Abstract
BackgroundFat storage is required for the life cycle of many organisms. The primary fat depot for most vertebrates is white adipose tissue. However, in primitive vertebrates (e.g., agnathan group and elasmobranchs), the liver is usually responsible for fat storage. Among the vertebrates, amphibians have a unique status, as their larvae live in the water and exhibit some primitive traits that are similar to fish. Although it has been recognized that adult frogs use their abdominal white adipose tissue as a primary fat depot, how tadpoles store their fat is still inconclusive. The metabolic traits and physiological functions of primitive fat depots may have wide-ranging implications on the pathology of abnormal lipid deposition in mammals and the evolution of fat storage.ResultsRana omeimontis tadpoles used their liver as the primary fat depot. In sufficiently fed tadpoles at stage 30–31, the hepatosomatic index (HSI) reached up to 7%, and triglycerides (TG) accounted for 15% of liver weight. Their liver resembled white adipose tissue in histological morphology, characterized by polygonal hepatocytes filled with fat. Their liver metabolic composition was unique, characterized by the dominance of maltotriose, arachidonic acid and dipeptides in soluble carbohydrates, free fatty acids and amino acids. Hepatic fat was the major metabolic fuel of fasted R. omeimontis tadpoles, which had similar reserve mobilization and allocation patterns as mammals. From a developmental perspective, hepatic fat was important to fuel late metamorphic climax. Interestingly, starvation induced accelerated metamorphosis in tadpoles with high HSI (4.96 ± 0.21%). However, this phenomenon was not observed in tadpoles with low HSI (2.71 ± 0.16%), even though they had similar initial body weight and developmental stage. Hepatic fat abundance was the most prominent difference between the two groups.ConclusionTo the best of our knowledge, this is the first report that liver can be the primary fat depot in vertebrates with higher evolutionary status than bony fish. The unique hepatic histological and metabolic traits likely either guard their liver against lipotoxicity or make their hepatocytes adapt to fat accumulation. This fatty liver could be a primitive counterpart of mammalian white adipose tissue (WAT). In addition, our study showed that the hepatic reserves of tadpoles, especially TG content, may provide body condition signals to modulate metamorphosis.
Highlights
Fat storage is required for the life cycle of many organisms
The histological patterns of their livers resembled the white adipose tissue (WAT), with enlarged hepatocytes filled by neutral lipid, which resulted in marginalized cell nuclei and glycogen (Fig. 2d-f)
The liver of geese should not be as significant as their adipose tissues in fat storage because their artificial fatty liver resulted from compulsive lipogenesis due to excessive carbohydrate intake and was impelled by the limited capacity of fat exportation from liver to peripheral WAT [13]
Summary
Fat storage is required for the life cycle of many organisms. The primary fat depot for most vertebrates is white adipose tissue. The metabolic traits and physiological functions of primitive fat depots may have wide-ranging implications on the pathology of abnormal lipid deposition in mammals and the evolution of fat storage. Amphibians, reptiles, birds and mammals, even though liver is still responsible for lipogenesis, white adipose tissue (WAT) appears and replaces liver to become their primary fat depot [2, 7,8,9,10]. Fat deposition in the liver is likely a primitive trait of vertebrate evolution [2] From this point of view, the metabolic traits and physiological functions of the primitive fatty liver may have wideranging implications on the pathology of abnormal lipid deposition in humans and shed light on the driving force behind evolution of fat depot [15]
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