Microsporidia: Diverse, dynamic, and emergent pathogens in aquatic systems

Trends in Parasitology

Volumn 29, Issue 11, 2013, Pages 567-578

  Stentiford, Grant D ^a   Feist, Stephen W ^a   Stone, David M ^a   Bateman, Kelly S ^a   Dunn, Alison M ^b  

^a CENTRE FOR ENVIRONMENT   (United Kingdom)

^b UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

Disease; Freshwater; Marine; Microsporidia; Pathogenesis; Taxonomy

Indexed keywords

SMALL SUBUNIT RIBOSOMAL RNA;

ABELSPORA; AGGLOMERATA; AGMASOMA; ALFVENIA; AMAZONSPORA; AMBYLOSPORA; AMESON; AMPHIACANTHA; AMPHIAMBLYS; AQUATIC SPECIES; ARTHROPOD; BACILLIDIUM; BACULEA; BERWALDIA; BINUCLEATA; BINUCLEOSPORA; BRYONOSEMA; CELL NUCLEUS; CILIATOSPORIDIUM; COUGOURDELLA; CUCUMISPORA; CYTOPLASM; DASYATISPORA; DESOMOZOON; DICTYOCOELA; ENCEPHALITOZOON; ENTEROCYTOZOON; ENTEROSPORA; EUPLOTESPORA; FACILISPORA; FIBRILLANOSEMA; FLABELLIFORMA; GLUGEA; GLUGOIDES; GURLEYA; GURLEYIDES; HAMILTOSPORIDIUM; HEPATOSPORA; HETEROSPORIS; HOLOBISPORA; HOST CELL; HOST PATHOGEN INTERACTION; HRABYEIA; ICHTHYOSPORIDIUM; INODOSPORUS; KABATANA; KINORHYNCHOSPORA; LANATOSPORA; LARSSONIA; LOMA; MARSSONIELLA; METCHNIKOVELLA; MICROBIAL DIVERSITY; MICROFILIUM; MICROGEMMA; MICROSPORIDIA; MORPHOLOGICAL TRAIT; MRAZEKIA; MYOSPORA; MYOSPORIDIUM; NADELSPORA; NAPAMICHUM; NELLIEMELBA; NEONOSEMOIDES; NONHUMAN; NORLEVINEA; NOSEMA; NOSEMOIDES; NUCLEOSPORA; NUCLEOTIDE SEQUENCE; OCTOSPOREA; ORDOSPORA; ORMIERESIA; OVIPLEISTOPHORA; PARANUCLEOSPORA; PARASITISM; PARATHELOHANIA; PEREZIA; PHYLOGENY; PLASTICITY; PLEISTOPHORA; POTASPORA; PSEUDOLOMA; PSEUDONOSEMA; PYROTHECA; RECTISPORA; REVIEW; SCHOEDERA; SPORANAUTA; SPRAGUEA; STEINHAUSIA; TAXONOMIC IDENTIFICATION; TETRAMICRA; THELOHANIA; TRICHONOSEMA; TRICHOTUZETIA; TRIWANGIA; TUZETIA; UNIKARYON; UNINDEXED SEQUENCE; VAIRIMORPHA; VAVRAIA; WITTMANNIA;

EUKARYOTA; INVERTEBRATA; MAMMALIA; MICROSPORIDIA; PROTISTA; VERTEBRATA;

DISEASE; FRESHWATER; MARINE; MICROSPORIDIA; PATHOGENESIS; TAXONOMY;

ANIMALS; AQUATIC ORGANISMS; BIODIVERSITY; BIOLOGICAL EVOLUTION; FISHES; HOST-PATHOGEN INTERACTIONS; INVERTEBRATES; MICROSPORIDIA;

EID: 84887022054     PISSN: 14714922     EISSN: 14715007     Source Type: Journal    
DOI: 10.1016/j.pt.2013.08.005     Document Type: Review

References (107)

