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Molecular and ultrastructural characterization of Dictyocoela diporeiae n. sp. (Microsporidia), a parasite of Diporeia spp. (Amphipoda, Gammaridea).

ABSTRACT: Dictyocoela diporeiae n. sp. is described from Diporeia spp. (Amphipoda, Gammaridea) collected from Lake Superior (USA), and its morphology and taxonomic affiliation are discussed. In hematoxylin- and eosin-stained sections of infected amphipods, the microsporidian was observed to infect muscle tissue surrounding the ovaries. Melanized hemocytic encapsulations were often observed in or near masses of microsporidians. The microsporidians appeared as spores measuring 1.99 ± 0.09 ?m long by 1.19 ± 0.05 ?m wide. Each spore contained eight coils of isofilar polar filaments that were arranged in single ranks. Polar filaments measured 71 ± 3 nm in diameter. A prominent lamellar polaroplast composed of ordered concentric membranes was found at the apical end of the spore surrounding the polar filament. A distinct posterior vacuole was observed at the distal end of the spore. Phylogenetic analysis based on 16s RNA sequences showed that the microsporidian belongs to the genus Dictyocoela, and is most similar to D. berillonum, yet distinctly different. The species is new, based on its morphology, genetic sequence, host, and location within the host.

SUBMITTER: Winters AD

PROVIDER: S-EPMC4059264 | biostudies-literature | 2014

REPOSITORIES: biostudies-literature

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Molecular and ultrastructural characterization of Dictyocoela diporeiae n. sp. (Microsporidia), a parasite of Diporeia spp. (Amphipoda, Gammaridea).

Winters Andrew David AD Faisal Mohamed M

Parasite (Paris, France) 20140617

Dictyocoela diporeiae n. sp. is described from Diporeia spp. (Amphipoda, Gammaridea) collected from Lake Superior (USA), and its morphology and taxonomic affiliation are discussed. In hematoxylin- and eosin-stained sections of infected amphipods, the microsporidian was observed to infect muscle tissue surrounding the ovaries. Melanized hemocytic encapsulations were often observed in or near masses of microsporidians. The microsporidians appeared as spores measuring 1.99 ± 0.09 μm long by 1.19 ± ...[more]

PMID: 24934702

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Project description:BackgroundThe phylum Haplosporidia contains coelozoic and histozoic, spore-forming, obligate protozoan endoparasites that infect a number of freshwater and marine invertebrates including bivalves, crustaceans, and polychaetes. In amphipods, haplosporidians cause systemic infection resulting in a range of pathologies. While amphipods belonging to the genus Diporeia (Gammarideae) have been shown to host haplosporidians, the taxonomic relationship of the Diporeia haplosporidian(s) is largely unknown due to the lack of phylogenetic and detailed ultrastructural studies.MethodsThe infection characteristics and taxonomic identity of a haplosporidian infecting Diporeia spp. (Diporeia) were based on microscopical investigation, electron microscopy, and Bayesian phylogenetic inference using haplosporidian 16S rRNA gene sequences.ResultsIn stained sections, the haplosporidian was observed to cause systemic infections in Diporeia that were often accompanied with host tissue degeneration. The haplosporidian appeared as binucleate plasmodia and sporocysts containing different spore maturation stages in the coelom, connective tissue, digestive tissue, and muscle. All of the observed systemic infections progressed to sporogenesis. Transmission electron microscopy revealed that fixed mature spores were slightly ellipsoidal and had a mean spore length X width of 5.34 ± 0.17 × 4.09 ± 0.15 μm. A hinged opercular lid with a length of 3.1 ± 0.17 μm was observed for a number of developing spores. The average thickness of the cell wall was 90.0 ± 8.33 nm. Thin filaments (70 nm) composed of spore wall material were observed projecting from an abopercular thickening of the spore wall. Phylogenetic analysis showed that the haplosporidian is novel bearing some similarities with the oyster pathogen Haplosporidium nelsoni, yet distinctly different.ConclusionsBased on its morphology, genetic sequence, and host, it became evident that the Diporeia haplosporidian is taxonomically novel and we propose its nomenclature as Haplosporidium diporeiae. This is the first report of a haplosporidian infecting Diporeia in Lake Superior.

Project description:The microsporidian genus Nosema is primarily known to infect insects of economic importance stimulating high research interest, while other hosts remain understudied. Nosema granulosis is one of the formally described Nosema species infecting amphipod crustaceans, being known to infect only two host species. Our first aim was to characterize Nosema spp. infections in different amphipod species from various European localities using the small subunit ribosomal DNA (SSU) marker. Second, we aimed to assess the phylogenetic diversity, host specificity and to explore the evolutionary history that may explain the diversity of gammarid-infecting Nosema lineages by performing a phylogenetic reconstruction based on RNA polymerase II subunit B1 (RPB1) gene sequences. For the host species Gammarus balcanicus, we also analyzed whether parasites were in excess in females to test for sex ratio distortion in relation with Nosema infection. We identified Nosema spp. in 316 individuals from nine amphipod species being widespread in Europe. The RPB1-based phylogenetic reconstruction using newly reported sequences and available data from other invertebrates identified 39 haplogroups being associated with amphipods. These haplogroups clustered into five clades (A-E) that did not form a single amphipod-infecting monophyletic group. Closely related sister clades C and D correspond to Nosema granulosis. Clades A, B and E might represent unknown Nosema species infecting amphipods. Host specificity seemed to be variable with some clades being restricted to single hosts, and some that could be found in several host species. We show that Nosema parasite richness in gammarid hosts is much higher than expected, illustrating the advantage of the use of RPB1 marker over SSU. Finally, we found no hint of sex ratio distortion in Nosema clade A infecting G. balcanicus. This study shows that Nosema spp. are abundant, widespread and diverse in European gammarids. Thus, Nosema is as diverse in aquatic as in terrestrial hosts.

Dataset Information

Molecular and ultrastructural characterization of Dictyocoela diporeiae n. sp. (Microsporidia), a parasite of Diporeia spp. (Amphipoda, Gammaridea).

Publications

Molecular and ultrastructural characterization of Dictyocoela diporeiae n. sp. (Microsporidia), a parasite of Diporeia spp. (Amphipoda, Gammaridea).

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