Origin of Microsporidia and their systematical position among Eukaryotes

Mikologiya I Fitopatologiya

Volumn 43, Issue 3, 2009, Pages 177-192

  Sokolova, Yu Ya ^a  

^a NONE

Author keywords

Fungi; Microsporidia; Molecular phylogeny; Origin of microsporidia

Indexed keywords

CHYTRIDIOMYCOTA; EUKARYOTA; FUNGI; MICROSPORIDIA; PROTOZOA; ZYGOMYCETES; ZYGOMYCOTA;

EID: 70449854900     PISSN: 00263648     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (85)

1. Adl S. M., Simpson A. G.B., Farmer M. A., Andersen R. A., Anderson O. R., Bart a J. R., Browser S. S., Brugerolle G., Fensome R. A., Fredericq S., James T. Y., Karpov S., Kugrens P., Krug J., Lane C. E., Lewis L. A., Lodge J., Lynn D. H., Mann D. G., McCourt R. M., Mendoza L., Moestrup O., Mozley-Standridge S. E., Nerad T. A., Shearer C. A., Smirno v A. V., Spiegel F. W., Taylor M. The new higher level classification of eukaryotes with emphasis on the taxonomy of protists // J. Eukaryotic Microbiol. 2005. Vol.52. P. 399-451.
2. Amiri H., Karlberg O., Andersson S. G. E. Deep origin of plastid/parasite ATP/ADP translocases // J. Molec. Evolution. 2003. Vol.56. P. 137-150.
3. Arisue N., Hasegawa M., Hashimoto T. Root of the eukaryota tree as inferred from combined maximum likelihood analyses of multiple molecular sequence data // Molec. Biol, and Evolution. 2005. Vol.22. P. 409-420.
4. Arisue N., Sachez L. B., Weiss L. M., Mul1er M., Hashimo to T. Mitochondrial-type hsp70 genes of the amitochondriate protists, Giardia intestinalis, Entamoeba histolytica and two microsporidians // Parasitol. International. 2002. Vol.51. P. 9-16.
5. Becknel J. J., Andreadis T. G. Microsporidia in insects // The Microsporidia and Microsporidiosis / Eds M. Wittner, L. M. Weiss. Washington: American Society of Microbiology, 1999. P. 447-501.
6. Benjamin R. K. Zygomycetes and their spores // The whole fungus / Ed. B. Kendrick. Ottawa: National Museums of Canada, 1979. P. 573-621.
7. Beznoussenko G. V., Dolgikh V. V., Seliverstova E. V., Semenov P. B., Tokarev Y. S., Trueco A., Micaroni M., Di Giandomenico D., Auinger P., Senderski y I.V., Skarlato S.O., Snigirevskaya E. S., Komissarchik Y. Y., Pavelka M., DeMatteis M. A., Luini A., Sokolova Y. Y., Mironov A. A. Analogs of the Golgi complex in microsporidia: structure and avesicular mechanisms of function // J. Cell Sci. 2007. Vol.120. P. 1288-1298.
8. Biderre C., Metenier G., Vivares C. P. A small spliceosomal-type intron occurs in a ribosomal protein gene, of the microsporidian Encephalitozoon cuniculi // Molec. and Biochem. Parasitol. 1998. Vol.94. P. 283-286. (Pubitemid 28377293)
9. Brown J. R., Doolittle W. F. Root of the universal tree of life base on ancient aminoacyl-transfer-RNA synthetase gene duplications // Proc. of the National Academy of Sciences of the United States of America. 1995. Vol.92. P. 2441-2445.
10. Bruns T. Evolutionary biology -a kingdom revised // Nature. 2006. Vol.443. P. 758.
11. Burri L., Williams B. A. P., Bursac D., Lithgow T., Keeling P.J. Microsporidian mitosomes retain elements of the general mitochondrial targeting system // Proc. of the National Academy of Sciences of the United States of America. 2006. Vol.103. P. 15 916-15 920.
12. Canning E. U., Vavra J. Phyllum Microsporida Balbiani 1882 // An Illustrated Guide to the Protozoa / Eds J. J. Lee et al. Society of Protozoologists, Lawrence Kansas USA, 2000. P. 39-126.
13. Cavalier-Smith T. A 6-kindom classification and a united phylogeny // Endocytobiology II / Eds W. Schwemmler, H. Schenk. Berlin: Gruyter, 1983. P. 265-279.
14. Cavalier-Smith T. Cell evolution // Evolution of life / Eds S. Osawa, T. Honjo. Tokyo: Springer-Verlag, 1991. P. 271-304.