1. Nägeli C. Über die neue krankheit der seidenraupe und verwandte org anismen. Bot. Zeitung. 1857, 15:760-761.
2. Pasteur L. Études sur la Maladie des Vers à Soie 1870, Gauthier-Villars, (reprinted in 1926 by Masson).
3. Gluge G. Notice sur quelques points d'anatomie pathologique comparée, suivie de quelques observations sur la structure des branchies dans épinoches. Bull. Acad. R. Belg. 1838, 5:771-785.
4. Henneguy F., Thélohan P. Myxosporidies parasites des muscles chez quelques crustacés décapodes. Ann. Microgr. 1892, 4:617-641.
5. Pérez C. Microsporidies parasites des crabes d'Arcachon. Note préliminaire. Soc. Sci. Arcachon 1905, 1905:8.
6. Franzen C. Microsporidia: a review of 150 years of research. Open Parasitol. J. 2008, 2:1-34.
7. Weiser J. Klic kurcovani Mikrosporidii. Acta Soc. Sci. Nat. Moravicae 1947, 18:1-64.
8. Weiser J. Contribution to the classification of microsporidia. Vestn. Cesk. Spol. Zool. 1977, 41:308-320.
9. Vávra J., Sprague V. Glossary for the microsporidia. Comparative Pathobiology 1976, Vol. 1:341-364. Plenum Press.
10. Issi I.V. Microsporidia as a phylum of parasitic protozoa. Protozoology 1986, 10:6-136.
11. Canning E.U., Lom J. The Microsporidia of Vertebrates 1986, Academic Press.
12. Sprague V., Becnel J.J. Appendix: checklist of available generic names for microsporidia with type species and type host. The Microsporidia and Microsporidiosis 1999, 517-530. ASM Press. M. Wittner, L.M. Weiss (Eds.).
13. Canning E.U., Vávra J. Phylum Microsporidia Balbiani 1882. An Illustrated Guide to the Protozoa 2000, vol. 1:39-126. Wiley-Blackwell. 2nd edn.
14. Vávra J., Lukeš J. Microsporidia and "the art of living together". Adv. Parasitol. 2013, 82:254-319.
15. Capella-Gutierrez S., et al. Phylogenomics supports microsporidia as the earliest diverging clade of sequenced fungi. BMC Biol. 2012, 10:47.
16. Weiss L. The first united workshop on Microsporidia from invertebrate and vertebrate hosts. Folia Parasitol. 2005, 52:1-7.
17. Redhead S.A., et al. Proposals to exclude the phylum Microsporidia from the Code. Taxon 2009, 58:658-672.
18. Vossbrinck C.R., Debrunner-Vossbrinck B.A. Molecular phylogeny of the Microsporidia: ecological, ultrastructural and taxonomic considerations. Folia Parasitol. 2005, 52:131-142.
19. Stentiford G.D., et al. Plastic parasites: extreme dimorphism creates a taxonomic conundrum in the phylum Microsporidia. Int. J. Parasitol. 2013, 43:339-352.
20. Jones S.R.M., et al. The diversity of Microsporidia in parasitic copepods (Caligidae: Siphonostomatoida) in the Northeast Pacific Ocean with description of Facilispora margolisi n. g., n. sp and a new family Facilisporidae n. fam. J. Eukaryot. Microbiol. 2012, 59:206-217.
21. Stentiford G.D., et al. Myospora metanephrops (n. g., 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.
22. Larsson J.I.R. Description of a new microsporidium of the water mite Limnochares aquatica and establishment of the new genus Napamichum (Microspora, Thelohaniidae). J. Invertebr. Pathol. 1990, 55:152-161.
23. Sagrista E., et al. Developmental cycle and ultrastructure of Steinhausia mytilovum, a microsporidian parasite of oocytes of the mussel, Mytilus galloprovincialis (Mollusca, Bivalvia). Eur. J. Protistol. 1998, 34:58-68.
24. Lohrmann K.B., et al. Microsporidiosis in queen scallops (Aequipecten opercularis L.) from UK waters. J. Shellfish Res. 2000, 19:71-75.
25. Clausen C. Light and ultrastructural observations on a microsporidium in the hydrozoan (Cnidaria). Sarsia 2000, 85:177-180.
