The consequences of reversible gill remodelling on ammonia excretion in goldfish (Carassius auratus)

Abstract

SUMMARYGoldfish acclimated to cold water (e.g. 7°C) experience a marked reduction in functional lamellar surface area owing to the proliferation of an interlamellar cell mass (ILCM), a phenomenon termed gill remodelling. The goal of the present study was to assess the consequences of the reduced functional surface area on the capacity of goldfish to excrete ammonia. Despite the expected impact of ambient temperature on functional surface area, fish acclimated to 7°C and 25°C exhibited similar rates of ammonia excretion (J net,amm ); the Q 10 values for fed and starved fish were 1.07 and 1.20, respectively. To control for possible temperature-related differences in rates of endogenous ammonia production, J net,amm was determined at the two acclimation temperatures after loading fish with 1.12molg -1 of NH 4 Cl. In the 3h post-injection period, J net,amm was elevated to a greater extent in the 25°C fish. To estimate the potential contribution of increased ventilation and cardiac output to ammonia clearance in the warmer fish, the ammonia loading experiment was repeated on the 7°C fish immediately after they were exercised to exhaustion. The rate of excretion of ammonia was significantly increased in the exercised 7°C fish (presumably experiencing increased ventilation and cardiac output for at least some of the measurement period) suggesting that differences in external and internal convection may at least partially explain the enhanced capacity of the 25°C fish to clear the ammonia load. To more specifically assess the contribution of the different functional surface areas on the differing rates of ammonia clearance at the two acclimation temperatures, the 7°C fish were exposed for 7days to hypoxia (P O2 10 mmHg1.33kPa), a treatment known to cause the disappearance of the ILCM. The results demonstrated that the hypoxia-associated loss of the ILCM was accompanied by a significant increase in the rate of ammonia clearance in the 7°C fish when returned to normoxic conditions. To determine whether compensatory changes in the ammonia transporting proteins might be contributing to sustaining J net,amm under conditions of reduced functional lamellar surface area, the relative expression and branchial distribution of four Rh proteins were assessed by western blotting and immunocytochemistry. Although the relative expression of the Rh proteins was unaffected by acclimation temperature, there did appear to be a change in the spatial distribution of Rhag, Rhbg and Rhcg1. Specifically, these three Rh proteins (and to a lesser extent Rhcg2) appeared to localize in cells on the outer edge of the ILCM that were enriched with Na + /K + -ATPase. Thus, we suggest that despite the impediment to ammonia excretion imposed by the ILCM, goldfish acclimated to 7°C are able to sustain normal rates of excretion owing to the redistribution of ammonia transporting cells.

Digestion of a single meal affects gene expression of ion and ammonia transporters and glutamine synthetase activity in the gastrointestinal tract of freshwater rainbow trout

“…Finally, as mRNA is only itself an indirect measurement of transporter expression, protein expression analysis (through immunocytochemical studies; e.g. Perry et al 2010) would reveal if the increase in mRNA expression relates to an increase in transporter number and not simply an increase in transporter turnover rate.…”

Effects of high ammonia concentrations on three cyprinid fish: Acute and whole-ecosystem chronic tests

“…Gill re-modelling has been widely suggested as an adaptive strategy to cope with stressful environments. An exposure test of goldfish, Carassius auratus (highly ammonia-resistant cyprinid), suggested that the posterior sides of the lamellae may play a role in the inter-lamellar cell mass´capacity to hinder branchial ammonia excretion (Perry et al, 2010b;Smith et al, 2012). Thickening of filaments and lamellae in the form of enlargement of inter-lamellar cell mass as observed in our study has also been found for common carp, Cyprinus carpio (a less ammonia-sensitive cyprinid), clearly for goldfish, and although less clear and very slowly (Sinha et al, 2014) even for rainbow trout, Oncorhynchus mykiss (highly ammonia sensitive).…”

The relationship between NMDA receptor function and the high ammonia tolerance of anoxia-tolerant goldfish

“…The possibility that increases in Rhesus (Rh) glycoprotein expression in the gills promoted ammonia excretion at HEA in these fish is another intriguing possibility given the role of these proteins in teleost ammonia excretion (for reviews, see Weihrauch et al, 2009;Wright and Wood, 2009). The Rh glycoproteins Rhcgb and Rhcg are not only found on the lamella of goldfish (Perry et al, 2010) but also on the inter-lamellar cell masses (ILCM) that are formed between lamellae of cold-acclimated goldfish (Sollid et al, 2005).…”