15. Cavalier-Smith T. Kingdom Protozoa and its 18 phyla // Microbiol. Rev. 1993. Vol.57. P. 953-994.
16. Cavalier-Smith T. Obcells as proto-organisms: Membrane heredity, lithophosphorylation, and the origins of the genetic code, the first cells, and photosynthesis // J. Molec. Evolution. 2001a. Vol.53. P. 555-595.
17. Cavalier-Smith T. What are fungi? // The Mycota / Eds D. J. McLaughlin et al. New York: Springer, 2001b. P. 3-37.
18. Cavalier-Smith T. Economy, speed and size matter: Evolutionary forces driving nuclear genome miniaturization and expansion // Ann. Bot. 2005. Vol.95. P. 147-175.
19. CorlissJ.O.Aninterimutilitarian(user-friendly) hierarchicalclassificationandcharacterizationoftheProtistsIActaProtozoologica. 1994.Vol.33.P.1-51.(Pubitemid2053148)
20. Corradi N.,Akiyoshi D. E., Morrison H.G., Feng X., Weiss L.M., Tzipori S., Keeling P. J. Patterns of genome evolution among the microsporidian parasites Encephalitozoon cuniculi, Antonospora locustae and Enterocytozoon bieneusi // PLoS ONE. 2007. Vol.2. P. 1277-1291.
21. Dacks J. B., Davis L. A. M., Sjogren A. M., Andersson J. O., Roger A. J., Doolittle W. F. Evidence for Golgi bodies in proposed 'Golgi-lacking' lineages // Proc. of the Royal Society of London Series B-Biological Sciences. 2003. Vol.270. P. S168-S171.
22. Dacks J. B., Doolittle W. F. Reconstructing/deconstructing the earliest eukaryotes: How comparative genomics can help t Cell. 2001. Vol.107. P. 419-425. (Pubitemid 33152778)
23. Edlind T.D., Li J., Visvesvara G. S., Vodkin M.H., McLaughlin G. L., Katiyar S. K. Phylogenese analysis of beta-tubulin sequences from amitochondrial protozoa / Molec. Phylogenet. and Evolution. 1996. Vol.5. P. 359-367.
24. Edman J. C., Kovacs J.A., Masur H., Santi D. V., Elwood H.J., Sogin M. L. Ribosomal RNA sequence shows Pneumocystis carini to be a member of the Fungi // Nature. 1988. Vol.334. P. 519-522. (Pubitemid 18190378)
25. Fast N. M., Doolittl e W. F. Trichomonas vaginalis possesses a gene encoding the essential spliceosomal component, PRP8 // Molec. and Biochem. Parasitol. 1999. Vol.99. P. 275-278.
26. Fast N.M., Law J. S.,Williams B. A., Keeling P. J. Bacterial catalase in the microsporidian Nosema locustae: implications for microsporidian metabolism and genome evolution // Eukaryot Cell. 2003. Vol.2. P. 1069-1075.
27. Fast N. M., Roger A. J., Richardson C. A., Doolittle W. F. U2 and U6 snRNA genes in the microsporidian Nosema locustae: evidence for a functional spliceosome // Nucl. Acids Res. 1998. Vol.26. P. 3202-3207.
28. Felsenstein J. Cases in which parsimony or compatibility methods will be positively misleading // Systematic Zoology. 1978. Vol.27. P.401-410.
29. Findley A. M., Weidner E. H., Carman K. R., Xu Z. M., Godbar J. S. Role of the posterior vacuole in Spraguea lophii (Microsporidia) spore hatching // Folia Parasitologica. 2005. Vol.52. P. 111-117.
30. Fischer W. M., Palmer J. D. Evidence from small-subunit ribosomal RNA sequences for a fungal origin of Microsporidia I Molec. Phylogenet. and Evolution. 2005. Vol.36. P. 606-622.
31. Flegel T. W., Pasharawipas T. A proposal for typical eukaryotic meiosis in microsporidians // Can. J. Microbiol. 1995. Vol.41. P. 1-11.
32. Fokin S. I., Di Giuseppe G., Erra F., Dini F. Euplotespora binucleatan. gen., n. sp (Protozoa : Microsporidia), a parasite infecting the hypotrichous ciliate Euplotes woodruffi, with observations on microsporidian infections in Ciliophora // J. Eukaryotic Microbiol. 2008. Vol.55. P. 214-228.
33. Germot A., Philippe H., LeGuyader H. Evidence for loss of mitochondria in Microsporidia from a mitochondrial-type HSP70 in Nosema locustae // Molec. and Biochem. Parasitol. 1997. Vol.87. P. 159-168.