26. Ardila-Garcia A.M., Fast N.M. Novel microsporidian species infects the free-living nematode Odontophora rectangular. J. Phycol. 2011, 47:S23.
27. Gorbunov A.K., Kosova A.A. Parasites in Rotifers from the Volga delta. Hydrobiologia 2001, 446:51-55.
28. Oumouna M., et al. Electron microscopic study of a new microsporean Microsporidium epithelialis sp. n. infecting Tubifex sp. (Oligochaeta). Folia Parasitol. 2000, 47:257-265.
29. Adrianov A.V., Rybakov A.V. Kinorhynchospora japonica gen. n, sp. n. (Microsporidia) from the intestine epithelium of Kinorhynchus yushini (Homalorhagida, Pychophyidae) from the Sea of Japan. Zool. Zh. 1991, 70:5-11.
30. Deburon I., et al. Infection and pathological alterations within the acanthocephalan Acanthocephaloides propinquus attributable to the microsporidian hyperparasite Microsporidium acanthocephali. Trans. Am. Microsc. Soc. 1990, 109:91-97.
31. Canning E.U., et al. Ultrastructure of Tuzetia weidneri sp. n. (Microsporidia: Tuzetiidae) in skeletal muscle of Litopenaeus setiferus and Farfantepenaeus aztecus (Crustacea: Decapoda) and new data on Perezia nelsoni (Microsporidia: Pereziidae) in L. setiferus. Acta Protozool. 2002, 41:63-77.
32. Morris D.J., Adams A. Development of Schroedera plumatellae gen. n., sp. n. (Microsporidia) in Plumatella fungosa (Bryozoa: Phylactolaemata). Acta Protozool. 2003, 41:383-396.
33. Desser S.S., et al. Trichonosema algonquinensis n. sp. (Phylum Microsporidia) in Pectinatella magnifica (Bryozoa: Phylactolaemata) from Algonquin Park, Ontario, Canada. J. Eukaryot. Microbiol. 2004, 51:389-393.
34. Lom J., Dykova I. Hrabyeia xerkophora n. gen, n. sp., a new microsporidian from the oligochaete Nais Christinae Kaspazak, 1973. Eur. J. Protistol. 1990, 25:243-248.
35. Larsson J.I.R. The ultrastructural cytology of Bacillidium strictum (Leger and Hesse, 1916) Jirovec, 1936 (Microspora, Bacillidiidae). Eur. J. Protistol. 1992, 28:175-183.
36. Sene A., et al. Ultrastructure of Unikaryon nomimoscolexi n. sp. (Microsporida, Unikaryonidae), a parasite of Nomimoscolex sp. (Cestoda, Proteocephalidea) from the gut of Clarotes laticeps (Pisces, Teleoste, Bagridae). Dis. Aquat. Organ. 1997, 29:35-40.
37. Ba C.T., et al. Ultrastructure of Nosema sp., microsporidia hyperparasite of Bothriocephalus clavipes (cestoda, bothriocephalidae) parasite of intestine of Anguilla anguilla (Pisces, Teleostei) from Corse, France. J. Eukaryot. Microbiol. 2007, 54:24S.
38. Levron C., et al. Ultrastructural description of the life cycle of Nosema diphterostomi sp. n., a microsporidia hyperparasite of Diphterostomum brusinae (Digenea: Zoogonidae), intestinal parasite of Diplodus annularis (Pisces: Teleostei). Acta Protozool. 2004, 43:329-336.
39. Levron C., et al. Ultrastructural description of the life cycle of Nosema monorchis n. sp. (Microspora, Nosematidae), hyperparasite of Monorchis parvus (Digenea, Monorchiidae), intestinal parasite of Diplodus annularis (Pisces, Teleostei). Eur. J. Protistol. 2005, 41:251-256.
40. Cable J., Tinsley R.C. Microsporidian hyperparasites and bacteria associated with Pseudodiplorchis americanus (Monogenea, Polystomatidae). Can. J. Zool. 1992, 70:523-529.
41. Czaker R. Wittmannia antarctica n. g., n. sp. (Nosematidae), a new hyperparasite in the Antarctic dicyemid mesozoan Kantharella antarctica. J. Eukaryot. Microbiol. 1997, 44:438-446.
