Aquaporin expression dynamics in osmoregulatory tissues of Atlantic salmon during smoltification and seawater acclimation

Abstract

SUMMARYOsmotic balance in fish is maintained through the coordinated regulation of water and ion transport performed by epithelia in intestine, kidney and gill. In the current study, six aquaporin (AQP) isoforms found in Atlantic salmon (Salmo salar) were classified and their tissue specificity and mRNA expression in response to a hyperosmotic challenge and during smoltification were examined. While AQP-1a was generic, AQP-1b had highest expression in kidney and AQP-3 was predominantly found in oesophagus, gill and muscle. Two novel teleost isoforms, AQP-8a and -8b, were expressed specifically in liver and intestinal segments, respectively. AQP-10 was predominantly expressed in intestinal segments, albeit at very low levels. Transfer from freshwater (FW) to seawater (SW) induced elevated levels of intestinal AQP-1a, -1b and -8b mRNA, whereas only AQP-8b was stimulated during smoltification. In kidney, AQP-1a, -3 and -10 were elevated in SW whereas AQP-1b was reduced compared with FW levels. Correspondingly, renal AQP-1a and -10 peaked during smoltification in April and March, respectively, as AQP-1b and AQP-3 declined. In the gill, AQP-1a and AQP-3 declined in SW whereas AQP-1b increased. Gill AQP-1a and -b peaked in April, whereas AQP-3 declined through smoltification. These reciprocal isoform shifts in renal and gill tissues may be functionally linked with the changed role of these organs in FW compared with SW. The presence and observed dynamics of the AQP-8b isoform specifically in intestinal sections suggest that this is a key water channel responsible for water uptake in the intestinal tract of seawater salmonids.

Differential expression and novel permeability properties of three aquaporin 8 paralogs from seawater-challenged Atlantic salmon smolts

“…During SW acclimation, Atlantic salmon aqp8ab mRNA is strongly upregulated in intestinal segments, indicating a possible role for this paralog in water balance (Tipsmark et al, 2010). Similar results were found for European and Japanese eels, where SWacclimated animals showed higher levels of aqp8 mRNA in the intestine (Cutler et al, 2009;Kim et al, 2010).…”

“…To date, the piscine aquaporin superfamily has only been characterized in the diploid zebrafish (Danio rerio) (TingaudSequeira et al, 2010), while other species of teleost have been examined with respect to basal expression patterns of selected aquaporins within osmoregulatory tissues Lignot et al, 2002;Martinez et al, 2005a;Martinez et al, 2005b;Raldúa et al, 2008;Tingaud-Sequeira et al, 2010;Tipsmark et al, 2010;Madsen et al, 2011). Although there is some consensus on the expression pattern of each paralog, there is emerging evidence that even closely related aquaporins, such as the tandemly duplicated aqp1aa and aqp1ab genes and alternatively duplicated aqp8 paralogs, have neofunctionalized in relation to their regulation and function (Martinez et al, 2005a;Martinez et al, 2005b;Tipsmark et al, 2010;Madsen et al, 2011;Finn and Cerdà, 2011;Zapater et al, 2011).…”

“…Although there is some consensus on the expression pattern of each paralog, there is emerging evidence that even closely related aquaporins, such as the tandemly duplicated aqp1aa and aqp1ab genes and alternatively duplicated aqp8 paralogs, have neofunctionalized in relation to their regulation and function (Martinez et al, 2005a;Martinez et al, 2005b;Tipsmark et al, 2010;Madsen et al, 2011;Finn and Cerdà, 2011;Zapater et al, 2011). In the stenohaline FW zebrafish, aqp8 is present as three paralogs (aqp8aa, -8ab and -8b) and fragments of each have been found in a partial transcriptome (EST library) of the Atlantic salmon (Tingaud-Sequeira et al, 2010;Cerdà and Finn, 2010;Engelund and Madsen, 2011).…”

“…In mammals, such as rats, only one AQP8 is expressed, and it is found in the proximal kidney tubules, hepatocytes, testes, salivary gland and intestine (Elkjaer et al, 2001). In teleosts such as the European eel (Anguilla anguilla), Japanese eel (Anguilla japonica), zebrafish and Atlantic salmon, several aqp8 transcripts have been located in some of the same tissues, although each paralog showed a distinct tissue mRNA expression pattern (Cutler et al, 2009;Kim et al, 2010;Tingaud-Sequeira et al, 2010;Tipsmark et al, 2010). Because of the extra round of genome duplication in salmonids, more aqp8s may exist in this species than in zebrafish and the present study probably does not reveal the full complement of aqp8s in Atlantic salmon.…”

“…We additionally examined the protein expression of Aqp8ab and Aqp8b in two intestinal segments to establish whether the suggested role of Aqp8ab during SW acclimation (Tipsmark et al, 2010) could be confirmed at the protein level and whether differences existed between the paralogs. The permeability properties of the three paralogs were investigated in Xenopus laevis oocytes in order to reveal potential neofunctionalization, which could shed light on whether tissue-specific expression patterns are linked to functional diversity.…”