34. Gill E. E., Fast N. M. Assessing the microsporidia-fungi relationships: combined phylogenetic analysis of eight genes // Gene. 2006. P. 103-109.
35. Hausmann S., Vivares C.P., Shuman S. Characterization of the mRNA capping apparatus of the microsporidian parasite Encephalitozoon cuniculi // J. Biol. Chem. 2002. Vol.277. P. 96-103.
36. Hawksworth D. L. The magnitude of fungal diversity: the 1.5 million species estimate revisited // Mycol. Res. 2001. Vol.105. P. 1422-1432.
37. Heckman D. S., Geiser D. M., Eidell B. R., Stauffer R. L., Kardos N. L., Hedges S.B. Molecular evidence for the early colonization of land by fungi and plants // Science. 2001. Vol.293. P. 1129-1133.
38. Hibbett D. S., Binder M., Bischoff J. F., Blackwell M., Cannon P. F., Eriksson O. E., Huhndorf S., James T., K irk P. M., Lucking R., Lumbsch H. T., Lutzoni F., Matheny P. B., McLaughlin D. J., Powell M. J., Redhead S., Schoch C. L., Spatafora J. W., Stalpers J. A., Vilgalys R., Aime M. C., Aptroot A., Bauer R., Begerow D., Benny G. L., Castlebury L. A., Crous P. W., Dai Y. C., Gams W., Geiser D.M., Griffith G. W., Gueidan C., Hawksworth D.L., Hestmark G., Hosaka K., Humber R. A., Hyde K.D., Ironside J. E., Koljalg U., Kurtzman C. P., Larsson K.H., Lichtwardt R., Longcore J., Miadlikowska J., Miller A., Moncalvo J.M., Mozley-Standridge S., Oberwinkler F., Parmasto E., Reeb V., Rogers J.D., Roux C., Ryvarden L., Sampaio J. P., Schussler A., Sugiyama J., Thorn R. G., Ti bell L., Untereiner W. A., Walker C., Wang Z., Weir A., Weiss M, White M. M., Winka K., Yao Y. J., Zhang N. A higher-level phylogenetic classification of the Fungi // Mycol. Res. 2007. Vol.111. P. 509-547.
39. HirtR.P.,HealyB.,VossbrinckC.R.,CanningE.U.,EmbleyT.M. AmitochondrialHsp70orthologueinVairimorphanecatrix: Molecularevidencethatmicrosporidiaoncecontainedmitochondria//CumBiology.1997. Vol.7.P.995-998.(Pubitemid28017078)
40. 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. of the National Academy of Sciences of the United States of America. 1999. Vol.96. P. 580-585. (Pubitemid 29061251)
41. In gold C.T. Mechanisms of liberation of spores and pollen // Hautarzt. 1972. Vol.23. P. 40-55.
42. James T. Y., Kauff F., Schoch C.L., Matheny P. B., Hofstetter V., Cox C. J., Celio G., Gueidan C., Fraker E., Miadlikowska J., Lumbsch H. T., Rauhut A., Reeb V., Arnold A. E., Amtoft A., Stajich J. E., Hosaka K., Sung G. H., Johnson D., O'Rourke B., Crockett M., Binder M., Curtis J.M., Slot J.C., Wang Z., Wilson A. W., Schussler A., Longcore J. E., O'Donnell K., Mozley-Standridge S., Porter D., Letcher P.M., Powell M. J., Taylor J. W., White M. M., Griffith G.W., Davies D. R., Humber R. A., Morton J. B., Sugiyama J., Rossman A. Y., Rogers J. D., Pfister D.H., Hewitt D., Hansen K., Hambleton S., Shoemaker R. A., Kohlmeyer J., Volkmann-Kohlmeyer B., Spotts R. A., Serdani M., Crous P. W., Hughes K. W., Matsuura K., Langer E., Langer G., Untereiner W. A., Lucking R., Budel B., Geiser D. M., Aptroot A., Diederich P., Schmitt I., Schultz M., Yahr R., Hibbett D.S., Lutzoni F., McLaughlin D. J., Spatafora J. W., Vilgalys R. Reconstructing the early evolution of Fungi using a six-gene phylogeny B Nature. 2006. Vol.443. P. 818-822.
43. KamaishiT.,HashimotoT.,NakamuraY.,MasudaY.,NakamuraF.,OkamotoK.,ShimizuM. ,HasegawaM. Completenucleotidesequencesofthegenesencodingtranslationelongationfactors1alph aand2fromamicrosporidianparasite,Glugeaplecoglossi: Implicationsforthedeepestbranchingofeukaryotes//J.Biochemistry.1996a.Vol.120.P. 1095-1103.(Pubitemid27029148)
