The taxonomy and phylogenetics of the human and animal pathogen Rhinosporidium seeberi: A critical review

Revista Iberoamericana de Micologia

Volumn 29, Issue 4, 2012, Pages 185-199

  Vilela, Raquel ^a,c,d   Mendoza, Leonel ^a,b  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b Federal University of Minas Gerais ^*  (United States)

^c FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^d Institute Superior of Medicine (ISMD)   (Brazil)

Author keywords

Mesomycetozoa; Phylogenetics; Plastids; Rhinosporidiosis; Rhinosporidium seeberi

Indexed keywords

CELL CYCLE; CELL MATURATION; CELL ULTRASTRUCTURE; DNA DETERMINATION; FUNGAL STRAIN; FUNGUS ISOLATION; LIFE CYCLE; MOLECULAR PHYLOGENY; MORPHOLOGICAL TRAIT; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITE IDENTIFICATION; PHYLOGENETIC TREE; PLASTID GENOME; POLYMERASE CHAIN REACTION; RHINOSPORIDIUM; SEQUENCE ANALYSIS; SHORT SURVEY;

ANIMALS; HUMANS; LIFE CYCLE STAGES; RHINOSPORIDIUM;

ANIMALIA; CHOANOZOA; COLLETOTRICHUM; CYANOBACTERIA; EUKARYOTA; FUNGI; MICROCYSTIS; PROKARYOTA; RHINOSPORIDIUM SEEBERI; SYNCHYTRIUM;

EID: 84867329941     PISSN: 11301406     EISSN: 21739188     Source Type: Journal    
DOI: 10.1016/j.riam.2012.03.012     Document Type: Short Survey

References (110)

