Electron microscopy reveals novel external specialized organs housing bacteria in eagle ray tapeworms

Abstract

Nutritionally-based mutualisms with bacteria are known to occur in a wide array of invertebrate phyla, although less commonly in the Platyhelminthes. Here we report what appears to be a novel example of this type of association in two geographically disparate and phylogenetically distant species of tapeworms of eagle rays—the lecanicephalidean Elicilacunosus dharmadii off the island of Borneo and the tetraphyllidean Caulobothrium multispelaeum off Senegal. Scanning and transmission electron microscopy revealed that the grooves and apertures on the outer surfaces of both tapeworms open into expansive cavities housing concentrations of bacteria. This led us to reject the original hypothesis that these structures, and their associated mucopolysaccharides, aid in attachment to the host mucosa. The cavities were found to be specialized in-foldings of the tapeworm body that were lined with particularly elongate filitriches. Given tapeworms lack a gut and employ filitriches to assist in nutrient absorption, enhanced nutrient uptake likely occurs in the cavities. Each tapeworm species appeared to host different bacterial monocultures; those in E. dharmadii were coccoid-like in form, while those in C. multispelaeum were bacillus-like. The presence of bacteria in a specialized structure of this nature suggests the structure is a symbiotic organ. Tapeworms are fully capable of obtaining their own nutrients, and thus the bacteria likely serve merely to supplement their diet. Given the bacteria were also extracellular, this structure is more consistent with a mycetome than a trophosome. To our knowledge, this is not only the first evidence of an external symbiotic organ of any type in a nutritionally-based mutualism, but also the first description of a mycetome in a group of invertebrates that lacks a digestive system. The factors that might account for the independent evolution of this unique association in these unrelated tapeworms are unclear—especially given that none of their closest relatives exhibit any evidence of the phenomenon.