Ordered transmembrane and extracellular structure in squid photoreceptor microvilli

Invertebrate retinas contain hexagonal arrays of microvilli that form the honeycomb structure of rhabdome photoreceptors. The largest and most crystalline rhabdomes are found in the squid retina, and we have taken advantage of their unique properties to derive a model for the electron density distribution in microvillar membranes using low angle X-ray diffraction combined with correlation averaging of electron microscope images. The model electron density map, calculated to a resolution of approximately 35 A, shows an unusually high protein content in the membranes. This may be associated with a dense meshwork of membrane junctions between neighboring microvilli as revealed by electron microscope image analysis. Membrane pair contacts are resolved as two or more strands of density crossing the membranes. The microvilli are also linked together by Y-shaped junctions at their three-way contacts. These two sorts of junctions link the membranes into a three-dimensional array and partition them into a mosaic of deformable and rigid domains. This arrangement maintains a remarkable degree of long-range order in squid rhabdomes, and may be responsible for the alignment of rhodopsin molecules. The structural order observed is necessary for these photoreceptors to achieve their high sensitivity to the plane of polarized light. Rhodopsin constitutes about one-half the microvillar protein. The remaining proteins, which can be divided into approximately equal detergent-soluble and insoluble fractions, could account for the composition of the new structures described.