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Analysis of aquaporins from the euryhaline barnacle Balanus improvisus reveals differential expression in response to changes in salinity

Barnacles are sessile macro-invertebrates, found along rocky shores in coastal areas worldwide. The euryhaline bay barnacle Balanus improvisus (Darwin, 1854) (= Amphibalanus improvisus) can tolerate a wide range of salinities, but the molecular mechanisms underlying the osmoregulatory capacity of th...

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Autores principales: Lind, Ulrika, Järvå, Michael, Alm Rosenblad, Magnus, Pingitore, Piero, Karlsson, Emil, Wrange, Anna-Lisa, Kamdal, Emelie, Sundell, Kristina, André, Carl, Jonsson, Per R., Havenhand, Jon, Eriksson, Leif A., Hedfalk, Kristina, Blomberg, Anders
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5513457/
https://www.ncbi.nlm.nih.gov/pubmed/28715506
http://dx.doi.org/10.1371/journal.pone.0181192
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author Lind, Ulrika
Järvå, Michael
Alm Rosenblad, Magnus
Pingitore, Piero
Karlsson, Emil
Wrange, Anna-Lisa
Kamdal, Emelie
Sundell, Kristina
André, Carl
Jonsson, Per R.
Havenhand, Jon
Eriksson, Leif A.
Hedfalk, Kristina
Blomberg, Anders
author_facet Lind, Ulrika
Järvå, Michael
Alm Rosenblad, Magnus
Pingitore, Piero
Karlsson, Emil
Wrange, Anna-Lisa
Kamdal, Emelie
Sundell, Kristina
André, Carl
Jonsson, Per R.
Havenhand, Jon
Eriksson, Leif A.
Hedfalk, Kristina
Blomberg, Anders
author_sort Lind, Ulrika
collection PubMed
description Barnacles are sessile macro-invertebrates, found along rocky shores in coastal areas worldwide. The euryhaline bay barnacle Balanus improvisus (Darwin, 1854) (= Amphibalanus improvisus) can tolerate a wide range of salinities, but the molecular mechanisms underlying the osmoregulatory capacity of this truly brackish species are not well understood. Aquaporins are pore-forming integral membrane proteins that facilitate transport of water, small solutes and ions through cellular membranes, and that have been shown to be important for osmoregulation in many organisms. The knowledge of the function of aquaporins in crustaceans is, however, limited and nothing is known about them in barnacles. We here present the repertoire of aquaporins from a thecostracan crustacean, the barnacle B. improvisus, based on genome and transcriptome sequencing. Our analyses reveal that B. improvisus contains eight genes for aquaporins. Phylogenetic analysis showed that they represented members of the classical water aquaporins (Aqp1, Aqp2), the aquaglyceroporins (Glp1, Glp2), the unorthodox aquaporin (Aqp12) and the arthropod-specific big brain aquaporin (Bib). Interestingly, we also found two big brain-like proteins (BibL1 and BibL2) constituting a new group of aquaporins not yet described in arthropods. In addition, we found that the two water-specific aquaporins were expressed as C-terminal splice variants. Heterologous expression of some of the aquaporins followed by functional characterization showed that Aqp1 transported water and Glp2 water and glycerol, agreeing with the predictions of substrate specificity based on 3D modeling and phylogeny. To investigate a possible role for the B. improvisus aquaporins in osmoregulation, mRNA expression changes in adult barnacles were analysed after long-term acclimation to different salinities. The most pronounced expression difference was seen for AQP1 with a substantial (>100-fold) decrease in the mantle tissue in low salinity (3 PSU) compared to high salinity (33 PSU). Our study provides a base for future mechanistic studies on the role of aquaporins in osmoregulation.
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spelling pubmed-55134572017-08-07 Analysis of aquaporins from the euryhaline barnacle Balanus improvisus reveals differential expression in response to changes in salinity Lind, Ulrika Järvå, Michael Alm Rosenblad, Magnus Pingitore, Piero Karlsson, Emil Wrange, Anna-Lisa Kamdal, Emelie Sundell, Kristina André, Carl Jonsson, Per R. Havenhand, Jon Eriksson, Leif A. Hedfalk, Kristina Blomberg, Anders PLoS One Research Article Barnacles are sessile macro-invertebrates, found along rocky shores in coastal areas worldwide. The euryhaline bay barnacle Balanus improvisus (Darwin, 1854) (= Amphibalanus improvisus) can tolerate a wide range of salinities, but the molecular mechanisms underlying the osmoregulatory capacity of this truly brackish species are not well understood. Aquaporins are pore-forming integral membrane proteins that facilitate transport of water, small solutes and ions through cellular membranes, and that have been shown to be important for osmoregulation in many organisms. The knowledge of the function of aquaporins in crustaceans is, however, limited and nothing is known about them in barnacles. We here present the repertoire of aquaporins from a thecostracan crustacean, the barnacle B. improvisus, based on genome and transcriptome sequencing. Our analyses reveal that B. improvisus contains eight genes for aquaporins. Phylogenetic analysis showed that they represented members of the classical water aquaporins (Aqp1, Aqp2), the aquaglyceroporins (Glp1, Glp2), the unorthodox aquaporin (Aqp12) and the arthropod-specific big brain aquaporin (Bib). Interestingly, we also found two big brain-like proteins (BibL1 and BibL2) constituting a new group of aquaporins not yet described in arthropods. In addition, we found that the two water-specific aquaporins were expressed as C-terminal splice variants. Heterologous expression of some of the aquaporins followed by functional characterization showed that Aqp1 transported water and Glp2 water and glycerol, agreeing with the predictions of substrate specificity based on 3D modeling and phylogeny. To investigate a possible role for the B. improvisus aquaporins in osmoregulation, mRNA expression changes in adult barnacles were analysed after long-term acclimation to different salinities. The most pronounced expression difference was seen for AQP1 with a substantial (>100-fold) decrease in the mantle tissue in low salinity (3 PSU) compared to high salinity (33 PSU). Our study provides a base for future mechanistic studies on the role of aquaporins in osmoregulation. Public Library of Science 2017-07-17 /pmc/articles/PMC5513457/ /pubmed/28715506 http://dx.doi.org/10.1371/journal.pone.0181192 Text en © 2017 Lind et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Lind, Ulrika
Järvå, Michael
Alm Rosenblad, Magnus
Pingitore, Piero
Karlsson, Emil
Wrange, Anna-Lisa
Kamdal, Emelie
Sundell, Kristina
André, Carl
Jonsson, Per R.
Havenhand, Jon
Eriksson, Leif A.
Hedfalk, Kristina
Blomberg, Anders
Analysis of aquaporins from the euryhaline barnacle Balanus improvisus reveals differential expression in response to changes in salinity
title Analysis of aquaporins from the euryhaline barnacle Balanus improvisus reveals differential expression in response to changes in salinity
title_full Analysis of aquaporins from the euryhaline barnacle Balanus improvisus reveals differential expression in response to changes in salinity
title_fullStr Analysis of aquaporins from the euryhaline barnacle Balanus improvisus reveals differential expression in response to changes in salinity
title_full_unstemmed Analysis of aquaporins from the euryhaline barnacle Balanus improvisus reveals differential expression in response to changes in salinity
title_short Analysis of aquaporins from the euryhaline barnacle Balanus improvisus reveals differential expression in response to changes in salinity
title_sort analysis of aquaporins from the euryhaline barnacle balanus improvisus reveals differential expression in response to changes in salinity
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5513457/
https://www.ncbi.nlm.nih.gov/pubmed/28715506
http://dx.doi.org/10.1371/journal.pone.0181192
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