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...

Full description

Bibliographic Details
Main Authors: Ulrika Lind, Michael Järvå, Magnus Alm Rosenblad, Piero Pingitore, Emil Karlsson, Anna-Lisa Wrange, Emelie Kamdal, Kristina Sundell, Carl André, Per R Jonsson, Jon Havenhand, Leif A Eriksson, Kristina Hedfalk, Anders Blomberg
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2017-01-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC5513457?pdf=render
id doaj-828da2e6bbd944f6aa3ebfe8f439f78a
record_format Article
spelling doaj-828da2e6bbd944f6aa3ebfe8f439f78a2020-11-25T01:41:52ZengPublic Library of Science (PLoS)PLoS ONE1932-62032017-01-01127e018119210.1371/journal.pone.0181192Analysis of aquaporins from the euryhaline barnacle Balanus improvisus reveals differential expression in response to changes in salinity.Ulrika LindMichael JärvåMagnus Alm RosenbladPiero PingitoreEmil KarlssonAnna-Lisa WrangeEmelie KamdalKristina SundellCarl AndréPer R JonssonJon HavenhandLeif A ErikssonKristina HedfalkAnders BlombergBarnacles 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.http://europepmc.org/articles/PMC5513457?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Ulrika Lind
Michael Järvå
Magnus Alm Rosenblad
Piero Pingitore
Emil Karlsson
Anna-Lisa Wrange
Emelie Kamdal
Kristina Sundell
Carl André
Per R Jonsson
Jon Havenhand
Leif A Eriksson
Kristina Hedfalk
Anders Blomberg
spellingShingle Ulrika Lind
Michael Järvå
Magnus Alm Rosenblad
Piero Pingitore
Emil Karlsson
Anna-Lisa Wrange
Emelie Kamdal
Kristina Sundell
Carl André
Per R Jonsson
Jon Havenhand
Leif A Eriksson
Kristina Hedfalk
Anders Blomberg
Analysis of aquaporins from the euryhaline barnacle Balanus improvisus reveals differential expression in response to changes in salinity.
PLoS ONE
author_facet Ulrika Lind
Michael Järvå
Magnus Alm Rosenblad
Piero Pingitore
Emil Karlsson
Anna-Lisa Wrange
Emelie Kamdal
Kristina Sundell
Carl André
Per R Jonsson
Jon Havenhand
Leif A Eriksson
Kristina Hedfalk
Anders Blomberg
author_sort Ulrika Lind
title 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_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_sort analysis of aquaporins from the euryhaline barnacle balanus improvisus reveals differential expression in response to changes in salinity.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2017-01-01
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.
url http://europepmc.org/articles/PMC5513457?pdf=render
work_keys_str_mv AT ulrikalind analysisofaquaporinsfromtheeuryhalinebarnaclebalanusimprovisusrevealsdifferentialexpressioninresponsetochangesinsalinity
AT michaeljarva analysisofaquaporinsfromtheeuryhalinebarnaclebalanusimprovisusrevealsdifferentialexpressioninresponsetochangesinsalinity
AT magnusalmrosenblad analysisofaquaporinsfromtheeuryhalinebarnaclebalanusimprovisusrevealsdifferentialexpressioninresponsetochangesinsalinity
AT pieropingitore analysisofaquaporinsfromtheeuryhalinebarnaclebalanusimprovisusrevealsdifferentialexpressioninresponsetochangesinsalinity
AT emilkarlsson analysisofaquaporinsfromtheeuryhalinebarnaclebalanusimprovisusrevealsdifferentialexpressioninresponsetochangesinsalinity
AT annalisawrange analysisofaquaporinsfromtheeuryhalinebarnaclebalanusimprovisusrevealsdifferentialexpressioninresponsetochangesinsalinity
AT emeliekamdal analysisofaquaporinsfromtheeuryhalinebarnaclebalanusimprovisusrevealsdifferentialexpressioninresponsetochangesinsalinity
AT kristinasundell analysisofaquaporinsfromtheeuryhalinebarnaclebalanusimprovisusrevealsdifferentialexpressioninresponsetochangesinsalinity
AT carlandre analysisofaquaporinsfromtheeuryhalinebarnaclebalanusimprovisusrevealsdifferentialexpressioninresponsetochangesinsalinity
AT perrjonsson analysisofaquaporinsfromtheeuryhalinebarnaclebalanusimprovisusrevealsdifferentialexpressioninresponsetochangesinsalinity
AT jonhavenhand analysisofaquaporinsfromtheeuryhalinebarnaclebalanusimprovisusrevealsdifferentialexpressioninresponsetochangesinsalinity
AT leifaeriksson analysisofaquaporinsfromtheeuryhalinebarnaclebalanusimprovisusrevealsdifferentialexpressioninresponsetochangesinsalinity
AT kristinahedfalk analysisofaquaporinsfromtheeuryhalinebarnaclebalanusimprovisusrevealsdifferentialexpressioninresponsetochangesinsalinity
AT andersblomberg analysisofaquaporinsfromtheeuryhalinebarnaclebalanusimprovisusrevealsdifferentialexpressioninresponsetochangesinsalinity
_version_ 1725039282076254208