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

Volumn 10, Issue 7, 2010, Pages 1027-1038

  Krebes, L ^a   Blank, M ^a   Frankowski, J ^a   Bastrop, R ^a  

^a UNIVERSITY OF ROSTOCK   (Germany)

Author keywords

Co evolution; Gammarus duebeni; Microsporidia; Parasite prevalence; Parasitism; Phylogeny; Small subunit ribosomal gene

Indexed keywords

ARTICLE; COEVOLUTION; CONTROLLED STUDY; DICTYOCOELA DUEBENUM; DICTYOCOELA MUELLERI; DNA BASE COMPOSITION; DNA SEQUENCE; EUROPE; FRESHWATER SPECIES; GAMMARUS; GENE; HOST PARASITE INTERACTION; INTRASPECIFIC VARIATION; MARINE SPECIES; MICROSPORIDIA; NONHUMAN; NOSEMA GRANULOSIS; NUCLEOTIDE SEQUENCE; PARASITE PREVALENCE; PARASITISM; PHYLOGENETIC TREE; PLEISTOPHORA MULLERI; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SEQUENCE ANALYSIS; SMALL RIBOSOMAL SUBUNIT; SMALL SUBUNIT RIBOSOMAL GENE; UNINDEXED SEQUENCE;

AMPHIPODA; ANIMALS; DEMOGRAPHY; DNA, FUNGAL; EVOLUTION, MOLECULAR; GENETIC VARIATION; HOST-PARASITE INTERACTIONS; MICROSPORIDIA; PHYLOGENY;

AMPHIPODA; ANIMALIA; CRUSTACEA; DICTYOCOELA DUEBENUM; DICTYOCOELA MUELLERI; EUKARYOTA; GAMMARUS DUEBENI; MICROSPORIDIA; MICROSPORIDIUM; NOSEMA GRANULOSIS; PLEISTOPHORA MULLERI;

EID: 77956265460     PISSN: 15671348     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.meegid.2010.06.011     Document Type: Article

References (51)

