Is aquaporin‐3 involved in water‐permeability changes in the killifish during hypoxia and normoxic recovery, in freshwater or seawater?

Abstract

Aquaporins are the predominant water‐transporting proteins in vertebrates, but only a handful of studies have investigated aquaporin function in fish, particularly in mediating water permeability during salinity challenges. Even less is known about aquaporin function in hypoxia (low oxygen), which can profoundly affect gill function. Fish deprived of oxygen typically enlarge gill surface area and shrink the water‐to‐blood diffusion distance, to facilitate oxygen uptake into the bloodstream. However, these alterations to gill morphology can result in unfavorable water and ion fluxes. Thus, there exists an osmorespiratory compromise, whereby fish must try to balance high branchial gas exchange with low ion and water permeability. Furthermore, the gills of seawater and freshwater teleosts have substantially different functions with respect to osmotic and ion fluxes; consequently, hypoxia can have very different effects according to the salinity of the environment. The purpose of this study was to determine what role aquaporins play in water permeability in the hypoxia‐tolerant euryhaline common killifish (Fundulus heteroclitus), in two important osmoregulatory organs—the gills and intestine. Using immunofluorescence, we localized aquaporin‐3 (AQP3) protein to the basolateral and apical membranes of ionocytes and enterocytes, respectively. Although hypoxia increased branchial AQP3 messenger‐RNA expression in seawater and freshwater, protein abundance did not correlate. Indeed, hypoxia did not alter AQP3 protein abundance in seawater and reduced it in the cell membranes of freshwater gills. Together, these observations suggest killifish AQP3 contributes to reduced diffusive water flux during hypoxia and normoxic recovery in freshwater and facilitates intestinal permeability in seawater and freshwater.

Salinity effects on expression and localization of aquaporin 3 in gills of the euryhaline milkfish (Chanos chanos)

“…In different species of euryhaline teleosts, AQP3 may be located on different sides of the ionocytes in the gill epithelium. In killifish and medaka, AQP3 is expressed on the basolateral side of ionocytes (Ellis et al, 2019; Ruhr et al, 2020). However, AQP3 is expressed on both the basolateral and apical sides of ionocytes in the European eel ( Anguilla anguilla ) (Lignot et al, 2002).…”

Osmo-respiratory compromise in the mosshead sculpin (Clinocottus globiceps): effects of temperature, hypoxia, and re-oxygenation on rates of diffusive water flux and oxygen uptake

“…Although the functional responses to warming alter gill permeability to oxygen, water, and ions, other factors, such as the temperature sensitivity of hemoglobin-O2 binding dynamics, may also contribute to the thermal sensitivity of whole-organism ṀO2, resulting in divergent thermal sensitivities of diffusive water flux and whole-organism ṀO2, as observed here (Table 1). Unlike ṀO2, diffusive water flux rates may be strongly influenced by aquaporins that have been implicated in playing an important role in facilitating water movement in gill epithelia (Tingaud-Sequiera et al 2010;Cerda and Finn 2010;Madsen et al 2015;Ruhr et al 2020). In contrast with tidepool sculpins, (Somo et al 2020) and a number of other freshwater and seawater species (see Introduction) but in agreement with recent reports on Pacific sanddab (Onukwufor and Wood 2022) and zebrafish (Onukwufor and Wood 2020b), mosshead sculpins exhibited lower overall thermal sensitivity for diffusive water flux than for ṀO2 (Table 1).…”

“…Thus, during acute hypoxia exposure and recovery, ṀO2 and diffusive water flux rates appear to be under the regulatory control of different mechanisms, thereby decoupling effective water permeability from effective O2 permeability. Future studies should analyze the impact of hypoxia exposure on ventilation, respiratory factors at the gill (e.g., Scott et al 2008), gill morphological responses to hypoxia (e.g., Wood et al 2009, Matey et al 2011, and the regulation of aquaporins (e.g., Ruhr et al 2020) and other protein channels to determine the mechanistic basis of the decoupling of oxygen and water permeability.…”

“…The osmo-respiratory compromise phenomenon has been widely studied in freshwater fish with respect to ṀO2 versus ion flux rates (e.g. Randall et al 1972;Gonzalez and McDonald 1992;Gonzalez and McDonald 1994;Postlethwaite and McDonald 1995;Iftikar et al 2010;Robertson et al 2015a, b), but less so with respect to the relationship between ṀO2 and water fluxes (Wood et al 2009(Wood et al , 2019Ruhr et al 2020;Giacomin et al 2020;Onukwufor and Wood 2018;Onukwufor and Wood 2020a;Onukwufor and Wood 2020 b), with even fewer studies in marine fish (Giacomin et al 2017;Wood et al 2019;Somo et al 2020;Onukwufor and Wood 2022).…”

The digestive tract as an essential organ for water acquisition in marine teleosts: lessons from euryhaline eels

“…The aqp3 expression is low in the intestines of Mozambique tilapia [ 254 ] and sea bass [ 64 ]. Among AQPs expressed in the eel intestine, AQP3 is the only AQP that has been found to localize on the basolateral membranes of epithelial cells [ 39 , 254 ], although AQP3 also localizes to the apical membrane in killifish [ 181 ]. In mammals, apical AQP2 and basolateral AQP3 are responsible for transcellular water absorption at the renal collecting duct [ 102 ].…”