Abstract
Swimbladder gas gland cells are known to produce lactic acid required for the acidification of swimbladder blood and decreasing the oxygen carrying capacity of swimbladder blood, i.e., the onset of the Root effect. Gas gland cells have also been shown to metabolize glucose via the pentose phosphate shunt, but the role of the pentose phosphate shunt for acid secretion has not yet been evaluated. Similarly, aerobic metabolism of gas gland cells has been largely neglected so far. In the present study, we therefore simultaneously assessed the role of glycolysis and of the pentose phosphate shunt for acid secretion and recorded oxygen consumption of isolated swimbladder gas gland cells of the European eel. Presence of glucose was essential for acid secretion, and at glucose concentrations of about 1.5 mmol l−1 acid secretion of gas gland cells reached a maximum, indicating that glucose concentrations in swimbladder blood should not be limiting acid production and secretion under physiological conditions. The data revealed that most of the acid was produced in the glycolytic pathway, but a significant fraction was also contributed by the pentose phosphate shunt. Addition of glucose to gas gland cells incubated in a glucose-free medium resulted in a reduction of oxygen uptake. Inhibition of mitochondrial respiration significantly reduced oxygen consumption, but a fraction of mitochondria-independent respiration remained in presence of rotenone and antimycin A. In the presence of glucose, application of either iodo-acetate inhibiting glycolysis or 6-AN inhibiting the pentose phosphate shunt did not significantly affect oxygen uptake, indicating an independent regulation of oxidative phosphorylation and of acid production. Inhibition of the muscarinic acetylcholine receptor caused a slight elevation in acid secretion, while forskolin caused a concentration-dependent reduction in acid secretion, indicating muscarinic and c-AMP-dependent control of acid secretion in gas gland cells.
Highlights
The energy metabolism of swimbladder gas gland cells of physoclist fish is peculiar in that they typically experience hyperoxic conditions, but glucose is mainly converted to lactic acid to generate sufficient protons for the acidification of swimbladder blood (D’Aoust 1970; Deck 1970; Pelster 1995b; Pelster and Scheid 1993)
Addition of iodo-acetate (IAA) to inhibit glycolysis caused a rapid decrease in extracellular acidification rate (ECAR) down to the initial values in both groups, and addition of 2-deoxyglucose (2-DG) to completely block glucose metabolism resulted in another slight decrease in ECAR (Fig. 2A)
Addition of IAA to these cells reduced acid secretion to 32% of the control value, and addition of 2-DG caused an additional reduction in ECAR, but in controls and in the presence of 6-AN, ECAR rates determined after completely blocking glucose metabolism using 2-DG, were not significantly different from ECAR rates determined in the presence of IAA (Fig. 3A)
Summary
The energy metabolism of swimbladder gas gland cells of physoclist fish is peculiar in that they typically experience hyperoxic conditions, but glucose is mainly converted to lactic acid to generate sufficient protons for the acidification of swimbladder blood (D’Aoust 1970; Deck 1970; Pelster 1995b; Pelster and Scheid 1993). Journal of Comparative Physiology B (2022) 192:447–457 swimbladder, so that hyperbaric oxygen partial pressures can be generated, sufficient to explain the secretion of oxygen against hydrostatic pressures of several 10 s or even more than 100 atmospheres (Kuhn et al 1963; Pelster 2001). Gas gland cells of the American eel and of the gulf toadfish have been shown to produce CO2 in the pentose phosphate shunt (Pelster et al 1994; Walsh and Milligan 1993). The possible contribution and the importance of the pentose phosphate shunt to acid secretion of gas gland cells and acidification of the blood, have never been addressed. NADPH is produced in the pentose phosphate shunt, which may affect the redox equilibrium in the cell
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