Electron microscopy reveals novel external specialized organs housing bacteria in eagle ray tapeworms
View/ Open
Issue Date
2021-01-22Author
Caira, Janine N.
Jensen, Kirsten
Publisher
Public Library of Science
Type
Article
Article Version
Scholarly/refereed, publisher version
Rights
© 2021 Caira, Jensen. This is an open access article distributed under the terms of the Creative Commons Attribution License.
Metadata
Show full item recordAbstract
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.
Collections
Citation
Caira JN, Jensen K (2021) Electron microscopy reveals novel external specialized organs housing bacteria in eagle ray tapeworms. PLoS ONE 16(1): e0244586. https://doi.org/10.1371/journal.pone.0244586
Items in KU ScholarWorks are protected by copyright, with all rights reserved, unless otherwise indicated.
We want to hear from you! Please share your stories about how Open Access to this item benefits YOU.