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

Date Published: July 17, 2017

Publisher: Public Library of Science

Author(s): 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, Giovanna Valenti.

http://doi.org/10.1371/journal.pone.0181192

Abstract

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.

Partial Text

Aquaporins (AQPs) are pore-forming integral membrane proteins that mainly facilitate transport of water and small solutes through cellular membranes. Aquaporins arose early in evolution and exist across all phyla [1, 2], indicating their fundamental importance in cell function. The number of aquaporins varies widely between species; there are two in the bacterium Escherichia coli, four in the yeast Saccharomyces cerevisiae, eight in the fruit fly Drosophila melanogaster, thirteen in humans and even higher numbers in plants with seventy-one paralogs in cotton [2–4].

Our analyses reveal that B. improvisus contains eight genes for aquaporins, where two of them, BIBL1 and BIBL2, encode proteins that constitute a new group of aquaporins not yet described in arthropods. In addition, we found that the expression of some of the aquaporins are regulated in response to salinity changes. In particular, the two paralogs of classical water transporting aquaporins display very different responses with AQP1 expression being almost fully repressed at low-salinity conditions. The AQP1-regulation is mainly apparent in the mantle, which is interesting given that the mantle earlier has been proposed as a site for osmoregulation in barnacles. B. improvisus is a truly brackish species that is well adapted to establish itself in low-salinity environments, enabling invasion of brackish waters like the Baltic sea where it was quite recently introduced (<200 years ago) [28]. Scenarios of global climate changes predict future enhanced rainfall leading to freshening of salty environments; the Baltic Sea is predicted an up to 50% salinity decrease by 2100; [57]. This will influence the success of B. improvisus, potentially leading to competitive exclusion of native species [58, 59]. To what extent the aquaporin repertoire in B. improvisus is unique and how it possibly plays a role in the extreme salinity tolerance of this species and in its preference for brackish environments is unclear. A better understanding of this has to await more mechanistic experimental data as well as comparative analysis of other barnacle species with varying salinity tolerance.   Source: http://doi.org/10.1371/journal.pone.0181192

 

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