1. Akaike H. A new look at the statistical model identification. IEEE Trans. Autom. Control 1974, 19:716-723.
2. Baker M.D., Vossbrinck C.R., Maddox J.V., Undeen A.H. Phylogenetic relationships among Vairimorpha and Nosema species (Microspora) based on ribosomal RNA sequence data. J. Invertebr. Pathol. 1994, 64:100-106.
3. Baker M.D., Vossbrinck C.R., Didier E.S., Maddox J.V., Shadduck J.A. Small subunit ribosomal DNA phylogeny of various microsporidia with emphasis on AIDS related forms. J. Eukaryot. Microbiol. 1995, 42:564-570.
4. Baker M.D., Vossbrinck C.R., Becnel J.J., Andreadis T.G. Phylogeny of Amblyospora (Microsporida: Amblyosporidae) and related genera based on small subunit ribosomal DNA data: a possible example of host parasite cospeciation. J. Invertebr. Pathol. 1998, 71:199-206.
5. Bulnheim H.P., Vávra J. Infection by the microsporidian Octosporea effeminans sp. n., and its sex determining influence in the amphipod Gammarus duebeni. J. Parasitol. 1968, 54:241-248.
6. Bulnheim H.P. Entwicklung, Übertragung und Parasit-Wirt-Beziehungen von Thelohania herediteria sp. n. (Protozoa, Microsporidia). Zeitschrift für Parasitenkunde 1971, 35:241-262.
7. Canning E.U., Nicholas J.P. Genus Pleistophora (Phylum Microspora): redescription of the type species, Pleistophora typicalis Gurley, 1893 and ultrastructural characterization of the genus. J. Fish Dis. 1980, 3:317-338.
8. Cheney S.A., Lafranchi-Tristem N.J., Canning E.U. Phylogenetic relationships of Pleistophora-like Microsporidia based on small subunit ribosomal DNA sequences and implications for the source of Trachipleistophora hominis infections. J. Eukaryot. Microbiol. 2000, 47:280-287.
9. Cheney S.A., Lafranchi-Tristem N.J., Bourges D., Canning E.U. Relationships of microsporidian genera, with emphasis on the polysporous genera, revealed by sequences of the largest subunit of RNA polymerase II (RPB1). J. Eukaryot. Microbiol. 2001, 48:111-117.
10. Combes C. Parasites, biodiversity and ecosystem stability. Biodivers. Conserv. 1996, 5:953-962.
11. Crawford G.I. The fauna of certain estuaries in West England and South Wales, with special reference to the Tanaidacea, Isopoda, and Amphipoda. J. Mar. Biol. Assoc. U. K. 1937, 21:647-662.
12. Dong S., Shen Z., Xu L., Zhu F. Sequence and phylogenetic analysis of SSU rRNA gene of five Microsporidia. Curr. Microbiol. 2009, 60:30-37.
13. Eden P.A., Schmidt T.M., Blakemore R.P., Pace N.R. Phylogenetic analysis of Aquaspirillum magnetotacticum using polymerase chain reaction-amplified 16S rRNA-specific DNA. Int. J. Syst. Bacteriol. 1991, 41:324-325.
14. Erickson B.W., Blanquet R.S. The occurrence of chitin in the spore wall of Glugea weissenbergi. J. Invertebr. Pathol. 1969, 14:358-364.
15. Gatehouse H.S., Malone L.A. The ribosomal RNA gene region of Nosema apis (Microspora): DNA sequence for small and large subunit rRNA genes and evidence of a large tandem repeat unit size. J. Invertebr. Pathol. 1998, 71:97-105.
16. Hall T.A. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl. Acids Symp. Ser. 1999, 41:95-98.
17. Hirt R.P., Logsdon J.M., Healy B., Dorey M.W., Doolittle W.F., Embley T.M. Microsporidia are related to Fungi: evidence from the largest subunit of RNA polymerase II and other proteins. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:580-585.
18. Hogg J.C., Ironside J.E., Sharpe R.G., Hatcher M.J., Smith J.E., Dunn A.M. Infection of Gammarus duebeni populations by two vertically transmitted microsporidia; parasite detection and discrimination by PCR-RFLP. Parasitology 2002, 125:59-63.
19. Hurst G.D.D., Jiggins F.M. Problems with mitochondrial DNA as a marker in population, phylogeographic and phylogenetic studies: the effects of inherited symbionts. Proc. R. Soc. B: Biol. Sci. 2005, 272:1525-1534.
20. Hynes H.B.N. The ecology of Gammarus duebeni Lilljeborg and its occurrence in fresh water in western Britain. J. Anim. Ecol. 1954, 23:38-84.
21. Hynes H.B.N. On the occurrence of Gammarus duebeni Lilljeborg in fresh water and of Asellus meridianus Racovitza in Western France. Hydrobiologia 1959, 12:152-155.
22. Ironside J.E., Dunn A.M., Rollinson D., Smith J.E. Association with host mitochondrial haplotypes suggests that feminizing microsporidia lack horizontal transmission. J. Evol. Biol. 2003, 16:1077-1083.
23. Ironside J.E., Wilkinson T.J., Rock J. Distribution and host range of the microsporidian Pleistophora mulleri. J. Eukaryot. Microbiol. 2008, 55:355-362.
