External CO₂ levels influence energy yielding metabolic pathways under hypoxia in the leech, Hirudo medicinalis

Abstract

Medicinal leeches, Hirudo medicinalis L., were exposed to hypocapnic (nominal pC02 0.0 kPa) or hypercapnic (pC0, 1.3 kPa) hypoxia (p02 2.0 kPa) for up to 4 days. Changes in blood concentrations and tissue content of organic acids were measured.In the early phase of hypercapnic hypoxia leeches accumulated mainly succinate, and the normally high malate concentrations in blood and tissue were reduced concomitantly. Between 2 and 24 h of hypoxia the animals started to produce propionate which is the major end-product of this type of hypoxia. Only low concentrations of lactate were found in blood and tissue. During the initial phase of hypocapnic hypoxia an accumulation of succinate was also observed, but at a higher rate than during hypercapnic hypoxia. Subsequently, propionate was also produced. Between 24 and 48 h of hypocapnic hypoxia the concentrations of succinate in blood and tissue decreased rapidly and lactate appeared as an end-product of anaerobic metabolism.The results indicate that, in leeches under "environmental" hypoxia, the external concentration of carbon dioxide affects the pathway of carbohydrate metabolism resulting in either succinatelpmpionate production or in lactate accumulation. 0 1992 Wiley-Liss, Inc.Many aquatic animals have to cope with situations of limited oxygen availability in their habitat. To sustain longer periods of severe hypoxia it is essential to maintain energy supply from metabolic pathways which are not dependent on the presence of oxygen. Transition to anaerobic metabolism and, in many cases, a decrease in metabolic rate occur when the oxygen partial pressure of the environment drops below critical values (Zebe and Schottler, '86; Hochachka, '86).In many animals under hypoxic conditions the degradation of glycogen to lactate via the EmbdenMeyerhof-Parnas pathway (anaerobic glycolysis) is the main energy-yielding process. In contrast, especially in those animals which are obligate anaerobes or sustain longer periods of "environmental" hypoxia (e.g., parasitic helminths in the intestine of vertebrates, some molluscs, and annelids), glycogen is degraded to succinate and propionate (Hochachka and Mustafa, '72) which is, in terms of ATP production, a more efficient metabolic pathway than lactate generation (Schottler, '77; Schroff and Zebe, '80).Succinate production in anaerobic annelids requires the carboxylation of phosphoenolpyruvate (PEP) which is catalyzed by phosphoenolpyruvate carboxykinase (PEPCK) (Hoffmann et al., '79). Another enzyme, pyruvate kinase (PK), competes for PEP at this metabolic branchpoint converting PEP to pyruvate, which is a n intermediate metabolite for lactate production. The direction of carbohydrate metabolism a t the level of PEP is determined by the activity ratio of PEPCK to PK as confirmed by the observation that specific inhibition of the PEPCK in hypoxic Arenicola marina resulted in lactate accumulation (Schottler and Wienhausen, '81) although lactate is not a regular end-product of anaerobiosis in this species. Various mechanisms have...

Mg2+-Malate Co-Transport, a Mechanism for Na+-Independent Mg2+Transport in Neurons of the LeechHirudo medicinalis

“…5). Extracellular succinate/propionate (hypercapnic conditions) or lactate concentrations (hypocapnic conditions) increase in parallel with the decrease in malate concentration (Hildebrandt 1992;Scholz and Zerbst-Boroffka 1998), but neither succinate nor lactate interfered with Na ϩ -independent Mg 2ϩ transport in the present experiments. Coupling malate uptake to Mg 2ϩ transport may be advantageous, because Mg 2ϩ is well buffered, both intraand extracellularly, so that initially the Mg 2ϩ gradient would be expected to remain almost constant and to disintegrate only slowly even over more extended periods of hypoxia.…”

“…This may be due to the feeding behavior of leeches, which are able to take up several times their own body weight and then live on this meal for several months. It may also be an adaptation to cope with limited oxygen availability in their habitat (Hildebrandt 1992). Similarly high concentrations in organic anions have also been found in other invertebrates, such as insects (Scholz and Zerbst-Boroffka 1998).…”