Energy metabolism and ATP free-energy change of the intertidal worm Sipunculus nudus below a critical temperature

Abstract

The intertidal worm Sipunculus nudus was exposed to various temperatures for an analysis of the integrated changes in energy and acid-base status. Animals were incubated in sea water or maintained for up to 8 days at 4 and 0°C while dwelling in the sediment. Cannulation of the animals prior to experimentation allowed the analysis of blood gas parameters (P -, P !-and pH). P -fell to 0 torr within 8 days at 0°C. A simultaneous reduction of ventilatory activity was derived from measurements of the pattern of coelomic fluid pressure changes associated with ventilatory movements. The increase in P !-and an onset of anaerobic metabolism, indicated by the accumulation of end products like acetate and propionate both in the coelomic fluid and the body wall musculature, led to the development of a progressive acidosis and a deviation from the alphastat regulation of intracellular pH seen in unburied animals. The drop in intracellular pH together with the depletion of the adenylates and the phosphagen, phospho-L-arginine, reflect a significant decrease in the Gibb's free-energy change of ATP hydrolysis. These changes are interpreted to indicate lethal cold injuries, because recovery was not possible when the animals were returned to 12°C after more than 2 days of exposure to 0°C. A low critical temperature indicating the onset of cold-induced anaerobiosis is concluded to exist below 4°C owing to the insufficient response of the ventilatory system to the developing hypoxia.

Oxygen limited thermal tolerance in fish?

“…Nonetheless, oxygen supply capacity becomes limiting in temperate water breathers exposed to cold temperatures, observed in cod (Lannig et al, 2004) in similar ways as seen in a temperate crustacean (Frederich and Pörtner, 2000) or in annelids and sipunculids (Zielinski and Pörtner, 1996;Sommer et al, 1997). The drop in venous P O 2 (in fish) or arterial P O 2 (in the crustacean) and the transition to anaerobic metabolism in the cold indicate a limited functional capacity of oxygen supply mechanisms likely elicited by cold induced slowing.…”

“…A temperature dependent optimization of oxygen supply capacity was visible in the form of maximized arterial P O 2 within a limited temperature range, equivalent to the window of mean temperatures in the natural environment (Frederich and Pörtner, 2000). Limitation of both ventilatory and circulatory capacities towards thermal extremes was found to explain these patterns of body fluid oxygenation (Zielinski and Pörtner, 1996;Frederich and Pörtner, 2000).…”

“…In this context, the question has regained interest whether limitations in oxygen availability or supply are involved in thermal limitation. Early evidence collected in marine invertebrates (annelids and sipunculids) demonstrated a transition to anaerobic metabolism (including mitochondrial anaerobiosis) at both cold and warm temperature extremes (Zielinski and Pörtner, 1996;Sommer et al, 1997), later on confirmed in crustaceans (Frederich and Pörtner, 2000) and molluscs, i.e. bivalves, gastropods and cephalopods (Pörtner and Zielinski, 1998;Pörtner et al, 1999;Peck et al, 2002;Sokolova and Pörtner, 2003).…”

“…bivalves, gastropods and cephalopods (Pörtner and Zielinski, 1998;Pörtner et al, 1999;Peck et al, 2002;Sokolova and Pörtner, 2003). Studies in a sipunculid (Sipunculus nudus, Zielinski and Pörtner, 1996) and the spider crab (Maja squinado, Frederich and Pörtner, 2000) investigated the pattern of coelomic fluid/haemolymph oxygen tensions in relation to warming and/or cooling and demonstrated development of hypoxia which preceded the onset of anaerobic metabolism towards both cold and warm temperature extremes. A temperature dependent optimization of oxygen supply capacity was visible in the form of maximized arterial P O 2 within a limited temperature range, equivalent to the window of mean temperatures in the natural environment (Frederich and Pörtner, 2000).…”

“…The work of Zielinski and Pörtner (1996), Sommer et al (1997), Pörtner et al (1999) and Frederich and Pörtner (2000) in marine invertebrates led to the concept of oxygen-limited thermal tolerance, which suggests that towards cold or warm extremes progressively inadequate oxygen supply and thus, decreasing body fluid oxygen levels finally lead to temperature induced anaerobiosis. Terminology was applied by adopting the one used in Shelford's law of tolerance (Shelford, 1931).…”