Plastic parasites: Extreme dimorphism creates a taxonomic conundrum in the phylum Microsporidia

International Journal for Parasitology

Volumn 43, Issue 5, 2013, Pages 339-352

  Stentiford, G D ^a   Bateman, K S ^a   Feist, S W ^a   Chambers, E ^a   Stone, D M ^a  

^a CENTRE FOR ENVIRONMENT   (United Kingdom)

Author keywords

Ameson; Carcinus maenas; Crustacea; Myospora; Myosporidae; Nadelspora; Taxonomy

Indexed keywords

SINGLE STRANDED RNA;

CLONE; CRAB; CYTOPLASM; DIMORPHISM; FUNGUS; HISTOLOGY; MORPHOLOGY; MUSCLE; PARASITE; PATHOGENICITY; PATHOLOGY; PHYLOGENETICS; PHYLOGENY; RNA; TAXONOMY; ULTRASTRUCTURE;

AMESON MICHAELIS; AMESON PULIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALLINECTES SAPIDUS; CARCINUS MAENAS; CELL LINEAGE; CELL ULTRASTRUCTURE; CLADISTICS; CONTROLLED STUDY; CRAB; CYTOPLASM; GENE AMPLIFICATION; GENE SEQUENCE; GENE TRANSFER; GENETIC IDENTIFICATION; GENETIC VARIABILITY; HEART MUSCLE; HISTOPATHOLOGY; METACARCINUS MAGISTER; MICROSPORIDIAN SPORE; MOLECULAR CLONING; MOLECULAR PHYLOGENY; MUSCLE CELL; MYOSITIS; NADELSPORA CANCERI; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITE; PHENOTYPIC PLASTICITY; PHYLUM; SARCOPLASM; SEQUENCE ANALYSIS; SEX DIFFERENCE; SKELETAL MUSCLE; TAXONOMY;

ANIMALS; BRACHYURA; DNA; MICROSPORIDIA; MOLECULAR SEQUENCE DATA; PHYLOGENY; POLYMERASE CHAIN REACTION;

AMESON; AMESON MICHAELIS; CALLINECTES SAPIDUS; CANCER MAGISTER; CARCINUS MAENAS; CRUSTACEA; DECAPODA (CRUSTACEA); MICROSPORIDIA; MICROSPORIDIUM; NADELSPORA; NADELSPORA CANCERI;

EID: 84875258575     PISSN: 00207519     EISSN: 18790135     Source Type: Journal    
DOI: 10.1016/j.ijpara.2012.11.010     Document Type: Article

References (42)

