Alveolar sacs of Tetrahymena: ultrastructural characteristics and similarities to subsurface cisterns of muscle and nerve

Abstract

The ultrastructure of the layer of alveolar sacs of Tetrahymena thermophila and its relationship with the plasma membrane were examined in thin sections and freeze-fracture replicas. In thin sections, the plasma membrane and outer alveolar membrane are seen to parallel each other closely and are linked by struts 9 nm wide spaced at 9 nm intervals. The plasma and alveolar membranes have different ultrastructural characteristics. The unit-membrane structure of the plasma membrane is asymmetric and thicker than that of the alveolar membrane. The unit-membrane structure of the alveolar membrane is symmetric. The lateral borders of adjacent alveolar sacs are closely apposed and flattened against one another, forming alveolar sutures. The pellicle at the cell surface, consisting of the plasma membrane, the alveolar sacs and the underlying epiplasm, overlies a single layer of mitochondria and a single layer of flattened cisterns of rough-surfaced endoplasmic reticulum (RER). Examination of freeze-fracture replicas reveals that the plasma membrane and the inner and outer alveolar membranes each have a unique population of unit-membrane particles. This suggests that they are separate membrane domains. The appearance of alveolar sutures, i.e. the apposed lateral borders of adjacent alveolar sacs, suggests that the alveolar membranes in this region are more rigid than elsewhere and may be sealed together by an adhesive substance. Interruptions in the sutures are interpreted as indicating that adjacent alveolar sacs are connected by small isthmuses or channels, confirming earlier reports that alveolar sacs are large chambers within a continuous, interconnected system. Alveolar sacs, in their relationship with the plasma membrane, closely resemble the subsurface cisterns of nerve and muscle cells. In muscle cells, the cisterns participate in the regulation of the cytoplasmic calcium ion concentration that controls contraction of myofilaments. Several functions of the surface of Tetrahymena, e.g. secretion of mucocysts and ciliary motility, are believed to be calcium-dependent, and the alveolar sacs may play a role in mechanisms that control the concentration of this divalent cation in localized regions along the cell surface. The alveolar sacs contain laminated inclusion bodies that appear to be rich in phospholipid. The inclusion bodies may represent reserves of phospholipid material stored in preparation for membrane formation.