42. Larsson J.I.R. The hyperparasitic microsporidium Amphiacantha longa Caullery et Mesnil, 1914 (Microspora: Metchnikovellidae) - description of the cytology, redescription of the species, emended diagnosis of the genus Amphiacantha and establishment of the new family Amphiacanthidae. Folia Parasitol. 2000, 47:241-256.
43. McDermott J.J. Nemerteans as hosts for symbionts: a review. J. Nat. Hist. 2006, 40:1007-1020.
44. Larsson J.I.R., Koie M. The ultrastructure and reproduction of Amphiamblys capitellides (Microspora, Metchnikovellidae), a parasite of the gregarine Ancora sagittata (Apicomplexa, Lecudinidae), with redescription of the species and comments on the taxonomy. Eur. J. Protistol. 2006, 42:233-248.
45. Scheid P. Mechanism of intrusion of a microspordian-like organism into the nucleus of host amoebae (Vannella sp.) isolated from a keratitis patient. Parasitol. Res. 2007, 101:1097-1102.
46. Fokin S.I., et al. Euplotespora binucleata n. gen., n. sp. (Protozoa: Microsporidia), a parasite infecting the hypotrichous ciliate Euplotes woodruffi, with observations on microsporidian infections in ciliophora. J. Eukaryot. Microbiol. 2008, 55:214-228.
47. Foissner I., Foissner W. Ciliatosporidium platyophryae nov. gen., nov. spec. (Microspora, Encephalitozoonidae), a parasite of Platyophrya terricola (Ciliophora, Colpodea). Eur. J. Protistol. 1995, 31:248-259.
48. Nylund S., et al. Diseases of farmed Atlantic salmon Salmo salar associated with infections by the microsporidian Paranucleospora theridion. Dis. Aquat. Organ. 2011, 94:41-57.
49. Sokolova Y.Y., et al. Fine structure of Metchnikovella incurvata Caullery and Mesnil 1914 (microsporidia), a hyperparasite of gregarines Polyrhabdina sp. from the polychaete Pygospio elegans. Parasitology 2013, 140:855-867.
50. Stentiford G.D., et al. Hepatospora eriocheir (Wang and Chen, 2007) gen. et comb. nov infecting invasive Chinese mitten crabs (Eriocheir sinensis) in Europe. J. Invertebr. Pathol. 2011, 108:156-166.
51. Sprague V. Annotated list of species of microsporidia. Comparative Pathobiology 1977, Vol. 2:31-334. Plenum Press.
52. 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 major revision of the genus Thelohania Henneguy, 1892. J. Eukaryot. Microbiol. 2006, 53:445-455.
53. Freeman M.A., et al. A hyperparasitic microsporidian infecting the salmon louse, Lepeophtheirus salmonis: an rDNA-based molecular phylogenetic study. J. Fish Dis. 2003, 26:667-676.
54. Tsaousis A.D., et al. A novel route for ATP acquisition by the remnant mitochondria of Encephalitozoon cuniculi. Nature 2008, 453:553-556.
55. Galbreath J.G.M.S., et al. Invasion success of Fibrillanosema crangonycis, n. sp., n. g.: a novel vertically transmitted microsporidian parasite from the invasive amphipod host Crangonyx pseudogracilis. Int. J. Parasitol. 2004, 34:235-244.
56. Lom J., Dykova I. Microsporidian xenomas in fish seen in wider perspective. Folia Parasitol. 2005, 52:69-81.
57. Mrázek A. Sporozoenstudien II. Glugea lophii Doflein. Sitzungsber. Böhm. Ges. Wiss. Math.-Naturwiss 1899, 34:1-8.
58. Chatton E., Courrier R. Formation d'un complexe xénoparasitaire géant avec bordure en brosse, sous l'influence d'une Microsporidie, dans le testicule de Cottus bubalis. C. R. Soc. Biol. (Paris) 1923, 89:579-583.
59. Debaisieux P. Études cytologiques du Mrazekia argoisi. Cellule 1931, 40:147-168.
60. Matthews R.A., Matthews B.F. Cell and tissue reactions of turbot Scopthalmus maximus (L.) to Tetramicra brevifilum gen. n., sp. n. (Microspora). J. Fish Dis. 1980, 3:495-515.
