleostean fishes may have developed an efficient Na(+) uptake for adaptation to the freshwater system Tseng, Yung-Che Yan, Jia-Jiun Furukawa, Fumiya Chen, Ruo-Dong Lee, Jay-Ron Tsou, Yi-Ling Liu, Tzu-Yen Tang, Yu-Hsin Hwang, Pung-Pung Front Physiol Physiology Understanding Na(+) uptake mechanisms in vertebrates has been a research priority since vertebrate ancestors were thought to originate from hyperosmotic marine habitats to the hypoosmotic freshwater system. Given the evolutionary success of osmoregulator teleosts, these freshwater conquerors from the marine habitats are reasonably considered to develop the traits of absorbing Na(+) from the Na(+)-poor circumstances for ionic homeostasis. However, in teleosts, the loss of epithelial Na(+) channel (ENaC) has long been a mystery and an issue under debate in the evolution of vertebrates. In this study, we evaluate the idea that energetic efficiency in teleosts may have been improved by selection for ENaC loss and an evolved energy-saving alternative, the Na(+)/H(+) exchangers (NHE3)-mediated Na(+) uptake/NH(4) (+) excretion machinery. The present study approaches this question from the lamprey, a pioneer invader of freshwater habitats, initially developed ENaC-mediated Na(+) uptake driven by energy-consuming apical H(+)-ATPase (VHA) in the gills, similar to amphibian skin and external gills. Later, teleosts may have intensified ammonotelism to generate larger NH(4) (+) outward gradients that facilitate NHE3-mediated Na(+) uptake against an unfavorable Na(+) gradient in freshwater without consuming additional ATP. Therefore, this study provides a fresh starting point for expanding our understanding of vertebrate ion regulation and environmental adaptation within the framework of the energy constraint concept. Frontiers Media S.A. 2022-10-05 /pmc/articles/PMC9581171/ /pubmed/36277196 http://dx.doi.org/10.3389/fphys.2022.947958 Text en Copyright © 2022 Tseng, Yan, Furukawa, Chen, Lee, Tsou, Liu, Tang and Hwang. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Physiology
Tseng, Yung-Che
Yan, Jia-Jiun
Furukawa, Fumiya
Chen, Ruo-Dong
Lee, Jay-Ron
Tsou, Yi-Ling
Liu, Tzu-Yen
Tang, Yu-Hsin
Hwang, Pung-Pung
Teleostean fishes may have developed an efficient Na(+) uptake for adaptation to the freshwater system
title Teleostean fishes may have developed an efficient Na(+) uptake for adaptation to the freshwater system
title_full Teleostean fishes may have developed an efficient Na(+) uptake for adaptation to the freshwater system
title_fullStr Teleostean fishes may have developed an efficient Na(+) uptake for adaptation to the freshwater system
title_full_unstemmed Teleostean fishes may have developed an efficient Na(+) uptake for adaptation to the freshwater system
title_short Teleostean fishes may have developed an efficient Na(+) uptake for adaptation to the freshwater system
title_sort teleostean fishes may have developed an efficient na(+) uptake for adaptation to the freshwater system
topic Physiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9581171/
https://www.ncbi.nlm.nih.gov/pubmed/36277196
http://dx.doi.org/10.3389/fphys.2022.947958
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