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Intracellular pH regulation: characterization and functional investigation of H(+) transporters in Stylophora pistillata

BACKGROUND: Reef-building corals regularly experience changes in intra- and extracellular H(+) concentrations ([H(+)]) due to physiological and environmental processes. Stringent control of [H(+)] is required to maintain the homeostatic acid-base balance in coral cells and is achieved through the re...

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Autores principales: Capasso, Laura, Ganot, Philippe, Planas-Bielsa, Víctor, Tambutté, Sylvie, Zoccola, Didier
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7941709/
https://www.ncbi.nlm.nih.gov/pubmed/33685406
http://dx.doi.org/10.1186/s12860-021-00353-x
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author Capasso, Laura
Ganot, Philippe
Planas-Bielsa, Víctor
Tambutté, Sylvie
Zoccola, Didier
author_facet Capasso, Laura
Ganot, Philippe
Planas-Bielsa, Víctor
Tambutté, Sylvie
Zoccola, Didier
author_sort Capasso, Laura
collection PubMed
description BACKGROUND: Reef-building corals regularly experience changes in intra- and extracellular H(+) concentrations ([H(+)]) due to physiological and environmental processes. Stringent control of [H(+)] is required to maintain the homeostatic acid-base balance in coral cells and is achieved through the regulation of intracellular pH (pH(i)). This task is especially challenging for reef-building corals that share an endosymbiotic relationship with photosynthetic dinoflagellates (family Symbiodinaceae), which significantly affect the pH(i) of coral cells. Despite their importance, the pH regulatory proteins involved in the homeostatic acid-base balance have been scarcely investigated in corals. Here, we report in the coral Stylophora pistillata a full characterization of the genomic structure, domain topology and phylogeny of three major H(+) transporter families that are known to play a role in the intracellular pH regulation of animal cells; we investigated their tissue-specific expression patterns and assessed the effect of seawater acidification on their expression levels. RESULTS: We identified members of the Na(+)/H(+) exchanger (SLC9), vacuolar-type electrogenic H(+)-ATP hydrolase (V-ATPase) and voltage-gated proton channel (H(v)CN) families in the genome and transcriptome of S. pistillata. In addition, we identified a novel member of the H(v)CN gene family in the cnidarian subclass Hexacorallia that has not been previously described in any species. We also identified key residues that contribute to H(+) transporter substrate specificity, protein function and regulation. Last, we demonstrated that some of these proteins have different tissue expression patterns, and most are unaffected by exposure to seawater acidification. CONCLUSIONS: In this study, we provide the first characterization of H(+) transporters that might contribute to the homeostatic acid-base balance in coral cells. This work will enrich the knowledge of the basic aspects of coral biology and has important implications for our understanding of how corals regulate their intracellular environment. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12860-021-00353-x.
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spelling pubmed-79417092021-03-09 Intracellular pH regulation: characterization and functional investigation of H(+) transporters in Stylophora pistillata Capasso, Laura Ganot, Philippe Planas-Bielsa, Víctor Tambutté, Sylvie Zoccola, Didier BMC Mol Cell Biol Research Article BACKGROUND: Reef-building corals regularly experience changes in intra- and extracellular H(+) concentrations ([H(+)]) due to physiological and environmental processes. Stringent control of [H(+)] is required to maintain the homeostatic acid-base balance in coral cells and is achieved through the regulation of intracellular pH (pH(i)). This task is especially challenging for reef-building corals that share an endosymbiotic relationship with photosynthetic dinoflagellates (family Symbiodinaceae), which significantly affect the pH(i) of coral cells. Despite their importance, the pH regulatory proteins involved in the homeostatic acid-base balance have been scarcely investigated in corals. Here, we report in the coral Stylophora pistillata a full characterization of the genomic structure, domain topology and phylogeny of three major H(+) transporter families that are known to play a role in the intracellular pH regulation of animal cells; we investigated their tissue-specific expression patterns and assessed the effect of seawater acidification on their expression levels. RESULTS: We identified members of the Na(+)/H(+) exchanger (SLC9), vacuolar-type electrogenic H(+)-ATP hydrolase (V-ATPase) and voltage-gated proton channel (H(v)CN) families in the genome and transcriptome of S. pistillata. In addition, we identified a novel member of the H(v)CN gene family in the cnidarian subclass Hexacorallia that has not been previously described in any species. We also identified key residues that contribute to H(+) transporter substrate specificity, protein function and regulation. Last, we demonstrated that some of these proteins have different tissue expression patterns, and most are unaffected by exposure to seawater acidification. CONCLUSIONS: In this study, we provide the first characterization of H(+) transporters that might contribute to the homeostatic acid-base balance in coral cells. This work will enrich the knowledge of the basic aspects of coral biology and has important implications for our understanding of how corals regulate their intracellular environment. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12860-021-00353-x. BioMed Central 2021-03-08 /pmc/articles/PMC7941709/ /pubmed/33685406 http://dx.doi.org/10.1186/s12860-021-00353-x Text en © The Author(s) 2021 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Capasso, Laura
Ganot, Philippe
Planas-Bielsa, Víctor
Tambutté, Sylvie
Zoccola, Didier
Intracellular pH regulation: characterization and functional investigation of H(+) transporters in Stylophora pistillata
title Intracellular pH regulation: characterization and functional investigation of H(+) transporters in Stylophora pistillata
title_full Intracellular pH regulation: characterization and functional investigation of H(+) transporters in Stylophora pistillata
title_fullStr Intracellular pH regulation: characterization and functional investigation of H(+) transporters in Stylophora pistillata
title_full_unstemmed Intracellular pH regulation: characterization and functional investigation of H(+) transporters in Stylophora pistillata
title_short Intracellular pH regulation: characterization and functional investigation of H(+) transporters in Stylophora pistillata
title_sort intracellular ph regulation: characterization and functional investigation of h(+) transporters in stylophora pistillata
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7941709/
https://www.ncbi.nlm.nih.gov/pubmed/33685406
http://dx.doi.org/10.1186/s12860-021-00353-x
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