1. Aben-Athar J. Um caso de Rhinosporidiose. Rev Acad Med Belém, Pará Br 1944, 2:3-7.
2. Acevedo P de. Rhinosporidium seeberi: Considerações sôbre morfologia, ciclo parasitário e posição sistemática. Thesis. Belém, Pará, Brasil: Facultade de Medicina, Universidade do Pará; 1958. p. 1-108.
3. Adl S.M., Simpson A.G., Farmer M.A., Andersen R.A., Anderson O.R., Barta J.R., et al. The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J Eukaryot Microbiol 2005, 52:399-451.
4. Alhuwalia K.B. Sequence analysis of 16S rDNA gene in Rhinosporidium seeberi shows similarity to plant chloroplast DNA. Bioinformation 2010, 5:89-96.
5. Alhuwalia K.B. Causative agent of rhinosporidiosis. Author's reply. J Clin Microbiol 2001, 39:413-415.
6. Alhuwalia K.B. Culture of the organism that causes rhinosporidiosis. J Laryngol Otol 1999, 113:523-528.
7. Alhuwalia K.B. Plant molecule in human disease, a novel association. Gene regulation and molecular aspects of muscle, liver, pancreas, connective tissue and plants 1992, vol. 5:289-292. Peeters Press, Lauven, Belgium.
8. Alhuwalia K.B. New interpretations in rhinosporidiosis, enigmatic disease of the last nine decades. J Submicrosc Cytol Pathol 1992, 24:109-114.
9. Alhuwalia K.B., Maheshwari N., Deka R.C. Rhinosporidiosis: a study that resolves etiologic controversies. Am J Rhinol 1997, 11:479-483.
10. Alhuwalia K.B., Sharma N., Kacher S.K., Deka R.C. Association of tapioca and chronic inflammation with rhinosporidiosis. Indian J Otolaryngol Head Neck Surg 1994, 3:25-27.
11. Allen F.R.W.K., Dave M. Treatment of rhinosporidiomycosis in man based on sixty cases. Ind Med Gaz 1936, 71:376-395.
12. Apple D.J. Papillome der conjunktiva bedingt durch rhinosporidiose. Fortschr Ophthalmol 1983, 79:571-574.
13. Arseculeratne S.N. Rhinosporidiosis: what is the cause. Curr Opin Infect Dis 2005, 18:113-118.
14. Arseculeratne S.N., Mendoza L. Rhinosporidiosis. Topley and Wilson's microbiology and microbial infections 2005, 436-475. ASM Press, Hodder Arnold. 10th edition. W.G. Merz, R. Hay (Eds.).
15. Arseculeratne S.N., Hussein F.N., Atapattu D.N., Pathmanathan R. Failure to infect congenitally immunodeficient SCID and NUDE mice with Rhinosporidium seeberi. Med Mycol 2000, 38:393-395.
16. Ashworth J.H. On Rhinosporidium seeberi (Wernicke, 1903) with special reference to its sporulation and affinities. Trans Roy Soc Edin 1923, 53:301-342.
17. Azadeh B., Baghoumian N., El-Bakri O.T. Rhinosporidiosis: immunohistochemical and electron microscopic studies. J Laryngol Otol 1994, 108:1048-1054.
18. Bader G., Grueber H.L.E. Histochemical studies on Rhinosporidium seeberi. Virchows Arch Abt A Pathol Anat 1970, 350:76-86.
19. Battie J.M. Rhinosporidium kinealyi: a sporozoon of the nasal mucous membrane. J Pathol Bacteriol 1906, 11:270-275.
20. Belou P. Tratado de Parasitología Animal: Ilustrado con 301 figuras intercaladas en el texto y 16 láminas en cromo-litografía 1903, vol. 303:62. Arsenio Guidi Buffarini (ed.), Buenos Aires, Argentina.
21. Brunberg A.K., Bostrom B. Coupling between benthic biomass of Microcystis and phosphorus release from the sediments of a highly eutrophic lake. Hydrobiologia 1992, 235:375-385.
22. Carini A. Sôbre um parasito smelhante ao Rhinosporidium encontrado em quisto da pele de uma Hyla. Arq Inst Biol 1940, 11:93-96.
23. Cavalier-Smith T. Neomonada and the origin of animal and fungi. Evolutionary Relationships Among Protozoa 1998, vol. 56:375-407. Kluwer, Dordrecht, The Netherlands.
24. Ceferri R., Redaelli P., Scatizzi I. Unitá etiologica della malattia di Seeber (Granuloma de Rhinosporidium seeberi) accertata com lo studio di materiali originali. Boll Soc Med Chir di Pavia 1936, 14:723-745.
25. Cole S.T., Eiglmeier K., Parkhill J., James K.D., Thomson N.R., Wheeler P.R., et al. Massive gene decay in the leprosy bacillus. Nature 2001, 409:1007-1011.
26. Cordero E.H., Vogelsang E.G. El probable modo de infección de las mucosas por Rhinosporidium. Bol Inst Clin Quir 1928, 28:573-574.
27. Datta S. Rhinosporidium seeberi, its cultivation and identity. J Vet Sci Anim Husban 1965, 35:1-17.
28. Delwiche C.F. Tracing the tread of plastid diversity through the tapestry of life. Am Nat 1999, 154:S165-S177.
