The evolutionary significance of pulmonary surfactant in lungfish (Dipnoi)

In this study, we characterized surfactant lipids from the lungs of the lungfish, Protopterus annectens, Lepidosiren paradoxa, and Neoceratodus fosteri (Sarcopterygiia: Dipnoi). We quantified the types of phospholipids present, the amounts of total phospholipid, disaturated phospholipid (DSP)--purported to be the primary surface tension-controlling agent--and cholesterol (CHOL), an important fluidizer. The surfactant phospholipid profiles of all three lungfish were very similar to each other and those of many other animals reported previously. Phosphatidylcholine was the dominant phospholipid (60% to 80%); phosphatidylglycerol was virtually absent; and there was a significant proportion of the combination of phosphatidylserine and phosphatidylinositol (10%). The Australian lungfish N. forsteri possessed a surfactant 5 times richer in CHOL and 2 and 3 times poorer in DSP than the surfactant of the African lungfish P. annectens and the South American lungfish L. paradoxa, respectively. Hence, the CHOL/DSP mass ratio of N. forsteri was 12 and 20 times greater than that of P. annectens and L. paradoxa, respectively. Therefore, the surfactant composition of the two derived species of lungfish (P. annectens and L. paradoxa) very closely resembles that of amphibians, whereas surfactant from the primitive lungfish (N. forsteri) is almost identical to that of the primitive air-breathing actinopterygiian fish. Thus, it is likely that pulmonary surfactant had only a single origin, coinciding with that of the vertebrates. As with most nonmammalian vertebrates, it is possible that lungfish surfactant functions as an antiglue at low lung volumes or when the lungs are completely collapsed. Furthermore, it appears that within a species, an increase in lung development correlates with an increase in the relative amount of surfactant cholesterol and a decrease in the phospholipid saturation level.