A role for adenosine in metabolic depression in the marine invertebrate Sipunculus nudus

Abstract

Involvement of neurotransmitters in metabolic depression under hypoxia and hypercapnia was examined in Sipunculus nudus. Concentration changes of several putative neurotransmitters in nervous tissue during anoxic or hypercapnic exposure or during combined anoxia and hypercapnia were determined. Among amino acids (gamma-aminobutyric acid, glutamate, glycine, taurine, serine, and aspartate) and monoamines (serotonin, dopamine, and norepinephrine), some changes were significant, but none were consistent with metabolic depression under all experimental conditions applied. Only the neuromodulator adenosine displayed concentration changes in accordance with metabolic depression under all experimental conditions. Levels increased during anoxia, during hypercapnia, and to an even greater extent during anoxic hypercapnia. Adenosine infusions into coelomic fluid via an indwelling catheter induced a significant depression of the normocapnic rate of O2 consumption from 0.36 +/- 0.04 to a minimum of 0.24 +/- 0.02 (SE) mumol.g-1.h-1 after 90 min (n = 6). Application of the adenosine antagonist theophylline caused a transient rise in O2 consumption 30 min after infusion during hypercapnia but not during normocapnia. Effects of adenosine and theophylline were observed in intact individuals but not in isolated body wall musculature. The results provide evidence for a role of adenosine in inducing metabolic depression in S. nudus, probably through the established effects of decreasing neuronal excitability and neurotransmitter release. In consideration of our previous finding that metabolic depression in isolated body wall musculature was elicited by extracellular acidosis, it is concluded that central and cellular mechanisms combine to contribute to the overall reduction in metabolic rate in S. nudus.

Biological Impact of Elevated Ocean CO2 Concentrations: Lessons from Animal Physiology and Earth History

“…5). Infusion of adenosine caused metabolic depression (Reipschläger et al, 1997). A similar role for adenosine is also known for some vertebrates (e.g.…”

“…Note that this picture is incomplete and hypothetical with respect to some details and ignores the specific phylogenetic constraints characterizing individual phyla and species (see text). The generalized cellular processes depicted on the left probably have their specific functional consequences in tissues like brain, heart or muscle depicted on the right (experimental results and concepts adopted from Pörtner and Reipschläger, 1996;Reipschläger and Pörtner, 1996;Reipschläger et al, 1997;Larsen et al, 1997;Pörtner et al, 2000;Pörtner, 2002, 2003;Pörtner, 2002;Shirayama, 2002;Ishimatsu et al, 2004;Kurihara et al, 2004).…”

“…Respiratory changes titrate nonbicarbonate buffer values with changing PCO 2 and lead to pH decreases and an accumulation of bicarbonate. In only a few species has this approach been combined with an analysis of CO 2 effects on metabolism, not only when hypoxia and anaerobic metabolism occur (Reipschläger et al, 1997) but also in the sense that CO 2 may affect overall metabolic rate and the partitioning of energy between individual metabolic processes by changes in either one or a combination of the different acid-base parameters in the water or in body compartments Pörtner et al, 2000;Langenbuch and Pörtner, 2002).…”

Energy budget of hepatocytes from Antarctic fish (Pachycara brachycephalumandLepidonotothen kempi) as a function of ambient CO2: pH-dependent limitations of cellular protein biosynthesis?

“…Concomitant shifts in cellular N metabolism indicate that a change in the use of amino acid substrates as well as a decrease of protein biosynthesis rates occurs under acidosis (Langenbuch and Pörtner, 2002). Furthermore, a drop in neuronal and motor activity, caused by the accumulation of the neurotransmitter adenosine, supports metabolic depression during hypercapnia and particularly during exposure to combined anoxia and hypercapnia (Reipschläger et al, 1997). The latter data clearly show that the problem of CO2 tolerance is not only defined at the cellular level.…”

Integrating climate-related stressor effects on marine organisms: unifying principles linking molecule to ecosystem-level changes

“…Overall, hypoxia and CO 2 constrain active tolerance to thermal extremes and rather stimulate the mechanisms supporting passive tolerance by enforcing metabolic depression (Fig. 5), for example via a decrease in body fluid pH or an accumulation of adenosine in nervous tissues (Reipschläger & Pörtner 1996, Reipschläger et al 1997. This may be useful for extending passive tolerance periods as in the intertidal.…”