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Mechanisms of Na+ Uptake, Ammonia Excretion, and Their Potential

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Mechanisms of Na+ Uptake, Ammonia Excretion, and Their Potential J Comp Physiol B (2014) 184:877–890 DOI 10.1007/s00360-014-0847-7 ORIGINAL PAPER Mechanisms of Na+ uptake, ammonia excretion, and their potential linkage in native Rio Negro tetras (Paracheirodon axelrodi, Hemigrammus rhodostomus, and Moenkhausia diktyota) Chris M. Wood · Lisa M. Robertson · Ora E. Johannsson · Adalberto Luis Val Received: 8 April 2014 / Revised: 10 July 2014 / Accepted: 19 July 2014 / Published online: 9 August 2014 © Springer-Verlag Berlin Heidelberg 2014 7 Abstract Mechanisms of Na+ uptake, ammonia excretion, blockade) by AgNO3 (10− M). A time course study on cardi- Na and their potential linkage were investigated in three charac- nal tetras demonstrated that Jin blockade by AgNO3 was very ids (cardinal, hemigrammus, moenkhausia tetras), using radi- rapid (<5 min), suggesting inhibition of branchial carbonic otracer flux techniques to study the unidirectional influx (Jin), anhydrase (CA), and exposure to the CA-blocker acetazola- 4 Na efflux (Jout), and net flux rates (Jnet) of Na+ and Cl−, and the mide (10− M) caused a 50 % reduction in Jin .. Addition- Na 5 net excretion rate of ammonia (JAmm). The fish were collected ally, Jin was unaffected by phenamil (10− M, Na+ channel 4 directly from the Rio Negro, and studied in their native “black- blocker), bumetanide (10− M, NKCC blocker), hydrochlo- 3 water” which is acidic (pH 4.5), ion-poor (Na+, Cl− ~20 µM), rothiazide (5 10− M, NCC blocker), and exposure to an 1 × and rich in dissolved organic matter (DOM 11.5 mg C l− ). acute 3 unit increase in water pH. None of these treatments, Na Cl Na Jin , Jin, and JAmm were higher than in previous reports on tet- including partial or complete elimination of Jin (by acetazola- ras obtained from the North America aquarium trade and/or mide and AgNO3 respectively), had any inhibitory effect on Na studied in low DOM water. In all three species, Jin was unaf- JAmm. Therefore, Na+ uptake in Rio Negro tetras depends on 4 fected by amiloride (10− M, NHE and Na+ channel blocker), an internal supply of H+ from CA, but does not fit any of the Na Cl but both Jin and Jin were virtually eliminated (85–99 % currently accepted H+-dependent models (NHE, Na+ channel/ V-type H+-ATPase), or co-transport schemes (NCC, NKCC), Communicated by G. Heldmaier. and ammonia excretion does not fit the current “Na+/NH4+ exchange metabolon” paradigm. Na+, K+-ATPase and V-type * C. M. Wood ( ) · L. M. Robertson H+-ATPase activities were present at similar levels in gill Department of Biology, McMaster University, homogenates, Acute exposure to high environmental ammo- 1280 Main St. West, Hamilton, ON L8S 4K1, Canada 3 Na e-mail: [email protected] nia (NH4Cl, 10− M) significantly increased Jin , and NH4+ was equally or more effective than K in activating branchial L. M. Robertson + e-mail: [email protected] Na+,(K+) ATPase activity in vitro. We propose that ammonia excretion does not depend on Na+ uptake, but that Na+ uptake C. M. Wood · A. L. Val (by an as yet unknown H+-dependent apical mechanism) Laboratory of Ecophysiology and Molecular Evolution, Instituto depends on ammonia excretion, driven by active NH entry Nacional de Pesquisas da Amazônia (INPA), Manaus, Amazonas, Brazil 4+ via basolateral Na+,(K+)-ATPase. C. M. Wood Rosenstiel School of Marine and Atmospheric Science, Keywords Characids · Low pH water · Silver nitrate · University of Miami, Coral Gables, FL, USA Na+/NH4+ exchange · Na+ · NH4+ATPase C. M. Wood · O. E. Johannsson Department of Zoology, University of British Columbia, Vancouver, BC, Canada Introduction O. E. Johannsson Department of Fisheries and Oceans, Burlington, ON, Canada The acidic, ion-poor “blackwaters” of the Rio Negro and e-mail: [email protected] its tributaries support over 1,000 species of teleost fish. 1 3 878 J Comp Physiol B (2014) 184:877–890 1 The ambient conditions (major cations <30 µmol l− , pH’s and Wood 2012, and Kwong et al. 2014) that this mecha- 3.5–5.5; Furch 1984; Val and Almeida-Val 1995) pose not nism becomes prominent in several species (Osorezan only severe physiological challenges to the fish, but also dace—Hirata et al. 2003, zebrafish—Kumai and Perry severe theoretical challenges to our current understanding 2011, Shih et al. 2012, and larval medaka—Lin et al. 2012) of how branchial Na+ uptake mechanisms work (Randall when chronically exposed to water of low pH and/or low et al. 1996; Gonzalez et al. 2005; Parks et al. 2008). In Na+ concentration. The theory proposes that the deproto- brief, thermodynamic considerations suggest that neither nation of NH4+ as NH3 enters the apical Rh channel cre- of the two dominant mechanisms seen in most freshwa- ates a source of protons to fuel Na+ uptake via NHEs and/ ter fish [apical Na+/H+ exchange (NHE), or Na+ uptake or Na+ channel/V-type H+-ATPase while at the same time, through an apical channel electrochemically coupled to H+ the NH3 leaving the Rh channel traps protons, thereby cre- extrusion via a V-type H+-ATPase] should work under Rio ating an external microenvironment in which [H+] is less Negro conditions. A third more recently proposed mecha- concentrated. Earlier, Randall et al. (1996) had speculated nism involving the apical co-transport of Na+ and Cl− that in Rio Negro fish, NH4+ might enter though the baso- driven by the electrochemical gradient for Na+ (reviewed lateral membrane by substituting for K+ on the Na+, K+- by Evans 2011) would appear to be subject to the same ATPase, which would presumably give an energetic boost energetic challenges under Rio Negro conditions. to the system, and provide an additional source of H+ ions This problem has led to considerable research on to exchange against Na+ at the apical membrane. While ionoregulation in Rio Negro teleosts (reviewed by Gonza- the thermodynamics have not been worked out, essentially lez et al. 2005). Not surprisingly, general conclusions from elevated ammonia excretion would drive Na+ uptake under these studies are that Na+ uptake mechanisms are charac- these conditions. terized by relatively high Na+ affinity and high resistance Ammonia excretion has been only sparsely studied in to inhibition by low pH (high H+) (e.g. Gonzalez et al. Rio Negro teleosts, with no clear picture emerging. In the 1997, 2002; Gonzalez and Preest 1999; Gonzalez and Wil- oscar, a cichlid, there appeared to be a close coupling of son 2001; Preest et al. 2005; Matsuo and Val 2007; Duarte Na+ uptake and ammonia excretion at circumneutral pH, et al. 2013). Amiloride has been tested in several species of both co-varying in a Michaelis–Menten fashion with exter- tetra, small members of the Characiformes, the most abun- nal [Na+] (Wood et al. 2007). When the tambaqui and neon 4 dant order in the Rio Negro. When applied at 10− M in the tetra, both characids, were transferred to low pH, ammo- water, a concentration which should powerfully block both nia excretion increased (Wilson 1996; Wilson et al. 1999). NHE’s and epithelial Na+ channels (Benos 1982; Kleyman However, there appeared to be no coupling of ammonia and Cragoe 1988), amiloride proved to be only margin- excretion to environmental [Na+] in either the neon tetra ally effective (Gonzalez et al. 1997; Gonzalez and Preest (Wilson 1996) or the blackskirt tetra (Gonzalez et al. 1997). 1999) in inhibiting unidirectional Na+ uptake. More exten- The Rio Negro blackwaters are rich in dissolved organic sive pharmacological investigation (Preest et al. 2005) with matter (DOM), and there is now considerable evidence that a range of amiloride analogues (selective for NHEs or for this aids ionoregulation in fish (Gonzalez et al. 1998, 2002; Na+ channels) confirmed this lack of effect. These findings Wood et al. 2003, 2011; Matsuo and Val 2007; Galvez et al. have led to the suggestion that the uptake mechanism(s) 2008) by promoting Na+ influx and ammonia excretion, might be unique, perhaps not involving reliance on H+ as and limiting Na+ efflux, especially under low pH condi- a counter-ion, and, therefore, very different from those in tions. With a few exceptions (Gonzalez et al. 1998, 2002), “standard” teleosts (Gonzalez and Preest 1999; Preest et al. most previous studies on Rio Negro teleosts have been per- 2005; Gonzalez et al. 2005). formed in waters lacking DOM, which may confound the The idea that Na+ uptake might be coupled to NH4+ interpretation. Furthermore, in most cases, the “Rio Negro” excretion was first presented by August Krogh (1938) and fish had been obtained from the aquarium trade in North since then has had a long and chequered history (reviewed America, raising the possibility of acclimation-related or by Wilkie 2002, and Kirschner 2004). However, in the adaptation-related (i.e. genetic) differences from native past few years, the discovery of ammonia-conductive Rh fish. proteins in teleost gills (Nakada et al. 2007; Nawata et al. With this background in mind, during a research expedi- 2007, 2010) has led to a new paradigm that a “Na+/NH4+ tion to the upper Rio Negro, we investigated Na+ uptake, exchange complex” consisting of several apical membrane ammonia excretion, and their potential coupling in three transporters (Rhcg, V-type H+-ATPase, NHE, Na+ channel, species of native tetras freshly collected from the blackwa- carbonic anhydrase) working together as a metabolon pro- ter, and tested in this water. The major focus was on the vides a loose coupling of Na+ uptake with ammonia excre- cardinal tetra (Paracheirodon axelrodi), as this is a spe- tion (Wright and Wood 2009; Ito et al. 2013). Furthermore, cies which has been studied extensively to date (Gonzalez evidence has started to accumulate (reviewed by Wright et al.
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