29. Delwiche C.F., Kuhsel M., Palmer J.D. Phylogenetic analysis of tufA sequences indicates a cyanobacterial origin of all plastids. Mol Phylogenet Evol 1995, 4:110-128.
30. Dhaulakhandi D.B., Alhuwalia K.B., Ravi A.K., Garg L.C. Detection of 16S rDNA gene in round bodies isolated from polyps of rhinosporidiosis. Infect Gen Evol 2006, 6:331-336.
31. Dhaulakhandi D.B., Alhuwalia K.B., Poduval P., Ravi A.K. Comparative RAPD analysis of causative agent of rhinosporidiosis and Microcystis isolated from waters. Curr Sci 2004, 86:386-388.
32. Dodge C.W. Rhinosporidium. Fungous diseases of men and other mammals 1935, The C.V. Mosby Company, St. Louis, p. 151-152.
33. Douglas S.E. Plastid evolution: origins, diversity, trends. Curr Opin Genet Dev 1998, 8:655-661.
34. Fonseca O.J.M., Lacaz C.daS. Estudo de culturas isoladas de blastomicose queloidiforme (doença de Jorge Lobo). Denominação ao seu agente etiològico. Rev Inst Med Trop São Paulo 1971, 13:225-251.
35. Fredricks D.N., Jolley J.A., Lepp P.W., Kosek J.C., Relman D.A. Rhinosporidium seeberi: a human pathogen from a novel group of aquatic protistan parasites. Emer Infect Dis 2000, 6:273-282.
36. Gabrielsen T.M., Minge M.A., Espelund M., Tooming-Klunderud A., Patil V., Nederbragt A.J., et al. Genome evolution of a tertiary dinoflagellate plastid. PLoS One 2011, 6:1-8.
37. Gori S., Scasso A. Cytologic and differential diagnosis of rhinosporidiosis. Acta Cytol 1994, 38:361-366.
38. Grover S. Cytological study of Rhinosporidium seeberi by electron microscopy. Indian J Pathol Bacteriol 1974, 17:29-32.
39. Grover S. Rhinosporidium seeberi: a preliminary study of the morphology and life cycle. Sabouraudia 1970, 7:219-231.
40. Herr R.A., Mendoza L., Arseculeratne S.N., Ajello L. Immunolocalization of an endogenous antigenic material of Rhinosporidium seeberi expressed only during mature sporangial development. FEMS Immunol Med Microbiol 2002, 23:2015-2212.
41. Herr A.R., Ajello L., Mendoza L. Chitin synthase class 2 (CHS2) gene from the human and animal pathogen Rhinosporidium seeberi. Proc. 99th Gen. Meet. Am. Soc. Microbiol. 1999, 296. [Abstr.].
42. Herr R.A., Tarcha E.J., Taborda P.R., Taylor J.W., Ajello L., Mendoza L. Phylogenetic analysis of Rhinosporidium seeberi's 18S small-sub unit ribosomal DNA groups this pathogen among members of the protistan Mesomycetozoa clade. J Clin Microbiol 1999, 37:2750-2754.
43. Janse I., Meima M., Kardinaal E.A., Zwart G. High-resolution differentiation of cyanobacteria by using rRNA-internal transcriber spacer denaturing gradient gel electrophoresis. Appl Environ Microbiol 2003, 69:6634-6643.
44. Jones D.D., Jost M. Isolation and chemical characterization of gas vacuole membranes from Microcystis aeruginosa Kütz. emend. Elenkin Arch Mikrobiol 1970, 70:43-64.
45. Kannan-Kutty M., Teh E.C. Rhinosporidium seeberi: an ultrastructural study of its endosporulation phase and trophocyte phase. Arch Pathol 1975, 99:51-54.
46. Kannan-Kutty M., Teh E.C. Rhinosporidium seeberi: an ultrastructural study of its life cycle. Pathology 1974, 6:63-70.
47. Kannan-Kutty M., Teh E.C. Rhinosporidium seeberi: cell wall formation in sporoplasts. Pathology 1974, 6:183-185.
48. Kannan-Kutty M., Gomez J.B. The ultrastructure and life history of Rhinosporidium seeberi. S E Asian J Trop Med Publ Health 1971, 2:9-16.
49. Karling J.S. Chytridiomycetarum iconographia. An illustrated and brief descriptive guide to the Chytridiomycetes genera with a supplement of the Hyphochytridiomycetes 1977, J. Cramer, New York, p. 43-59.
50. Karling J.S. Resting spore germination in Synchytrium australe in relation to its classification. Mycologia 1955, 47:185-192.
51. Karling J.S. Prosori in Synchytrium. Bull Torrey Bot Club 1955, 82:218-236.
52. Karling J.S. Micromyces and Synchytrium. Mycologia 1953, 45:276-287.
53. Karpova M.F. On the morphology of rhinosporidiosis. Mycopathologia 1964, 23:281-286.
54. Kennedy F.A., Buggage R.R., Ajello L. Rhinosporidiosis: a description of an unprecedented outbreak of captive swans (Cygnus spp.) and a proposal for revision of the ontogenic nomenclature of Rhinosporidium seeberi. J Med Vet Mycol 1995, 33:157-165.
