Partial amino acid catabolism leading to the formation of alanine in Periophthalmodon schlosseri (mudskipper): a strategy that facilitates the use of amino acids as an energy source during locomotory activity on land.

Abstract

When the mudskipper Periophthalmodon schlosseri was exposed to terrestrial conditions under a 12h:12h dark:light regime the fish could be very active, and levels of total free amino acids increased significantly in the muscle and plasma. Alanine levels increased threefold in the muscle, fourfold in the liver and twofold in the plasma. Similar phenomena were not observed in the more aquatic mudskipper, Boleophthalmus boddaerti. From these results, we concluded that P. schlosseri was capable of partial catabolism of certain amino acids to support activity on land. The amino groups of these amino acids were transferred directly or indirectly to pyruvate to form alanine. The resulting carbon chain was fed into the Krebs cycle and partially oxidized to malate, which could replenish pyruvate through the function of malic enzyme. This favourable ATP yield from partial amino acid catabolism was not accompanied by a net release of ammonia. Such an adaptation would be advantageous to P. schlosseri confronted with the problem of ammonia excretion during aerial exposure. Indeed, when P. schlosseri were forced to exercise on land after 24 h of aerial exposure, the alanine level in the muscles increased significantly, with no apparent change in glycogen content. In addition, there was no significant change in the ATP level and energy charge of the muscle. In contrast, when B. boddaerti were exercised on land, glycogen levels in the muscles decreased significantly and lactate levels increased. In addition, muscle energy charge was not maintained and the ATP level decreased significantly. Hence, it was concluded that when P. schlosseri were active on land, they were capable of using certain amino acids as a metabolic fuel, and avoided ammonia toxicity through partial amino acid catabolism. Such a strategy is the most cost-effective way of slowing down internal ammonia build-up without involving energy-expensive ammonia detoxification pathways. Furthermore, an examination of the balance between nitrogenous excretion and accumulation in a 70 g P. schlosseri revealed that degradation of amino acids in general was likely to be suppressed to slow down the build-up of ammonia internally. It is possible that such a strategy may be widely adopted, especially by obligatory air-breathing fishes, to avoid ammonia intoxication during aerial exposure.