Rapid initiation of ion transport occurs in the lower Malpighian tubule of the insect Rhodnius prolixus following feeding in vivo or stimulation with 5-hydroxytryptamine (5-HT) in vitro. Using the electron microscope, we have conducted a morphometric analysis of cells in the lowest one-third of the lower tubule, demonstrating that 5-HT also induces mitochondrial movement and microvillar growth simultaneously with, but independent of, the onset of ion transport. Mitochondria move from a position below the cell cortex to one inside the microvilli within 10 min of stimulation with 5-HT, resulting in an 8- to 10-fold increase in the volume of mitochondria within the microvilli. Previous findings indicated that mitochondrial movement is dependent on actin-containing microfilaments, but not microtubules. As the mitochondria enter the microvillus, the core microfilaments are reorganized into a sheath of microfilaments, which extends closely parallel to the outer mitochondrial membrane down into the cell interior. This sheath of microfilaments is also observed around mitochondria in the axopods. We suggest that the core microfilaments are responsible for mitochondrial movement into the microvilli and axopods. Stimulation with 5-HT induces a shift in mitochondrial configuration from orthodox to condensed, indicating a possible increase in oxidative phosphorylation. Following stimulation, the microvilli grow about 3 X in volume and 2.5 X in surface area. These increases are more than can be accounted for by mitochondrial invasion and must involve the addition of new membrane and microfilament polymerization. The observed changes - microvillar growth, insertion of additional membrane, activation and movement of mitochondria adjacent to the ion transport membrane - are described in the light of their significance in ion transport. A simple model is proposed which unifies the observed ultrastructural changes and known ion movements in the lower tubule.

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