61. Sanchez J.G., et al. Localization of the initial developmental stages of Loma salmonae in rainbow trout (Oncorhynchus mykiss). Vet. Pathol. 2001, 38:540-546.
62. Stentiford G.D., Neil D.M. Diseases of Nephrops and Metanephrops: a review. J. Invertebr. Pathol. 2011, 106:92-109.
63. Tourtip S., et al. Enterocytozoon hepatopenaei sp. nov. (Microsporida: Enterocytozoonidae), a parasite of the black tiger shrimp Penaeus monodon (Decapoda: Penaeidae): fine structure and phylogenetic relationships. J. Invertebr. Pathol. 2009, 102:21-29.
64. Zbinden M., et al. Experimental evolution of field populations of Daphnia magna in response to parasite treatment. J. Evol. Biol. 2008, 21:1068-1078.
65. Agnew P., et al. Host life history responses to parasitism. Microbes Infect. 2000, 2:891-896.
66. Dunn A.M., et al. Transovarial transmission in the microsporidia. Adv. Parasitol. 2001, 48:57-100.
67. Smith J.E. The ecology and evolution of microsporidian parasites. Parasitology 2009, 136:1901-1914.
68. Terry R.S., et al. Widespread vertical transmission and associated host sex-ratio distortion within the eukaryotic phylum Microspora. Proc. R. Soc. Lond. B: Biol. Sci. 2004, 271:1783-1789.
69. Lucarotti C.J., Andreadis T.G. Reproductive strategies and adaptations for survival among obligatory microsporidian and fungal parasites of mosquitos - a comparative analysis of Ambylospora and Coelomomyces. J. Am. Mosq. Control Assoc. 1995, 11:111-121.
70. Ebert D., Herre E.A. The evolution of parasitic disease. Parasitol. Today 1996, 12:96-101.
71. Bandi C., et al. Inherited microorganisms, sex-specific virulence and reproductive parasitism. Trends Parasitol. 2001, 17:88-94.
72. Dunn A.M., Smith J.E. Microsporidian life cycles and diversity: the relationship between virulence and transmission. Microbes Infect. 2001, 3:381-388.
73. Koella J.C., et al. Coevolutionary interactions between host life histories and parasite life cycles. Parasitology 1998, 116:S47-S55.
74. Engelstaedter J., Hurst G.D.D. The ecology and evolution of microbes that manipulate host reproduction. Annu. Rev. Ecol. Evol. Syst. 2009, 40:127-149.
75. Cordaux R., et al. The impact of endosymbionts on the evolution of host sex-determination mechanisms. Trends Genet. 2011, 27:332-341.
76. Hurst L.D. The incidences and evolution of cytoplasmic male killers. Proc. R. Soc. Lond. B: Biol. Sci. 1991, 244:91-99.
77. Kellen W.R., et al. Host-parasite relationships of some Thelohania from mosquitos (Nosematidae: Microsporidia). J. Invertebr. Pathol. 1965, 7:161-166.
78. Hatcher M.J., Dunn A.M. Evolutionary consequences of cytoplasmically inherited feminizing factors. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 1995, 348:445-456.
79. Hatcher M.J., et al. Local adaptation and enhanced virulence of Nosema granulosis artificially introduced into novel populations of its crustacean host, Gammarus duebeni. Int. J. Parasitol. 2005, 35:265-274.
80. Rodgers-Gray T.P., et al. Mechanisms of parasite-induced sex reversal in Gammarus duebeni. Int. J. Parasitol. 2004, 34:747-753.
81. Jahnke M., et al. Effects of feminizing microsporidia on the masculinizing function of the androgenic gland in Gammarus duebeni. J. Invertebr. Pathol. 2013, 112:146-151.
82. Kohler S.L., Hoiland W.K. Population regulation in an aquatic insect: the role of disease. Ecology 2001, 82:2294-2305.
83. Hatcher M.J., Dunn A.M. Parasites in Ecological Communities; From Interactions to Ecosystems 2011, Cambridge University Press.
