Glycerol-3-phosphatase and not lipid recycling is the primary pathway in the accumulation of high concentrations of glycerol in rainbow smelt (Osmerus mordax)

Abstract

Rainbow smelt is a small fish that accumulates glycerol in winter as a cryoprotectant when the animal is in seawater. Glycerol is synthesized in liver from different substrates that all lead to the formation of glycerol-3-phosphate (G3P). This study assesses whether glycerol is produced by a direct dephosphorylation of G3P by a phosphatase (G3Pase) or by a cycling through the glycerolipid pool followed by lipolysis. Foremost, concentrations of on-board glycerolipids and activity of G3Pase and of enzymes involved in lipid metabolism were measured in smelt liver over the glycerol cycle. Concentrations of on-board glycerolipids did not change over the cycle and were too low to significantly contribute directly to glycerol production but activities of enzymes involved in both potential pathways were up-regulated at the onset of glycerol accumulation. A second experiment conducted with isolated hepatic cells producing glycerol showed 1) that on-board glycerolipids were not sufficient to produce the glycerol released even though phospholipids could account for up to 17% of it, 2) that carbon cycling through the glycerolipid pool was not involved as glycerol was produced at similar rates following inhibition of this pathway, and 3) that G3Pase activity measured was sufficient to allow the synthesis of glycerol at the rate observed. These results are the first to clearly support G3Pase as the metabolic step leading to glycerol production in rainbow smelt and the first to provide strong support for a G3Pase in any animal species.