1. Baker M.D., Vossbrinck C.R., Becnel J.J., Andreadis T.G. Phylogeny of Ambylospora (Microsporida, Ambylosporidae) and related genera based on small ribosomal DNA data: a possible example of host parasite cospeciation. J. Invertbr. Pathol. 1998, 71:199-206.
2. Baker M.D., Vossbrinck C.R., Becnel J.J., Maddox J.V. Phylogenetic position of Ambylospora Hazard and Oldacre (Microspora, Ambylosporidae) based on small subunit rRNA data and its implications for the evolution of the Microsporidia. J. Eukary. Microbiol. 1997, 44:220-225.
3. Becnel J.J., Andreadis T.G. Microsporidia in insects. The Microsporidia and Microsporidiosis 1999, 447-501. American Society of Microbiology Press, Washington, DC. M. Witter, L.M. Weiss (Eds.).
4. Brown A.M.V., Adamson M.L. Phylogenetic distance of Thelohania butleri Johnston, Vernick, and Sprague, 1978 (Microsporidia; Thelohaniidae), a parasite of the smooth pink shrimp Pandalus jordani, from its congeners suggests need for a major revision of the Genus Thelohania Henneguy, 1892. J. Eukaryot. Microbiol. 2006, 53:445-455.
5. Canning E.U., Vavra J. Phylum microsporida. The Illustrated Guide to the Protozoa 2000, 39-126. Society for Protozoologists, Allen Press, USA. second ed. J.L. Lee, G.F. Leedale, P. Bradbury (Eds.).
6. Choi J., Park J., Kim D., Jung K., Kang S., Lee Y.-H. Fungal secretome database: integrated platform for annotation of fungal secretomes. BMC Genomics 2010, 11:105.
7. Docker M.F., Devlin R.H., Richard J., Khattra J., Kent M.L. Sensitive and specific polymerase chain reactionassay for detection of Loma salmonae (Microsporea). Dis. Aquat. Org. 1997, 29:41-48.
8. Edling T.D., Li J., Visvesvara G.S., Vodkin M.H., McLaughlin G.L., Katiyar S.K. Phylogenetic analysis of beta-tubulin sequences from amitochondrial protozoa. Mol. Phylogenet. Evol. 1996, 5:359-367.
9. Freeman M.A., Sommerville C. Desmozoon lepeophtherii n. gen., n. sp., (Microsporidia: Enterocytozoonidae) infecting the salmon louse Lepeophtheirus salmonis (Copepoda: Caligidae). Parasites Vectors 2009, 2:58.
10. Hazard E.I., Fukuda T. Stempellia milleri sp. n. (Microsporida: Nosematidae) from the mosquito Culex pipiens quinquefasciatus: Its morphological and behavioral characteristics as compared to other described Stempellia diseases. J. Protozool. 1974, 21:497-504.
11. Hopwood D. Theory and practice of histopathological techniques. Fixation and Fixatives 1996, 23-46. Churchill Livingstone, Hong Kong. fourth ed. J.D. Bamcroft, A. Stevens (Eds.).
12. James T.Y., et al. Reconstructing the early evolution of Fungi using a six-gene phylogeny. Nature 2006, 443:818-822.
13. Keeling P.J., Doolittle W.F. Alpha-tubulin from early-diverging eukaryotic lineages and the evolution of the tubulin family. Mol. Biol. Evol. 1996, 13:1297-1305.
14. Kelling W.R., Lipa J.J. Thelohania californica n. sp., a microsporidian parasite of Culex tarsalis Coquillett. J. Insect Pathol. 1960, 2:1-12.
15. Kiryu Y., Behringer D.C., Landsberg J.H., Petty B.D. Microsporidiosis in the Caribean spiny lobster Panulirus argus from Southeastern Florida, USA. Dis. Aquat. Org. 2009, 84:237-242.
16. Kramer J.P. Nosema necatrix sp. n and Thelohania diazoma sp. n., microsporidians from the armyworm Pseudaletia unipuncta (Haworth). J. Invertebr. Pathol. 1965, 7:117-121.
17. Kudo R. On the structure of some microsporidian spores. J. Parasitol. 1920, 6:178-182.
18. Loubès C., Maurand J., Comps M., Campillo A. Observations ultrastructurales sur Ameson nelson (Sprague, 1950) microsporidia parasite de la crevette Parapenaeus longirostris Lucas consequences taxonomiques. Rev. Trav. De l'Inst. Pêch. Marit. 1977, 41:217-222.
19. Nylund S., Nylund A., Watanabe K., Arnesen C.E., Karlsbank E. Paranucleospora theridion n. gen., n. sp. (Microsporidia, Enterocytozoonidae) with a Life Cycle in the Salmon Louse (Lepeophtheirus salmonis, Copepoda) and Atlantic Salmon (Salmo salar). J. Eukaryot. Microbiol. 2010, 57:95-114.
20. Olson R.E., Tiekotter K.L., Reno P.W. Nadelspora canceri N. G., N. Sp., an unusual microsporidian parasite of the Dungeness crab, Cancer magister. J. Eukaryot. Microbiol. 1994, 41:349-359.