44. Kamaishi T., Hashimoto T., Nakamura Y., Nakamura F., Murata S., Okada N., Okamoto K., Shimizu M., Hasegawa M. Protein phylogeny of translation elongation factor EF-I alpha suggests microsporidians are extremely ancient eukaryotes // J. Molec. Evolution. 19966. Vol.42. P. 257-263.
45. Katinka M.D., Duprat S., Cornillot E., Metenier G., Thomarat F., Prensier G., Barbe V., Peyretaillade E., Brottier P., Wincker P., Delbac F., El Alaoui H., Peyret P., Saurin W., Gouy M., Weissenbach J., Vivares C.P. Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi // Nature. 2001. Vol.414. P. 450-453.
46. Keeling P. J. Parasites go the full monty // Nature. 2001. Vol.414. P. 401-402.
47. Keeling P. J. Congruent evidence from alpha-tubulin and beta-tubulin gene phylogenies for a zygomycete origin of microsporidia Il Fungal Genetics and Biology. 2003. Vol.38. P. 298-309.
48. Keeling P. J., Doo1ittle W. F. Alpha-tubulin from early-diverging eukaryotic lineages and the evolution of the tubulin family // Molec. Biol, and Evolution. 1996. Vol.13. P. 1297-1305.
49. Keeling P. J., Fast N. M. Microsporidia: Biology and evolution of highly reduced intracellular parasites // Ann. Rev. Microbiol. 2002. Vol.56. P. 93-116.
50. Keeling P. J., Fast N. M., Law J. S., Williams B. A. P., Slamovits C. H. Comparative genomics of microsporidia // Folia Parasitologica. 2005. Vol.52. P. 8-14.
51. Keeling P. J., McFadden G. I. Origins of microsporidia // Trends in Microbiology. 1998. Vol.6. P. 19-23.
52. Keeling P. J., Slamovits C. H. Simplicity and complexity of microsporidian genomes // Eukaryotic Cell. 2004. Vol.3. P. 1363-1369.
53. Keohane E. M., Weiss L. M. The structure, function, and composition of the microsporidian polar tube // The Microsporidia and Microsporidiosis / Eds M. Wittner, L. M. Weiss. Washington: American Society of Microbiology, 1999. P. 196-224.
54. Koonin E.V., Fedorova N. D., Jackson J. D., Jacobs A. R., Krylov D. M., Makarova K. S., Mazumder R., Mekhedov S. L., Nikolskaya A. N., Rao B. S., Rogozin I. B., Smirnov S., Sorokin A.V., Sverdlov A. V., Vasudevan S., Wolf Y. I., Yin J. J., Natale D. A. A comprehensive evolutionary classification of proteins encoded in complete eukaryotic genomes // Genome Biology. 2004. Vol.5(2). P. R7.
55. Kudo R. A biological and taxonomie study of the microsporidia // Illinois Biol. Monograph. 1924. Vol.9. P. 1-268.
56. Kudo R. Protozoology 5th ed. / Ed. C.T. Charles. Spriengfield, Illinois, 1966. 568p.
57. Labbe A. Sporozoa // Friedlander u Sohn. Berlin, 1899. 218 S.
58. Larss on 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 Parasitologica. 2000. Vol.47. P. 241-256.
59. 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 // Europ. J. Protistology. 2006. Vol.42. P. 233-248. (Pubitemid 44739261)
60. Levine N. D., Corliss J. O., Cox F. E. G., Deroux G., Grain J., Honigberg B. M., Leedale G.F., Loeblich A. R., Lorn J., Lynn D., Merinfeld E. G., Page F. C., Poljansky G., Sprague V., Vavra J., Wallace F. G. A newly revised classification of the Protozoa // J. Protozoology. 1980. Vol.27. P. 37-58.
61. Liu Y. J., Hodson M. C., Hall B.D. Loss of the flagellum happened only once in the fungal lineage: phylogenetic structure of Kingdom Fungi inferred from RNA polymerase II subunit genes // BMC Evolut. Biol. 2006. Vol.6. P. 1-13.
62. Philippe H., Laurent J. How good are deep phylogenetic trees? // Curr. Opin. in Genet. Development. 1998. Vol.8. P. 616-623. (Pubitemid 28558522)
63. Philippe H., Lopez P., Brinkmann H., Budin K., Germot A., Laurent J., Moreira D., Muller M., Le Guyader H. Early-branching or fast-evolving eukaryotes? An answer based on slowly evolving positions // Proc. of the Royal Society of London Series B-Biological Sciences. 2000. Vol.267. P. 1213-1221.
