skip to main content

Explore Research Products in the NSF-PAR

Title: Electron microscopy reveals novel external specialized organs housing bacteria in eagle ray tapeworms
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.  more » « less
Award ID(s):
1921411 1921404
NSF-PAR ID:
10250499
Author(s) / Creator(s):
;
Editor(s):
Ruiz-Rodriguez, Magdalena
Date Published:
Journal Name:
PLOS ONE
Volume:
16
Issue:
1
ISSN:
1932-6203
Page Range / eLocation ID:
e0244586
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. ; ( , Invertebrate Systematics)
    Worsaae, Katrine (Ed.)
    The three members of the lecanicephalidean tapeworm family Eniochobothriidae are unusual among tapeworms in that they lack a vagina and possess a series of expanded proglottids forming a trough at the anterior end of their body. They exclusively parasitise cownose rays of the genus Rhinoptera (Myliobatiformes: Rhinopteridae). New collections from six of the nine known species of cownose rays from the waters off Australia, Mexico, Mozambique, Senegal, Taiwan and the United States (off Mississippi, Louisiana and South Carolina) yielded eight new species and a new genus of eniochobothriids. Here we erect Amiculucestus, gen. nov. and describe six of the eight new species – four in the new genus and two in Eniochobothrium – expanding the number of genera in the family to two and the number of described species in the family to nine. Morphological work was based on light and scanning electron microscopy. The tree resulting from a maximum likelihood analysis of sequence data for the D1–D3 region of the 28S rDNA gene for 11 species of eniochobothriids supports the reciprocal monophyly of both genera. The mode of attachment to the mucosal surface of the spiral intestine of the host was investigated using histological sections of worms in situ. These cestodes appear to use the anterior trough-like portion of their body, which consists of an unusual series of barren proglottids, rather than their scolex, to attach to the mucosal surface. Based on our new collections, we estimate that the total number of eniochobothriids across the globe does not exceed 27 species. ZooBank LSID: urn:lsid:zoobank.org:pub:0740EC72‐AC3F‐43AA‐BD41‐B9820BA9D0CE 
    more » « less
  2. ; ; ; ; ; ; ; ; ; ; et al ( , Proceedings of the National Academy of Sciences)

    The recent recognition that many symbioses exhibit daily rhythms has encouraged research into the partner dialogue that drives these biological oscillations. Here we characterized the pivotal role of the versatile cytokine macrophage migration inhibitory factor (MIF) in regulating a metabolic rhythm in the model light-organ symbiosis betweenEuprymna scolopesandVibrio fischeri. As the juvenile host matures, it develops complex daily rhythms characterized by profound changes in the association, from gene expression to behavior. One such rhythm is a diurnal shift in symbiont metabolism triggered by the periodic provision of a specific nutrient by the mature host: each night the symbionts catabolize chitin released from hemocytes (phagocytic immune cells) that traffic into the light-organ crypts, where the population ofV. fischericells resides. Nocturnal migration of these macrophage-like cells, together with identification of anE. scolopesMIF (EsMIF) in the light-organ transcriptome, led us to ask whether EsMIF might be the gatekeeper controlling the periodic movement of the hemocytes. Western blots, ELISAs, and confocal immunocytochemistry showed EsMIF was at highest abundance in the light organ. Its concentration there was lowest at night, when hemocytes entered the crypts. EsMIF inhibited migration of isolated hemocytes, whereas exported bacterial products, including peptidoglycan derivatives and secreted chitin catabolites, induced migration. These results provide evidence that the nocturnal decrease in EsMIF concentration permits the hemocytes to be drawn into the crypts, delivering chitin. This nutritional function for a cytokine offers the basis for the diurnal rhythms underlying a dynamic symbiotic conversation.

     
    more » « less
  3. ; ; ( , MicrobiologyOpen)
    Abstract

    The binary association between the squid,Euprymna scolopes, and its symbiont,Vibrio fischeri, serves as a model system to study interactions between beneficial bacteria and the innate immune system. Previous research demonstrated that binding of the squid's immune cells, hemocytes, toV. fischeriis altered if the symbiont is removed from the light organ, suggesting that host colonization alters hemocyte recognition ofV. fischeri. To investigate the influence of symbiosis on immune maturation during development, we characterized hemocyte binding and phagocytosis ofV. fischeriand nonsymbioticVibrio harveyifrom symbiotic (sym) and aposymbiotic (apo) juveniles, and wild‐caught and laboratory‐raised sym and apo adults. Our results demonstrate that while light organ colonization byV. fischeridid not alter juvenile hemocyte response, these cells bound a similar number ofV. fischeriandV. harveyiyet phagocytosed onlyV. harveyi. Our results also indicate that long‐term colonization altered the adult hemocyte response toV. fischeribut notV. harveyi. All hemocytes from adult squid, regardless of apo or sym state, both bound and phagocytosed a similar number ofV. harveyiwhile hemocytes from both wild‐caught and sym‐raised adults bound significantly fewerV. fischeri, although moreV. fischeriwere phagocytosed by hemocytes from wild‐caught animals. In contrast, hemocytes from apo‐raised squid bound similar numbers of bothV. fischeriandV. harveyi, although moreV. harveyicells were engulfed, suggesting that blood cells from apo‐raised adults behaved similarly to juvenile hosts. Taken together, these data suggest that persistent colonization by the light organ symbiont is required for hemocytes to differentially bind and phagocytoseV. fischeri. The cellular immune system ofE. scolopeslikely possesses multiple mechanisms at different developmental stages to promote a specific and life‐long interaction with the symbiont.

