High-energy turnover at low temperatures: recovery from exhaustive exercise in Antarctic and temperate eelpouts

Abstract

Earlier work on Notothenioids led to the hypothesis that a reduced glycolytic capacity is a general adaptation to low temperatures in Antarctic fish. In our study this hypothesis was reinvestigated by comparing changes in the metabolic status of the white musculature in two related zoarcid species, the stenothermal Antarctic eelpout Pachycara brachycephalum and the eurythermal Zoarces viviparus during exercise and subsequent recovery at 0°C. In both species, strenuous exercise caused a similar increase in white muscle lactate, a drop in intracellular pH (pHi) by about 0.5 pH units, and a 90% depletion of phosphocreatine. This is the first study on Antarctic fish that shows an increase in white muscle lactate concentrations. Thus the hypothesis that a reduced importance of the glycolytic pathway is characteristic for cold-adapted polar fish cannot hold. The recovery process, especially the clearance of white muscle lactate, is significantly faster in the Antarctic than in temperate eelpout. Based on metabolite data, we calculated that during the first hour of recovery aerobic metabolism is increased 6.6-fold compared with resting rates in P. brachycephalum vs. an only 2.9-fold increase in Z. viviparus. This strong stimulation of aerobic metabolism despite low temperatures may be caused by a pronounced increase of free ADP levels, in the context of higher levels of pHi and ATP, which is observed in the Antarctic species. Although basal metabolic rates are identical in both species, the comparison of metabolic rates during situations of high-energy turnover reveals that the stenothermal P. brachycephalum shows a higher degree of metabolic cold compensation than the eurythermal Z. viviparus. Muscular fatigue after escape swimming may be caused by a drop of the free energy change of ATP hydrolysis, which is shown to fall below critical levels for cellular ATPases in exhausted animals of both species.

Influence of temperature, habitat and body mass on routine metabolic rates of Subantarctic teleosts

“…A Q 10 with a similar value, around 9, has been calculated for the Antarctic eelpout Pachycara brachycephalum at 3-9ºC (Hardewig et al, 1998). It is therefore possible to assume a greater effect of temperature limiting the oxygen consumption for the sluggish Subantarctic eelpout in this thermal range.…”

Critical temperatures in the cephalopodSepia officinalisinvestigated usingin vivo31P NMR spectroscopy

“…pH i would be significantly decreased to 7.19 and ͉dG/d͉ would drop to below 44·kJ·mol -1 in the radial fibre compartment of the mantle organ. These calculations correspond to similar ͉dG/d͉ values for mantle muscle of three species of squid following fatiguing exercise, which ranged from 42 to 47·kJ·mol -1 , while values for two species of exercise-fatigued eelpout (P. brachycephalum, Z. viviparous) (Hardewig et al, 1998) white muscle ranged from 46.6 to 48·kJ·mol -1 . Possibly, reductions in the free energy of ATP hydrolysis as calculated for cuttlefish radial muscle could contribute to muscle fibre fatigue in that vital muscle due to functional impairments of ATPase functions.…”

An examination of the metabolic processes underpinning critical swimming in Atlantic cod (Gadus morhua L.) using in vivo31P-NMR spectroscopy

“…The consequent drop in pH i indicated that anaerobic metabolism was also being used to maintain ATP concentrations. Both Pörtner et al and Hardewig et al (Hardewig et al, 1998) have argued that as the cytosol becomes more acidic and, more importantly, as the phosphagen (PCr in case of fish) is lysed to Pi and Cr, there is a drop in ⌬G/d ATP . For two species of Zoarcid eelpouts, the free energy of ATP hydrolysis was observed to drop from -60·kJ·mol -1 to approximately -46·kJ·mol -1 and for rainbow trout, ⌬G/d ATP dropped from -60 to -47·kJ·mol -1 after exhaustive exercise (Hardewig et al, 1998).…”

“…Building on previous work (Hibberd et al, 1985), Debold et al add that inorganic phosphate and H + also reduce the force generated by cross-bridge cycling (Debold et al, 2004). Others have argued that a drop in the Gibbs free energy of ATP hydrolysis (dG/d ATP ) below a certain threshold results in fatigue (Hardewig et al, 1998).…”

“…where Cr is the estimated creatine concentration in mol·g -1 , PCr is phosphocreatine concentration in mol·g -1 and 0.65 is the ratio of PCr:Cr measured in resting fish white muscle (Hardewig et al, 1998).…”