64. Roger A. J. Reconstructing early events in eukaryotic evolution // Amer. Naturalist. 1999. Vol.154. P. S146-S163.
65. Schussler A. Molecular phylogeny, taxonomy, and evolution of Geosiphon pyriformis and arbuscular mycorrhizal fungi // Plant and Soil. 2002. Vol.244. P. 75-83.
66. Slamovit s C. H., Fast N. M., Law J. S., Keeling P. J. Genome compaction and stability in microsporidian intracellular parasites // Curr. Biol. 2004. Vol.14. P. 891-896.
67. Sokolova Y. Y., Mironov A. A. Structure and function of the Golgi organelle in parasitic protists // The Golgi Apparatus. State of art 110 years after Camillo Golgi's discovery / Eds A. Mironov, M. Pavelka. Wienn; New York: Springer, 2008. P. 647-675.
68. Sprague V. Classification and phylogeny of the Microsporidia // Comparative Pathobiology/ Eds J. L. A. Bulla, T. C. Cheng. New York; London: Plenum Press, 1977. P. 1-31.
69. Sprague V., Becnel J. J., Hazard E. I. Taxonomy of Phylum Microspora // Crit. Rev. in Microbiol. 1992. Vol.18. P. 285-395.
70. Tanabe Y., O'Donnell K., Saikawa M., Sugiyama J. Molecular phylogeny of parasitic Zygomycota (Dimargaritales, Zoopagales) based on nuclear small subunit ribosomal DNA sequences // Molec. Phylogenet. and Evolution. 2000. Vol.16. P. 253-262.
71. Tanabe Y., Saikawa M., Watanabe M. M., Sugiyama J. Molecular phylogeny of Zygomycota based on EF-I alpha and RPB1 sequences: limitations and utility of alternative markers to rDNA // Molec. Phylogenet. and Evolution. 2004. Vol.30. P. 438-449. (Pubitemid 38162045)
72. Tanabe Y., Watanabe M. M., Sugiyama J. Are Microsporidia really related to Fungi?: a reappraisal based on additional gene sequences from basal fungi // Mycol. Res. 2002. Vol.106. P. 1380-1391.
73. Van de Peer Y., Ben Ali A., Meyer A. Microsporidia: accumulating molecular evidence that a group of amitochondriate and suspectedly primitive eukaryotes are just curious fungi // Gene. 2000. Vol.246. P. 1-8.
74. Vavra J., Canning E. U., Barker R. J., Desportes I. Characters of microsporidia genera // Parasitology. 1981. Vol.82. P. 131-142.
75. Vavra J., Larsson R. Structure of Microsporidia I The Microsporidia and Microsporidiosis / Eds M. Wittner, L. M. Weiss. Washington: American Society of Microbiology, 1999. P. 55-77.
76. Vossbrinck C R., Maddox J. V., Friedman S., Debrunner-Vossbrinck B. A., Woese C. R. Ribosomal-RNA sequence suggests Microsporidia are extremely ancient eukaryotes // Nature. 1987. Vol.326. P.411-414.
77. VossbrinckC.R.,WoeseC.R.Eukaryoticribosomesthatlacka5.8sRNA//Nature.1986. Vol.320.P.287-288.(Pubitemid16040248)
78. Weidner E., Findley A. Peroxisomal catalase in extrusion apparatus posterior vacuole of microsporidian spores // Biol. Bull. 2002. Vol.203. P. 212.
79. Weidner E., Findley A. Catalase in microsporidian spores before and during discharge // Biol. Bull. 2003. Vol.205. P. 236-237.
80. Williams B. A. P., Hirt R. P., Lucocq J. M., Embley T. M. A mitochondrial remnant in the microsporidian Trachipleistophora hominis // Nature. 2002. Vol.418. P. 865-869. (Pubitemid 34966303)
81. Williams B. A. P., Keeling P. J. Microsporidian mitochondrial proteins: expression in Antonospora locustae spores and identification of genes coding for two further proteins / J. Eukaryotic Microbiol. 2005. Vol.52. P. 271-276.
82. Williams B. A. P., Slamovits C. H., Patron N. J., Fast N.M., Keeling P.J. A high frequency of overlapping gene expression in compacted eukaryotic genomes // Proc. of the National Academy of Sciences of the United States of America. 2005. Vol.102. P. 10 936-10 941.
83. Yuan X. L., Xiao S. H., Taylor T. N. Lichen-like symbiosis 600 million years ago // Science. 2005. Vol.308. P. 1017-1020. (Pubitemid 40664411)