84. Hatcher M.J., et al. Diverse effects of parasites in ecosystems: linking interdependent processes. Front. Ecol. Environ. 2012, 10:186-194.
85. Trait-mediated Indirect Interactions 2012, Cambridge University Press. T. Ohgushi (Ed.).
86. Kohler S.L., Wiley M.J. Pathogen outbreaks reveal large-scale effects of competition in stream communities. Ecology 1997, 78:2164-2176.
87. Kohler S.L. The ecology of host-parasite interactions in aquatic insects. Aquatic Insects: Challenges to Populations 2008, 55-80. CAB International. J. Lancaster (Ed.).
88. Werner E.E., Peacor S.D. A review of trait-mediated indirect interactions in ecological communities. Ecology 2003, 84:1083-1100.
89. Dunn A.M., et al. Indirect effects of parasites in invasions. Funct. Ecol. 2012, 26:1262-1274.
90. Terry R.S., et al. Resolution of a taxonomic conundrum: an ultrastructural and molecular description of the life cycle of Pleistophora mulleri (Pfeiffer 1895; Georgevitch 1929). J. Eukaryot. Microbiol. 2003, 50:266-273.
91. Fielding N.J., et al. Ecological impacts of the microsporidian parasite Pleistophora mulleri on its freshwater amphipod host Gammarus duebeni celticus. Parasitology 2005, 131:331-336.
92. MacNeil C., et al. Parasite transmission and cannibalism in an amphipod (Crustacea). Int. J. Parasitol. 2003, 33:795-798.
93. MacNeil C., et al. Parasite altered micro-distribution of Gammarus pulex (Crustacea: Amphipoda). Int. J. Parasitol. 2003, 33:57-64.
94. Haddaway N.R., et al. Predatory functional response and prey choice identify predation differences between native/invasive and parasitised/unparasitised crayfish. PLoS ONE 2012, 7:e32229.
95. Simberloff D., et al. Impacts of biological invasions: what's what and the way forward. Trends Ecol. Evol. 2013, 28:58-66.
96. Bojko J., et al. Baseline histopathological survey of a recently invading island population of killer shrimp, Dikerogammarus villosus. Dis. Aquat. Organ. 2013, 10.3354/dao02658.
97. Cleaveland S., et al. Overviews of pathogen emergence: which pathogens emerge, when and why?. Curr. Top. Microbiol. Immunol. 2013, 315:85-111.
98. Lafferty K.D., et al. Are diseases increasing in the ocean?. Annu. Rev. Ecol. Evol. Syst. 2004, 35:31-54.
99. Peeler E.J., et al. Non-native aquatic animals introductions have driven disease emergence in Europe. Biol. Invasions 2011, 13:1291-1303.
100. Okamura B., Feist S.W. Emerging diseases in freshwater systems. Freshwater Biol. 2011, 56:627-637.
101. Wu J.Y., et al. Honey bees (Apis mellifera) reared in brood combs containing high levels of pesticide residues exhibit increased susceptibility to Nosema (Microsporidia) infection. J. Invertebr. Pathol. 2012, 109:326-329.
102. Didier E.S., Weiss L.M. Microsporidiosis: not just in AIDS patients. Curr. Opin. Infect. Dis. 2011, 24:490-495.
103. Didier E.S. Microsporidiosis: an emerging and opportunistic infection in humans and animals. Acta Trop. 2005, 94:61-76.
104. Zhi-Qiang Z. Phylum Arthropoda von Siebold, 1848. Animal biodiversity: an outline of higher-level classification and survey of taxonomic richness. Zootaxa 2011, 4138:99-103.
105. Martin, J.W. and Davis, G.E. (2001) An Updated Classification of the Recent Crustacea (Science Series, No. 39), pp. 132, Natural History Museum of Los Angeles County.
106. James T.Y., et al. Shared signatures of parasitism and phylogenomics unite the Cryptomycota with the Microsporidia. Curr. Biol. 2013, 23:1548-1553.
107. Keeling P. Five questions about Microsporidia. PLoS Pathog. 2009, 5:e1000489.