Metabolic depression during environmental stress: the role of extracellular versus intracellular pH in Sipunculus nudus

Abstract

Environmental stresses such as hypoxia or hypercapnia are known to cause acid-base disturbances and in several organisms they lead to metabolic depression. The present study was undertaken to quantify the influence of these changes in acid&shyp;base parameters on metabolic rate. We determined the rate of oxygen consumption in a non-perfused preparation of the body wall musculature of the marine worm Sipunculus nudus at various levels of extra- and intracellular pH (pHe and pHi, respectively), PCO2 and [HCO3-]. The acid&shyp;base status of the tissue was modified and clamped by long-term exposure to media set to specific values of extracellular pH, PCO2 and [HCO3-]. At a pHe of 7.90, which is equivalent to the normoxic normocapnic in vivo extracellular pH, and an ambient PCO2 of 0.03 kPa (control conditions), pHi was 7.26±0.02 (mean ± s.d., N=5). A reduction of extracellular pH from 7.90 to 7.20 resulted in a significant decrease of pHi to 7.17±0.05 at 0.03 kPa PCO2 (normocapnia) and to 7.20±0.02 at 1.01 kPa PCO2 (hypercapnia). At the same time, the rate of oxygen consumption of the tissue was significantly depressed by 18.7±4.7 % and 17.7±3.0 %, respectively. A significant depression of oxygen consumption by 13.7±4.7 % also occurred under hypercapnia at pHe 7.55 when pHi was elevated above control values (7.32±0.01). No significant changes in oxygen consumption were observed when pHe was either drastically elevated to 8.70 under normocapnia (pHi 7.36±0.05) or maintained at 7.90 during hypercapnia (pHi 7.37±0.03). ATP and phospho-l-arginine concentrations, as well as the Gibbs free energy change of ATP hydrolysis (dG/dATP), were maintained at high levels during all treatments, indicating an equilibrium between energy supply and demand. We conclude that the depression of aerobic energy turnover in isolated body wall musculature of S. nudus is induced by low extracellular pH. A model is proposed which could explain a reduced ATP cost of pHi regulation during extracellular acidosis, thus contributing to metabolic depression.