The Changing State of Surfactant Lipids: New Insights from Ancient Animals

Abstract

Pulmonary surfactant is a mixture of phospholipids (including disaturated phospholipids), cholesterol and proteins lining the air-liquid interface within the lung. Surfactant acts to reduce surface tension, thereby increasing lung compliance and also preventing edema. The saccular lungs, or other gas-holding structures, of nonmammals have 7-70% more surfactant/cm 2 of surface than lungs of mammals. Nonmammalian surfactant acts as an antiglue that decreases the inflation pressures of collapsed lungs by reducing the adherence of apposing epithelial surfaces. The autonomic nervous system appears to be the primary system controlling release of surfactant in nonmammals. The lipid composition is highly conserved within the vertebrates, except that surfactant of teleost fish is dominated by cholesterol whereas tetrapod surfactant consists primarily of disaturated phospholipids (DSP). The dipnoan Neoceratodus forsteri demonstrates a "fish-type" surfactant profile while the other derived dipnoans demonstrate a surfactant profile similar to that of tetrapods. Homology of the surfactant protein SP-A within the vertebrates points to a single evolutionary origin for the system and indicates that fish surfactant is a "protosurfactant". Amongst the tetrapods, the relative proportions of DSP and cholesterol vary in response to lung structure, habitat, and body temperature (T b ) but not in relation to phytogeny. The cholesterol content of surfactant is elevated in species with simple saccular lungs, in aquatic species, and in species with low T b . The DSP content is highest in complex lungs, particularly of aquatic species or species with high T b . The cholesterol content of surfactant also increases in response to acute decreases in T b in lizards and torpid marsupials, presumably to maintain fluidity of the lipid mixture.