24. Keeling P.J., Luker M.A., Palmer J.D. Evidence from beta-tubulin phylogeny that Microsporidia evolved from within the Fungi. Mol. Biol. Evol. 2000, 17:23-31.
25. Keeling P.J., Fast N.M. Microsporidia: biology and evolution of highly reduced intracellular parasites. Annu. Rev. Microbiol. 2002, 56:93-116.
26. Kelly A., Hatcher M.J., Dunn A.M. The impact of a vertically transmitted microsporidian, Nosema granulosis on the fitness of its Gammarus duebeni host under stressful environmental conditions. Parasitology 2003, 126:119-124.
27. Krebes L., Blank M., Jürss K., Zettler M.L., Bastrop R. Glacial-driven vicariance in the amphipod Gammarus duebeni. Mol. Phylogenet. Evol. 2010, 54:372-385.
28. Larsson J.I.R. Molecular versus morphological approach to microsporidian classification. Folia Parasitol. 2005, 52:143-144.
29. MacNeil C., Dick J.T., Hatcher M.J., Fielding N.J., Hume K.D., Dunn A.M. Parasite transmission and cannibalism in an amphipod (Crustacea). Int. J. Parasitol. 2003, 33:795-798.
30. Minchella D.J., Scott M.E. Parasitism: a cryptic determinant of animal community structure. Trends Ecol. Evol. 1991, 6:250-254.
31. Nylander J.A.A. MrModeltest v2. Program Distributed by the Author 2004, Evolutionary Biology Centre, Uppsala University.
32. O'Mahony E.M., Tay W.T., Paxton R.J. Multiple rRNA variants in a single spore of the Microsporidian Nosema bombi. J. Eukaryot. Microbiol. 2007, 54:103-109.
33. Pacaud A. Les Amphipodes de la faune nutritive des eaux douces francaises. Bull. Franc. Piscic. 1945, 136:105-120.
34. Refardt D., Canning E.U., Mathis A., Cheney S.A., Lafranchi-Tristem N.J., Ebert D. Small subunit ribosomal DNA phylogeny of microsporidia that infect Daphnia (Crustacea: Cladocera). Parasitology 2002, 124:381-389.
35. Reid D.M. On the occurrence of Gammarus duebeni (Lillj.) Crustacea, Amphipoda) in Ireland. Proc. R. Ir. Acad. B 1939, 45:207-214.
36. Rock J., Ironside J., Potter T., Whiteley N., Lunt D. Phylogeography and environmental diversification of a highly adaptable marine amphipod, Gammarus duebeni. Heredity 2007, 99:102-111.
37. Ronquist F., Huelsenbeck J.P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19:1572-1574.
38. Smith J.E. The ecology and evolution of microsporidian parasites. Parasitology 2009, 136:1901-1914.
39. Solter L.F., Maddox J.V. Physiological host specificity of microsporidia as an indicator of ecological host specificity. J. Invertebr. Pathol. 1998, 71:207-216.
40. Swofford D.L. PAUP Phylogenetic Analysis Using Parsimony (and Other Methods), Version 4 2003, Sinauer Associates, Sunderland, MA.
41. 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.
42. Terry R.S., Smith J.E., Dunn A.,M. Impact of a novel, feminising microsporidium on its crustacean host. J. Eukaryot. Microbiol. 1998, 45:497-501.
43. Terry R.S., Smith J.E., Bouchon D., Rigaud T., Duncanson P., Sharpe R.G., Dunn A.M. Ultrastructural characterisation and molecular taxonomic identification of Nosema granulosis n. sp., a transovarially transmitted feminising (TTF) microsporidium. J. Eukaryot. Microbiol. 1999, 46:492-499.
44. Terry R.S., MacNeil C., Dick J.T.A., Smith J.E., Dunn A.M. 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.
45. Terry R.S., Smith J.E., Sharpe R.G., Rigaud T., Littlewood D.T.J., Ironside J.E., Rollinson D., Bouchon D., MacNeil C., Dick J.T.A., Dunn A.M. 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.
46. Vossbrinck C.R., Andreadis T.G., Vavra J., Becnel J.J. Molecular phylogeny and evolution of mosquito parasitic Microsporidia (Microsporidia: Amblyosporidae). J. Eukaryot. Microbiol. 2004, 51:88-95.
47. Vossbrinck C.R., Debrunner-Vossbrinck B.A. Molecular phylogeny of the Microsporidia: ecological, ultrastructural and taxonomic considerations. Folia Parasitol. 2005, 52:131-142.
48. Wittner M. Historic perspective on the Microsporidia: expanding horizons. The Microsporidia and Microsporidiosis 1999, 1-6. ASM Press, Washington, DC. M. Wittner, L.M. Weiss (Eds.).
49. Wolinska J., Giessler S., Koerner H. Molecular identification and hidden diversity of novel Daphnia parasites from European lakes. Appl. Environ. Microbiol. 2009, 75:7051-7059.
50. Zhang Z., Schwartz S., Wagner L., Miller W. A greedy algorithm for aligning DNA sequences. J. Comput. Biol. 2000, 7:203-214.
51. Zhu X., Wittner M., Tanowitz H.B., Kotler D., Cali A., Weiss L.M. Small subunit rRNA sequence of Enterocytozoon bieneusi and its potential diagnostic role with use of the polymerase chain reaction. J. Infect. Dis. 1993, 168:1570-1575.