21. Owens L., Glazebrook J.S. Microsporidiosis in prawns from Northern Australia. Aust. J. Mar. Freshwater Res. 1988, 39:301-305.
22. Perez C. Sur une novella glugeidee parasite du Carcinus maenas. C.R. Soc. Biol. 1905, 58:146-148.
23. Perez C. Microsporidies parasites des crabs d'Archachon. Soc. Sci. Arcachon. Trav. 1905, 8:15-36.
24. Reynolds E.S. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 1963, 17:208-212.
25. Ryazanova T.V., Eliseikina M.G. Microsporidia of the genera Thelohania (Thelohaniidae) and Ameson (Pereziidae) in two species of lithodid crabs from the Sea of Okhotsk. Russ. J. Mar. Biol. 2010, 36:435-442.
26. Stentiford G.D., Bateman K.S., Dubuffett A., Stone D. Hepatospora eriocheir (Wang & Chen, 2007) gen. et comb. nov. from European Chinese mitten crabs (Eriocheir sinensis). J. Invertebr. Pathol. 2011, 108:156-166.
27. Stentiford G.D., Bateman K.S., Feist S.W. Enterospora canceri n.gen., n.sp., an intranuclear microsporidian infecting European edible crab (Cancer pagurus). Dis. Aquat. Org. 2007, 75:61-72.
28. Stentiford G.D., Bateman K.S., Small H.J., Moss J., Shields J.D., Reece K.S., Tuck I. Myospora metanephrops (n. gn., n. sp.) from marine lobsters and a proposal for erection of a new Order and Family (Crustaceacida; Myosporidae) in the Class Marinosporidia (Phylum Microsporidia). Int. J. Parasitol. 2010, 40:1433-1446.
29. Sumpton W.D. Infection of sand crabs (Portunus pelagicus) by the microsporidian Ameson sp. in Moreton Bay. Proc. R. Soc. Qd. 1994, 104:85-87.
30. Tamura K., Dudley J., Nei M., Kumar S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 2007, 24:1596-1599.
31. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., Higgins D.G. The CLUSTAL_X windows interface. flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 1997, 25:4876-4882.
32. Tourtip S., Wongtripop S., Sritunyalucksana K., Stentiford G.D., Bateman K.S., Sriurairatana S., Chayaburakul K., Chavadej K., Withyachumnarnkul B. Enterocytozoon hepatopenaei sp. nov. (Microspora: Enterocytozoonidae), a parasite of the black tiger shrimp Penaeus monodon (Decapoda: Penaeidae): fine structure and phylogenetic relationships. J. Invertebr. Pathol. 2009, 102:21-29.
33. van Ooij C., Tamez P., Bhattacharjee S., Hiller N.L., Harrison T., Liolios K., Kooij T., Ramesar J., Balu B., Adams J., Waters A., Janse C., Haldar K. The Malaria secretome: from algorithms to essential function in blood stage infection. PLoS Pathog. 2008, 4(6):e1000084.
34. Vávra J., Barker R.J., Vivarès C.P. A scanning electron microscope study of a microsporidian with a pansporoblast: Thelohania maenadis. J. Invert. Pathol. 1981, 37:47-53.
35. Vivarès C.P. Etude ultrastructurale de Thelohania maenadis (Microspora, Microsporida) et données nouvelles sur le genre Thelohania Henneguy. Archiv Für Protisten 1980, 37:47-53.
36. Vivarès C.P., Sprague V. The fine sructure of Ameson pulvis (Microspora, Microsporida) and its implications regarding classification and chromosome cycle. J. Invert. Pathol. 1979, 33:40-52.
37. Vivarès C.P., Azevedo C. Ultrastructural observations of the life cycle stages of Ameson atlanticum sp., nov., a microsporidian parasitizing Cancer pagurus L. J. Fish Dis. 1988, 11:379-387.
38. Vossbrinck C.R., Andreadis T.G., Vávra J., Becnel J.J. Molecular phylogeny and evolution of mosquito parasitic Microsporidia (Microsporidia, Ambylosporidae). J. Eukaryot. Microbiol. 2004, 51:88-95.
39. Vossbrinck C.R., Debrunner-Vossbrinck B.A. Molecular phylogeny of the Microsporidia: ecological, ultrastructural and taxonomic considerations. Folia Parasitol. 2005, 52:131-142.
40. Weidner E. Ultrastructural study of microsporidian development. I. Nosema sp. Sprague, 1965 in Callinectes sapidus Rathbun. Z. Zellforsch. 1970, 105:33-54.
41. Weissenberg R. Microsporidian interactions with host cells. Comparative Pathobiology. Biology of the Microsporidia 1976, vol. 1:203-237. Plenum, New York.
42. Zhu X., Wittner M., Tanowitz H.B., Cali A., Weiss L.M. Nucleotide sequence of the small subunit rRNA of Ameson michaelis. Nucleic Acids Res. 1993, 21(16):3895.