Functional design of microvilli in the Malpighian tubules of the insect Rhodnius prolixus

Abstract

The Malpighian tubules of Rhodnius prolixus are divided into two regions; the upper tubule, which is the site of isosmotic secretion and haemolymph filtration, and the lower tubule where water and KCl are resorbed. In the upper tubule the microvilli are arranged in clumps consisting of several hundred microvilli lying closely parallel. The microvillar plasma membranes do not touch but are held approximately equal to 16 nm apart along the full length of the microvilli. As a consequence, the extracellular space between the microvilli consists of long narrow channels. A morphometric analysis of extracellular, cytoplasmic, endoplasmic reticular and mitochondrial volume within the clumps was conducted. Using the secretion rate of the epithelium and the channel dimensions, it was calculated that the mean residence time for secreted fluid in the intermicrovillar spaces was approximately equal to 0.4s. In view of our current knowledge of the physiology and morphology of the upper tubule, it is argued: (1) that osmotically driven water passes principally through the cells, not the junctional spaces; and (2) that the microvillar clumps are a morphological specialization, which serves to maximize solute-water coupling in the upper tubule. The microvilli in the lower tubule are free-standing, with no pattern of clumping as in the upper tubule. The axopods are about twice as long as the microvilli (10-14 micron) and are found in all regions of the lower tubule. This is in agreement with the proposal that the motile axopods serve to propel uric acid crystals through the lower tubule. No morphological difference was found between the upper and lower halves of the lower tubule, although the two portions are known to be physiologically distinct.