55. Köhler S., Delwiche C.F., Denny P.W., Tilney L.G., Webster P., Wilson R.J., et al. A plastid of probable green algal origin in apicomplexan parasites. Science 1997, 275:1485-1489.
56. Komárek J., Komárková J. Review of the European Microcystis-morphospecies (Cyanoprokaryotes) from nature. Czech Phycol 2002, 2:1-24.
57. Komárek J., Anagnostidis K. Cyanoprokaryota, 1. Teil: Chroococcales. Süsswasserflora von Mitteleuropa, Band 19/1 1999, 1-548. Gustav Fischer Verlag, Jena. H. Ettl, G. Gärtner, H. Heynig, D. Mollenhauer (Eds.).
58. Krishnamoorthy S., Sreedharan V.P., Koshy P., Kumar S., Anilakumari C.K., Krishnamoorty S., et al. Culture of Rhinosporidium seeberi: preliminary report. J Layngol Otol 1989, 103:178-180.
59. Kurunaratne W.A.E. Rhinosporidiosis in man 1964, University of London, London, Toronto, New York, p. 1-146, The Athlone Press.
60. Kurunaratne W.A. The pathology of rhinosporidiosis. J Pathol 1936, 1:193-202.
61. Lacaz CdaS. Doença de Jorge Lôbo (Lobo's Disease). Rev Iberoamer Micol 1996, 13:819-826.
62. Lang N.J. The fine structure of the blue-green algae. Annu Rev Microbiol 1968, 22:15-46.
63. Laveran A., Petit A. Sur une épizootic des truites. C R Acad Sci Paris 1910, 151:421-423.
64. Lengfelder D.D., Pospischil A. Rhinosporidiosse beim pferd. Histopathologische und elecktronenmikroskopische untersuchung eines falles. Zentralbl Veterinaermed [B] 1980, 27:326-339.
65. Levy M.G., Meuten D.J., Breitschwerdt E.B. Cultivation of Rhinosporidium seeberi in vitro: interaction with epithelial cells. Science 1986, 234:474-476.
66. Matsuo E. Leprosy as a challenge to science on the ability to decode its enigma. A hypothesis on how to respond. Jpn J Infect Dis 2005, 58:59-64.
67. Melo MTde. Estudos sôbre o Rhinosporidium seeberi. Thesis. Rio de Janeiro, Brasil: Estudos Gráficos, Muniz Press; 1946, p. 1-145.
68. Mendoza L., Taylor J.W., Ajello L. The class Mesomycetozoea: a heterogeneous group of microorganisms at the animal-fungal boundary. Annu Rev Microbiol 2002, 56:315-344.
69. Mendoza L., Ajello L., Taylor J.W. The taxonomic status of Lacazia loboi and Rhinosporidium seeberi has been finally resolved with the use of molecular tools. Rev Iberoam Micol 2001, 39:309-314.
70. Mendoza L., Herr R.A., Ajello L. Causative agent of Rhinosporidiosis. Author's reply. J Clin Microbiol 2001, 39:413-415.
71. Mendoza L., Herr R., Arseculeratne S.N., Ajello L. In vitro studies on the mechanisms of endospore release by Rhinosporidium seeberi. Mycopathologia 1999, 148:9-15.
72. Minchin E.A., Fantham H.B. Rhinosporidium kinealyi n.g., n.sp. a new sporozoan from the mucous membrane of the septum nasi of man. Q J Microsc Sci 1905, 49:521-532.
73. Mishra R.K., Anand K., Kacker S.K., Sinhea A.N. Ultrastructure of sporangium of Rhinosporidium seeberi. Ind J Microbiol 1968, 8:215-220.
74. Mlouka A., Comte K., Castets A.M., Bouchier C., Tandeau de Marsac N. The gas vesicle gene cluster from Microcystis aeruginosa and DNA rearrangements that lead to loss of cell buoyancy. J Bateriol 2004, 186:2355-2365.
75. Moses J.S., Balachandran C., Singh B., Shanmugan A., Moses D. Rhinosporidium seeberi: light, phase contrast, fluorescent and scanning electron microscopic study. Mycopathologia 1991, 114:17-20.
76. Mulisch M. Chitin in protistan organisms. Eur J Prostistol 1993, 29:1-18.
77. O'Kinealy F. Localised psorospermosis of the mucous membrane of the septum nasi. Proceedings of the Laryngology Society of London 1903, 109-112. [Abstr.].
78. Osawa N. Growth of Mycobacterium leprae in vitro. Proc Japan Acad Ser B 1997, 73:144-149.
79. Otsuka S., Suda S., Li R.H., Matsumoto S., Watanabe M.M. Morphological variability of colonies of Microcystis morphospecies in culture. J Gen Appl Microbiol 2000, 46:39-50.
80. Palinska K.A., Krumbein W.E. Patterns of growth in coccoid, aggregate forming cyanobacteria. Ann Bot Fennici 1998, 35:219-227.
81. Pattyn S.R. The problem of cultivation of Mycobacterium leprae. A review with criteria for evaluating recent experiment work. Bull Org Mond Santé, Bull World Health Org 1973, 49:403-410.
82. Pereira C.N., Di Rosa I., Fagotti A., Simoncelli F., Pascolini R., Mendoza L. The pathogen of frogs and Amphibiocystidium ranae is a member of the order Dermocystida in the class Mesomycetozoea. J Clin Microbiol 2005, 43:192-198.
