The effects of gill remodeling on transepithelial sodium fluxes and the distribution of presumptive sodium-transporting ionocytes in goldfish (Carassius auratus)

Abstract

Goldfish, Carassius auratus, adaptively remodel their gills in response to changes in ambient oxygen and temperature, altering the functional lamellar surface area to balance the opposing requirements for respiration and osmoregulation. In this study, the effects of thermal- and hypoxia-mediated gill remodeling on branchial Na(+) fluxes and the distribution of putative Na(+)-transporting ionocytes in goldfish were assessed. When assessed either in vitro (isolated gill arches) or in vivo at a common water temperature, the presence of an interlamellar cell mass (ILCM) in fish acclimated to 7°C clearly decreased Na(+) efflux across the gill relative to fish maintained at 25°C and lacking an ILCM. However, loss of the ILCM in 7°C-acclimated fish exposed to hypoxia led to a decrease in Na(+) efflux (assessed under hypoxic conditions) despite the apparent large increases in functional lamellar surface area. Goldfish possessing an ILCM were able to sustain Na(+) uptake, albeit at a lower rate matched to efflux, owing to the re-distribution of ionocytes expressing genes thought to be involved in Na(+) uptake [Na(+)/H(+) exchanger isoform 3 (NHE3) and V- type H(+)-ATPase] to the edge of the ILCM where they can establish contact with the surrounding environment. NHE-expressing cells co-localized with Na(+)/K(+)-ATPase expression, suggesting a role for NHE in Na(+)-uptake in the goldfish. Implications of the ILCM on ion fluxes in the goldfish are discussed.

The role of acid-sensing ion channels (ASICs) in epithelial Na+ uptake in adult zebrafish (Danio rerio).

“…This model is supported by empirical evidence from several freshwater fish species (e.g. Bradshaw et al, 2012;Esaki et al, 2007;Hirata et al, 2003;Yan et al, 2007); however, a limitation of this model is the questionable ability of the electroneutral NHE to function in low-Na + waters (Na + <0.1 mmol l −1 ) and/or low pH ( pH<5), where gradients for Na + and H + would be reversed (Avella and Bornancin, 1989;Parks et al, 2008). Recently, the NHE model has been extended by the addition of an ammonia (NH 3 )-transporting Rhesus (Rh) protein (Nakada et al, 2007;Nawata et al, 2007), whereby NHE2/3 and Rh protein form a metabolon, which locally decreases H + concentration in the boundary layer and facilitates NHE function in acidic environments (Wright and Wood, 2009).…”

Implications for Osmorespiratory Compromise by Anatomical Remodeling in the Gills of Arapaima gigas

“…In C. auratus, exhibiting ILCM, branchial Na 1 and Cl 2 efflux and ammonia excretion decreases compared to those lacking an ILCM (Mitrovic and Perry, 2009;Bradshaw et al, 2012;Smith et al, 2012). However, in A. gigas, despite a thicker gill epithelium, Gonzales et al (2010) found significantly higher influx and efflux rates of Na 1 in the gills of 724 g fish than in smaller individuals.…”

Physiological and molecular responses of the goldfish kidney (Carassius auratus) to metabolic acidosis, and potential mechanisms of renal ammonia transport

“…Primer sequences were derived from Sinha et al (2013), A. K. Sinha, H. J. Liew, C. M. Nawata, R. Blust, C.M.W. and G. De Boeck (unpublished) and Bradshaw et al (2012) (supplementary material Table S1). qPCR reactions consisted of a total volume of 10 µl: 4 µl of cDNA sample, 5 µl of 2× SSoFast EvaGreen Supermix (Bio-Rad Laboratories Inc., Hercules, CA, USA), 0.8 µl (10 µmol l −1 ) of both the reverse and forward primers (Mobix, Hamilton, ON, Canada) and 0.2 µl of RNase-free water.…”

“…We used the goldfish, Carassius auratus (Linnaeus 1758), the species in which renal ammonia excretion was first studied directly (King and Goldstein, 1983) and for which a suite of molecular probes are now available (Bradshaw et al, 2012;Sinha et al, 2013). We hypothesized that elevated urinary ammonia excretion during metabolic acidosis would be predominantly mediated by increased renal tubular secretion, rather than by increased glomerular filtration.…”