Larvae of the midge Chironomus riparius possess two distinct mechanisms for ionoregulation in response to ion-poor conditions

Abstract

Nguyen H, Donini A. Larvae of the midge Chironomus riparius possess two distinct mechanisms for ionoregulation in response to ion-poor conditions. Am J Physiol Regul Integr Comp Physiol 299: R762-R773, 2010. First published July 14, 2010 doi:10.1152/ajpregu.00745.2009.-This study examined the role of the anal papillae of the freshwater (FW) chironomid larva Chironomus riparius in ionoregulation under ion-poor conditions. The scanning ion-selective electrode technique (SIET) was utilized to characterize the species, direction, and rates of inorganic ion transport by the anal papillae following acute and long-term exposure to ion-poor water (IPW). The major inorganic ions in the hemolymph of larvae treated as above were measured using standard ion-selective microelectrodes. The anal papillae of C. riparius are sites of net NaCl uptake and H ϩ secretion under FW and IPW conditions and are not likely to be a major contributor of K ϩ exchange. Acute and long-term exposure to IPW increased total net transport of Na ϩ , Cl Ϫ , and H ϩ by the anal papillae, but the mechanisms underlying the increase under the two conditions were different. Acute IPW exposure increased the magnitude of net ion fluxes at sites along the anal papillae, while long-term IPW exposure resulted in increased size of the anal papillae with no change in the magnitude of net ion fluxes. The contribution of the anal papillae to observed alterations of hemolymph ion activities upon exposure to IPW is discussed. Inhibitors of the Na ϩ /H ϩ exchangers (EIPA) and carbonic anhydrase (methazolamide) provide evidence for Na ϩ /H ϩ and Cl Ϫ /HCO 3 Ϫ exchange mechanisms in the anal papillae. This study demonstrates that C. riparius larvae employ two different mechanisms to upregulate the total net transport of ions by the anal papillae, and these mechanisms are at least partially responsible for regulating hemolymph ion activity. chironomid; anal papilla; transepithelial ion transport; inorganic ions; homeostasis HOMEOSTATIC REGULATION OF the ionic and osmotic composition of the blood is critical for survival. Aquatic animals are common inhabitants of dilute freshwater (FW) environments, which are less concentrated than their blood, and thus, are faced with a number of ionic and osmotic challenges in the regulation of salt and water balance (25,31,35,37,41). The paucity of ions in the external medium establishes diffusional ion gradients that favor the osmotic influx of water and passive loss of ions. To counteract the water uptake and dilution of the blood, large amounts of dilute hypotonic urine are produced (6,25,31). To maintain ion balance, ions are actively absorbed from the external medium to replenish the ions lost through excretion and metabolic processes (25,31,44,54,66).FW habitats are variable, and environmental salinity can fluctuate with changes in climate that can lead to dilution through rainfall or concentration through evaporation (43). One of the principal difficulties in assessing the effects of climate change on the environment is the ...

Aedes aegypti Rhesus glycoproteins contribute to ammonia excretion by larval anal papillae

“…The scanning ion-selective electrode technique (SIET) system used in this study has been previously described (Donini and O'Donnell, 2005;Nguyen and Donini, 2010;Chasiotis et al, 2016). NH 4 + microelectrodes were made (see below) and calibrated in solutions of 0.1, 1 and 10 mmol 1 −1 NH 4 Cl.…”

Pharmacological characterisation of apical Na+ and Cl– transport mechanisms of the anal papillae in the larval mosquitoAedes aegypti

“…Ion-selective microelectrodes (ISMEs) were fabricated utilizing a protocol adapted from Smith et al and explained in detail by Nguyen and Donini (Smith et al, 1999;Nguyen and Donini, 2010). In brief the following ionophore cocktails and backfill electrolyte solutions (in parentheses) were used: Na + ionophore II cocktail A (100mmoll -1 NaCl); Cl -ionophore I cocktail A (1 moll -1 NaCl); Cl -ionophore II/TDMACL/-NPOE (100mmoll -1 NaCl, Messerli et al, 2008) 54.71±0.91, 22).…”

“…In brief the following ionophore cocktails and backfill electrolyte solutions (in parentheses) were used: Na + ionophore II cocktail A (100mmoll -1 NaCl); Cl -ionophore I cocktail A (1 moll -1 NaCl); Cl -ionophore II/TDMACL/-NPOE (100mmoll -1 NaCl, Messerli et al, 2008) 54.71±0.91, 22). The SIET methodology is described in detail elsewhere (see Nguyen and Donini, 2010;Rheault and O'Donnell, 2001;Rheault and O'Donnell, 2004). ISMEs were connected to a headstage with an Ag-AgCl wire electrode holder (World Precision Instruments) and the headstage was connected to an ion polarographic amplifier (IPA-2, Applicable Electronics, Forestdale, MA, USA).…”

“…Automated scanning electrode technique (ASET) Version 2.0 software (Science Wares, East Falmouth, MA, USA) was used to position the ISMEs and record voltage measurements. This sampling protocol was previously established and utilized for measuring ion gradients at the anal papillae of mosquitoes and midges (see Donini and O'Donnell, 2005;Nguyen and Donini, 2010).…”

“…A0554 and D3514). The doses of the inhibitors were selected based on previous invertebrate or vertebrate tissue studies such that they were selective for their intended targets [phenamil (Reid et al, 2003;Kleyman and Cragoe, 1988); ouabain (MacVicker et al, 1993); bafilomycin (Beyenbach et al, 2000); methazolamide, DIDS and SITS (Smith et al, 2010;Nguyen and Donini, 2010); HMA (Kleyman and Cragoe, 1988;Tsui et al, 2009)]. All inhibitors were dissolved in DMSO to yield stock solutions that were subsequently diluted in bathing solution as described above.…”