83. Prins C., Tange R.A., Dingemans K.P. Rhinosporidiosis in The Netherlands. A case report including ultramicroscopic features. ORL J Otorhinolaryngol Relat Spec 1983, 45:237-244.
84. Ragan M.A., Goggin C.L., Cawthorn R.J., Cerenius L., Jamieson A.V., Plourde S.M., et al. A novel clade of protistan parasites near the animal-fungal divergence. Proc Natl Acad Sci USA 1996, 93:11907-11912.
85. Rao S.N. Rhinosporidium seeberi. A histochemical study. Indian J Exp Biol 1966, 4:10-14.
86. Sato S. The apicomplexan plastid and its evolution. Cell Mol Life Sci 2011, 68:1285-1296.
87. Savino D.F., Margo C.E. Conjunctival rhinosporidiosis: light and electron microscopic study. Ophthalmology 1983, 90:1482-1489.
88. Seeber GR. Un nuevo esporozuario parasito del hombre. Dos casos encontrados en polypos nasales. Thesis. Buenos Aires, Argentina: Universidad Nacional de Buenos Aires, Imprenta Libreria Boullosa; 1900.
89. Seeber G.R. Rhinosporidium kinealyi et Rhinosporidium seeberi une question de priorité 1912, La Ciencia Médica, Buenos Aires, Argentina, p. 10.
90. Senba M., Yamashita H. Autofluorescense of Rhinosporidium seeberi. Am J Clin Pathol 1985, 83:132.
91. Silva V., Pereira C.N., Ajello L., Mendoza L. Molecular evidence for multiple host-specific strains in the genus Rhinosporidium. J Clin Microbiol 2005, 43:1865-1868.
92. Sleyter U.B., Messner P., Pum D., Sára M. Crystalline bacterial cell surface layers. Berlin, Heidelberg 1988, Springer-Verlag, New York, London, Paris, Tokyo.
93. Spanggaard B., Huss H.H., Brescianni J. Morphology of Ichthyophonus hoferi assessed by light and scanning electron microscopy. J Fish Dis 1995, 18:567-577.
94. Suh L.H., Barron J., Dubovy S.R., Gaunt M.L., Ledee D.R., Miller D., et al. Occular rhinosporidiosis presenting as chronic follicular conjunctivitis in a contact lens wearer. Arch Ophthalmol 2009, 127:1076-1077.
95. Teh E.C. Surface structure of the endospores of Rhinosporidium seeberi. Sabouraudia 1974, 12:263-265.
96. Teh E.C., Kannan-Kutty M. Rhinosporidium seeberi: spherules and their significance. Pathology 1975, 7:133-137.
97. Thankamani V., Lipin-Dev M.S. Rhinosporidium seeberi proven as a fungus for the first time after a century since its discovery. Res Biotechnol 2012, 3:41-46.
98. Thankamani V., Lipin-Dev M.S. Demonstration of viability and development stages of 10 years old refrigerated culture of Rhinosporidium seeberi (?.) UMH.48 first ever isolated from nasal Rhinosporidiosis yet another milestone, a tribute to Guillermo Seeber. IJPI's J Biotech Biother 2011, 1:11-21.
99. Thankamani V. Rhinosporidium seeberi grown in culture. A ray of hope for the thousands of patients with rhinosporidiosis!!!. South Asian J Socio-Political Studies (SAJOSPS) 2005, 5:118-123.
100. Thianprasit M., Thagernpol K. Rhinosporidiosis. Curr Top Med Mycol 1989, 3:64-85.
101. Vanbreuseghem R. Ultrastructure of Rhinosporidium seeberi. Int J Dermatol 1973, 12:20-28.
102. Vilela R., Rosa P.S., Belone A.F., Taylor J.W., Diório S.M., Mendoza L. Molecular phylogeny of animal pathogen Lacazia loboi inferred from rDNA and DNA coding sequences. Mycol Res 2009, 113:851-857.
103. Vilela R., Martins J.E., Pereira C.N., Melo N., Mendoza L. Molecular study of archival fungal strains isolated from cases of lacaziosis (Jorge Lobo's disease). Mycoses 2007, 50:470-474.
104. Walsby A.E. Structure and function of gas vacuoles. Bacteriol Rev 1972, 36:1-32.
105. Wernicke R. Ueber einen protozoenbefund bei mycosis fungoindes. Zentralbl Bakteriol 1892, 12:859-861.
106. Woodard B., Hudson J. Rhinosporidiosis: ultrastructural study on an infection in South Carolina. South Med J 1984, 77:1587-1588.
107. Wright J. A nasal sporozoon (R. kinealyi). New York Med J 1907, 86:1149-1153.
108. Xinzhang L., Tinnxi L. Observations on the ultrastructure of Rhinosporidium seeberi. Chin J Dermatol 1981, 14:72-74.
109. Yamamoto Y., Shiah F.K. Relationship between cell growth and frequency of dividing cells of Microcystis aeruginosa. Plankton Benthos Res 2010, 5:131-135.
110. Zschokke E. Ein Rhinosporidium beim pferd. Schweizer Arch Tierheilkd 1913, 55:641-650.