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

Parasite

and Mohamed Faisal¹  Andrew David Winters² 

[1] Department of Pathobiology and Diagnostic Investigation, Michigan State University, 1129 Farm Lane, 174 Food Safety and Toxicology Building,East Lansing,Michigan 48824,USA;Department of Fisheries and Wildlife, Michigan State University, 1129 Farm Lane, 177K Food Safety and Toxicology Building,East Lansing,Michigan 48824,USA

关键词: Small subunit ribosomal DNA;    Diporeia;    Microsporidia;    Dictyocoela diporeiae n. sp.;   

Others  :  808320
DOI  :  doi:10.1051/parasite/2014028

【 摘 要 】

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 ± 0.05 μm 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.

【 授权许可】

   
© A.D. Winters and M. Faisal , published by EDP Sciences, 2014

【 图 表 】

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【 参考文献 】

• [1]Alderman D, Polglase JL, Holdich D, Lowery R. 1988. Pathogens, parasites and commensals. Freshwater crayfish. Biology, management and exploitation, in Freshwater crayfish: biology, management and exploitation. Holdich DM, Lowery RS, Editors. Croom Helm (Chapman and Hall): London. p. 167–212.
• [2]Baker MD, Vossbrinck CR, Didier ES, Maddox JV, Shadduck JA. 1995. Small subunit ribosomal DNA phylogeny of various microsporidia with emphasis on AIDS related forms. Journal of Eukaryotic Microbiology, 42(5), 564–570.
• [3]Barbiero RP, Schmude K, Lesht BM, Riseng CM, Warren GJ, Tuchman ML. 2011. Trends in Diporeia populations across the Laurentian Great Lakes, 1997–2009. Journal of Great Lakes Research, 37(1), 9–17.
• [4]Bousfield E. 1989. Revised morphological relationships within the amphipod genera Pontoporeia and Gammaracanthus and the “glacial relict” significance of their postglacial distributions. Canadian Journal of Fisheries and Aquatic Sciences, 46(10), 1714–1725.
• [5]Darriba D, Taboada GL, Doallo R, Posada D. 2012. jModelTest 2: more models, new heuristics and parallel computing. Nature Methods, 9(8), 772.
• [6]Dermott R, Kerec D. 1997. Changes to the deepwater benthos of eastern Lake Erie since the invasion of Dreissena: 1979–1993. Canadian Journal of Fisheries and Aquatic Sciences, 54(4), 922–930.
• [7]Dunn A, Hatcher M, Terry R, Tofts C. 1995. Evolutionary ecology of vertically transmitted parasites: transovarial transmission of a microsporidian sex ratio distorter in Gammarus duebeni. Parasitology, 111(S1), S91–S109.
• [8]Dunn AM, Terry RS, Smith JE. 2001. Transovarial transmission in the microsporidia. Advances in Parasitology, 48, 57–100. [PubMed]
• [9]Edgerton BF, Evans LH, Stephens FJ, Overstreet RM. 2002. Synopsis of freshwater crayfish diseases and commensal organisms. Aquaculture, 206(1), 57–135.
• [10]Fielding N, et al. 2005. Ecological impacts of the microsporidian parasite Pleistophora mulleri on its freshwater amphipod host Gammarus duebeni celticus. Parasitology, 131(03), 331–336. [PubMed]
• [11]Fitzgerald SA, Gardner WS. 1993. An algal carbon budget for pelagic-benthic coupling in Lake Michigan. Limnology and Oceanography, 38(3), 547–560.
• [12]Hatcher MJ, Taneyhill DE, Dunn AM, Tofts C. 1999. Population dynamics under parasitic sex ratio distortion. Theoretical Population Biology, 56(1), 11–28. [PubMed]
• [13]Hogg J, Ironside J, Sharpe R, Hatcher M, Smith J, Dunn A. 2002. Infection of Gammarus duebeni populations by two vertically transmitted microsporidia; parasite detection and discrimination by PCR-RFLP. Parasitology, 125(01), 59–63. [PubMed]
• [14]Huelsenbeck JP, Ronquist F. 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics, 17(8), 754–755. [PubMed]
• [15]Kelly JF. 1979. Tissue specificities of Thelohania duorara, Agmasoma penaei, and Pleistophora sp., microsporidian parasites of pink shrimp, Penaeus duorarum. Journal of Invertebrate Pathology, 33(3), 331–339.
• [16]Krebes L, Blank M, Frankowski J, Bastrop R. 2010. Molecular characterisation of the Microsporidia of the amphipod Gammarus duebeni across its natural range revealed hidden diversity, wide-ranging prevalence and potential for co-evolution. Infection, Genetics and Evolution, 10(7), 1027–1038.
• [17]Langdon J. 1991. Microsporidiosis due to a pleistophorid in marron, Cherax tenuimanus (Smith), (Decapoda: Parastacidae). Journal of Fish Diseases, 14(1), 33–44.
• [18]Lozano SJ, Scharold JV, Nalepa TF. 2001. Recent declines in benthic macroinvertebrate densities in Lake Ontario. Canadian Journal of Fisheries and Aquatic Sciences, 58(3), 518–529.
• [19]Luna LG. 1968. Manual of histologic staining methods of the Armed Forces Institute of Pathology, vol. 121, McGraw-Hill: New York.
• [20]Nalepa TF, Faisal M. Submitted. Final Report: Mechanistic approach to identify the role of pathogens in causing Diporeia spp. decline in the Laurentian Great Lakes. Great Lakes Fisheries Trust Grant No. 3001637444.
• [21]Nalepa TF, Fanslow DL, Pothoven SA, Foley AJ III, Lang GA. 2007. Long-term trends in benthic macroinvertebrate populations in Lake Huron over the past four decades. Journal of Great Lakes Research, 33(2), 421–436.
• [22]Nalepa TF, Hartson DJ, Fanslow DL, Lang GA, Lozano SJ. 1998. Declines in benthic macroinvertebrate populations in southern Lake Michigan, 1980–1993. Canadian Journal of Fisheries and Aquatic Sciences, 55(11), 2402–2413.
• [23]Rodriguez F, Oliver J, Marin A, Medina JR. 1990. The general stochastic model of nucleotide substitution. Journal of Theoretical Biology, 142(4), 485–501. [PubMed]
• [24]Ryan JA, Kohler SL. 2010. Virulence is context-dependent in a vertically transmitted aquatic host-microparasite system. International Journal for Parasitology, 40(14), 1665–1673. [PubMed]
• [25]Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28(10), 2731–2739. [PubMed]
• [26]Terry RS, Smith JE, Sharpe RG, Rigaud T, Littlewood DTJ, Ironside JE, Rollinson D, Bouchon D, MacNeil C, Dick JTA, Dunn AM. 2004. Widespread vertical transmission and associated host sex-ratio distortion within the eukaryotic phylum Microspora. Proceedings of the Royal Society of London. Series B: Biological Sciences, 271(1550), 1783–1789.
• [27]Vossbrinck CR, Woese CR. 1986. Eukaryotic ribosomes that lack a 5.8S RNA. Nature, 320, 287–288. [PubMed]
• [28]Wilkinson TJ, Rock J, Whiteley NM, Ovcharenko MO, Ironside JE. 2011. Genetic diversity of the feminising microsporidian parasite Dictyocoela: New insights into host-specificity, sex and phylogeography. International Journal for Parasitology, 41(9), 959–966. [PubMed]
• [29]Wittner M, Weiss LM. 1999. The Microsporidia and Microsporidiosis. ASM Press: Washington.