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. 2005 Jan;43(1):192-8.
doi: 10.1128/JCM.43.1.192-198.2005.

The Pathogen of Frogs Amphibiocystidium Ranae Is a Member of the Order Dermocystida in the Class Mesomycetozoea

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The Pathogen of Frogs Amphibiocystidium Ranae Is a Member of the Order Dermocystida in the Class Mesomycetozoea

Cristiane N Pereira et al. J Clin Microbiol. .
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Abstract

The pathogen of frogs Amphibiocystidium ranae was recently described as a new genus. Due to its spherical shape, containing hundred of endospores, it was thought to be closely related to the pathogens of fish, mammals, and birds known as Dermocystidium spp., Rhinosporidium seeberi, and Sphaerothecum destruens in the Mesomycetozoea, but further studies were not conducted to confirm this relationship. To investigate its phylogenetic affinities, total genomic DNA was extracted from samples collected from infected frogs containing multiple cysts (sporangia) and endospores. The universal primers NS1 and NS8, used to amplify the 18S small-subunit rRNA by PCR, yielded approximately 1,770-bp amplicons. Sequencing and basic local alignment search tool analyses indicated that the 18S small-subunit rRNA of A. ranae from both Rana esculenta and Rana lessonae was closely related to all of the above organisms. Our phylogenetic analysis placed this pathogen of frogs as the sister group to the genus Dermocystidium and closely related to Rhinosporidium. These data strongly supported the placement of the genus Amphibiocystidium within the mesomycetozoeans, which is in agreement with the phenotypic features that A. ranae shares with the other members of this class. Interestingly, during this study Dermocystidium percae did not group within the Dermocystidium spp. from fish; rather, it was found to be the sister group to Sphaerothecum destruens. This finding suggests that D. percae could well be a member of the genus Sphaerothecum or perhaps represents a new genus.

Figures

FIG. 1.
FIG. 1.
Hematoxylin- and eosin-stained micrographs of the skin infected by Amphibiocystidium ranae in Rana esculenta (A) and Rana lessonae (B). The intradermal cysts were located subjacent to the epidermis, which is more hyperplasic in R. esculenta than in R. lessonae. The A. ranae endospores appear more developed in the skin sample of R. esculenta than in R. lessonae. A, ×15; B, ×10.
FIG. 2.
FIG. 2.
Detail of cysts and endospores of Amphibiocystidium ranae in infected Rana esculenta (A) and Rana lessonae (B). Inflammatory cells, such as eosinophils and neutrophils, are also observed near the cysts. Hematoxylin and eosin, ×40. Note that the endospores within the cysts of A. ranae in R. esculenta (A) appear more developed than in R. lessonae (B).
FIG. 3.
FIG. 3.
(A) Transmission electron micrograph of Amphibiocystidium ranae mature sporangium (cyst) containing endospores from an infected frog. The arrow points to the sporangium cell wall; B depicts multiple electron dense bodies; N, nucleus; W, capsule of the endospores. Bar, 2 μm. (B) Rhinosporidium seeberi from a Sri Lankan man with rhinosporidiosis. The arrow points to the mature sporangium cell wall. B, electron-dense bodies; W, endospore wall. Bar, 2 μm. Note the striking ultrastructural similarities between these two pathogenic mesomycetozoeans. The left lower insert in panel B shows a transmission electron micrograph of R. seeberi endospores with a prominent nucleus and a nucleolus (arrowhead). Bar, 2.5 μm.
FIG. 4.
FIG. 4.
Hematoxylin- and eosin-stained micrographs depicting the spherical phenotypic characteristic (arrows) of Amphibiocystidium ranae from an infected frog (A, ×20), Dermocystidium salmonis from an infected salmon (B, ×20), and Rhinosporidium seeberi from an infected human (C, ×10). The three panels illustrate the typical spherical phenotype with endospores in these pathogens. The morphological features of the endospores from each organism are depicted in the lower section of panels A, B, and C. Note the similarities between the endospores of A. ranae and D. salmonis, a feature that contrasts with those in R. seeberi (right lower corner, panels A and B, and left lower corner, panel C), ×40.
FIG. 5.
FIG. 5.
Phylogenetic relationship between the 18S small-subunit rRNA of 18 mesomycetozoeans, one coralochytrean, and two choanoflagellates previously studied by Mendoza et al. (25). Multiple hit correction and 1,000 bootstrap-resampled data sets were used to assess branch support. The genus Rhinosporidium (R. canis from a dog and R. seeberi from humans) and Dermocystidium spp. from fish are both in two different well-supported groups. In this tree, Amphibiocystidium ranae is the sister group to D. fennicum and D. salmonis. In turn, both sister groups are linked to R. seeberi. The numbers above the branches are percentages of bootstrap-resampled data sets as obtained by neighbor joining. Corallochytrium limacisporum, Acanthocoepsis unguilata, and Diaphanoeca grandis were used as the outgroup. The scale bar represents evolutionary distance in substitutions per nucleotide.

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