Pentastomids and the tetrapod lung

Abstract

Pentastomids comprise a highly specialized taxon of arthropod-like parasites that probably became adapted to the lungs of amphibians and reptiles early in their long evolutionary history. Few other macroparasites exploit this particular niche. Pentastomids are often large, long-lived and yet they cause little observable pathology in lungs, despite being haematophagous. The lungs of all tetrapods are lined with pulmonary surfactant, a remarkable biological material consisting of a complex mixture of phospholipids, neutral lipids and proteins that has the unique ability to disperse over the air-liquid lining of the lung. In the lower tetrapods it acts as an anti-glue preventing adhesion of respiratory surfaces when lungs collapse during swallowing prey or upon expiration. In mammals, pulmonary surfactant also plays a critical role regulating the activity of alveolar macrophages, the predominant phagocytes of the lower airways and alveoli. This review outlines the evidence suggesting that lung-dwelling pentastomids, and also nymphs encysted in the tissues of mammalian intermediate hosts, evade immune surveillance and reduce inflammation by coating the chitinous cuticle with a their own stage-specific surfactant. The lipid composition of surfactant derived from lung instars of the pentastomid Porocephalus crotali cultured in vitro is very similar to that recovered from the lung of its snake host. Pentastomid surfactant, visualised as lamellate droplets within sub-parietal cells, is delivered to the cuticle via chitin-lined efferent ducts that erupt at a surface density of < 400 mm(-2). The fidelity of the system, which ensures that every part of the cuticle surface is membrane-coated, testifies to its strategic importance. Two other extensive glands discharge membrane-associated (hydrophobic?) proteins onto the hooks and head; some have been purified and partly characterized but their role in minimising inflammatory responses is, as yet, undetermined.