     
    more » « less
  4. ; ; ( , BMC Ecology and Evolution)
    Abstract Background Feather feeding lice are abundant and diverse ectoparasites that complete their entire life cycle on an avian host. The principal or sole source of nutrition for these lice is feathers. Feathers appear to lack four amino acids that the lice would require to complete development and reproduce. Several insect groups have acquired heritable and intracellular bacteria that can synthesize metabolites absent in an insect’s diet, allowing insects to feed exclusively on nutrient-poor resources. Multiple species of feather feeding lice have been shown to harbor heritable and intracellular bacteria. We expected that these bacteria augment the louse’s diet with amino acids and facilitated the evolution of these diverse and specialized parasites. Heritable symbionts of insects often have small genomes that contain a minimal set of genes needed to maintain essential cell functions and synthesize metabolites absent in the host insect’s diet. Therefore, we expected the genome of a bacterial endosymbiont in feather lice would be small, but encode pathways for biosynthesis of amino acids. Results We sequenced the genome of a bacterial symbiont from a feather feeding louse ( Columbicola wolffhuegeli ) that parasitizes the Pied Imperial Pigeon ( Ducula bicolor ) and used its genome to predict metabolism of amino acids based on the presence or absence of genes. We found that this bacterial symbiont has a small genome, similar to the genomes of heritable symbionts described in other insect groups. However, we failed to identify many of the genes that we expected would support metabolism of amino acids in the symbiont genome. We also evaluated other gene pathways and features of the highly reduced genome of this symbiotic bacterium. Conclusions Based on the data collected in this study, it does not appear that this bacterial symbiont can synthesize amino acids needed to complement the diet of a feather feeding louse. Our results raise additional questions about the biology of feather chewing lice and the roles of symbiotic bacteria in evolution of diverse avian parasites. 
    more » « less
  5. ; ( , PeerJ)
    Since 2010, the trypanorhynch tapeworm family Rhinoptericolidae Carvajal & Campbell, 1975 has housed just two distinctive, monotypic genera ( Rhinoptericola Carvajal & Campbell, 1975 and Nataliella Palm, 2010). However, global collections of tapeworms from sharks and rays over the last more than three decades brought to light the need for major revision of the family by suggesting a much greater species-level diversity for the nominal genus Rhinoptericola . Through synonymy and the description of new species, the number of species in the genus is increased from one to eight. A phylogenetic analysis of the D1–D3 gene region of 28S rRNA (28S), including seven of the now nine species of rhinoptericolids, and a broad sampling of the other Trypanobatoida is the first to recover a monophyletic Rhinoptericolidae. In addition to systematic revision, this study allowed for the first evaluation of the degree of intraspecific vs interspecific variation in 28S for adult trypanorhynchs across the various hosts and geographic localities from which they have been reported, suggesting a relatively consistent boundary for Rhinoptericola . It is further suggested that detailed scanning electron microscopy (SEM) images of both the basal and metabasal armatures greatly aid in the interpretation of hook arrangement and shape. A schematic to streamline determination of the tentacular surface presented in scanning electron micrographs and line drawings of trypanorhynchs is presented for species with both two and four bothria. In combination, these methodological refinements can now be used as a model to resolve issues of classification and non-monophyly within both major lineages of the Trypanorhyncha. As a result of the taxonomic work, Rhinoptericola megacantha Carvajal & Campbell, 1975 (previously only known from the American cownose ray from the Chesapeake Bay and the Ticon cownose ray from the Gulf of Mexico, Venezuela, and Brazil) is now known from an additional species of cownose ray and a species of stingray, and is revealed to have a transatlantic distribution. Data from SEM suggest a simpler interpretation of hook arrangement in the metabasal armature for Rhinoptercola and—in combination with 28S sequence data—support Shirleyrhynchus Beveridge & Campbell, 1988 (a former rhinoptericolid) as its junior synonym. The three species formerly assigned to Shirleyrhynchus are thus transferred to Rhinoptericola . Data from light microscopy on whole-mounted specimens and histological sections, SEM, and 28S showed the eutetrarhynchid Prochristianella jensenae Schaeffner & Beveridge, 2012b to be morphologically consistent with species of Rhinoptericola and it is thus transferred to the genus. The type series of P. jensenae was determined to be mixed, representing two distinct species which are here redescribed and described as new, respectively. Two additional novel species of Rhinoptericola are described from cownose rays from off Mozambique and the Gulf of California. 
    more » « less
  • Citation Formats
  • MLA
  • APA
  • Chicago
  • BibTeX
  • Save / Share this Record
  • Send to Email