Ho. Portner et al., METABOLIC AND ENERGY CORRELATES OF INTRACELLULAR PH IN PROGRESSIVE FATIGUE OF SQUID (L-BREVIS) MANTLE MUSCLE, American journal of physiology. Regulatory, integrative and comparative physiology, 40(5), 1996, pp. 1403-1414
Squid (Lolliguncula brevis) were exercised at increasing swimming spee
ds to allow us to analyze the correlated changes in intracellular meta
bolic, acid-base, and energy status of the mantle musculature. Beyond
a critical swimming velocity of 1.5 mantle lengths/s, an intracellular
acidosis developed that was caused by an initial base loss from the c
ells, the onset of respiratory acidification, and, predominantly, octo
pine formation. The acidosis was correlated with decreasing levels of
phospho-L arginine and, thus, supported ATP buffering at the expense o
f the phosphagen. Monohydrogenphosphate, the actual substrate of glyco
gen phosphorylase, accumulated, enabling glycogen degradation, despite
progressive acidosis. In addition to octopine, succinate, and alpha-g
lycerophosphate accumulation, the onset of acidosis characterizes the
critical velocity and indicates the transition to a non-steady-state t
ime-limited situation. Accordingly, swimming above the critical veloci
ty caused cellular energy levels (in vivo Gibbs free energy change of
ATP hydrolysis) to fall. A minimal value was reached at about -45 kJ/m
ol. Model calculations demonstrate that changes in free Mg2+ levels on
ly minimally affect ATP free energy, but mimumum levels are relevant i
n maintaining functional concentrations of Mg2+-complexed adenylates.
Model calculations also reveal that phosphagen breakdown enabled L. br
evis to reach swimming speeds about three times higher than the critic
al velocity. Comparison of two offshore squid species (Loligo pealei a
nd Ilex illecebrosus) with the estuarine squid L. brevis indicates tha
t the latter uses a strategy to delay the exploitation of high-energy
phosphates and protect energy levels at higher than the minimum levels
(-42 kJ/mol) characterizing fatigue in the other species. A more econ
omical use of anaerobic resources and an early reduction in performanc
e may enable L. brevis to tolerate more extreme environmental conditio
ns in shallow estuarine waters and even hypoxic environments and to pr
event a fatal depletion of energy stores.