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Black Yeast Biota in the Mangrove, in Search of the Origin of the Lethargic Crab Disease (LCD)

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Abstract

Knowledge of natural ecology is essential for a better understanding of pathogenicity and opportunism in black yeast-like fungi. Although etiological agents of diseases caused by these fungi are supposed to originate from the environment, their isolation from nature is difficult. This is probably due to their oligotrophic nature, low competitive ability, and, overall, insufficient data on their natural habitat. We obtained environmental samples from mangrove areas where mortalities by lethargic crab disease (LCD) are reported and areas without disease recorded. Isolation of chaetothyrialean black yeasts and relatives was performed using a highly selective protocol. Species-specific primers were used to determine if these isolates represented Exophiala cancerae or Fonsecaea brasiliensis, two proven agents of LCD, in order to test hypotheses about the origin of the disease. Isolates, identified by morphology as Fonsecaea- or Exophiala-like, were tested specific diagnostic markers for the fungi associated with LCD. Although several black fungi were isolated, the main causative agent of the LCD, E. cancerae, was not found. Molecular markers for F. brasiliensis revealed 10 positive bands for isolates from biofilms on mangrove leaves, branches, and aerial roots, of which four were confirmed by ITS sequencing. The absence of E. cancerae in environmental samples suggests that the species is dependent on the crab, as a genuine pathogen, different from F. brasiliensis, which is probably not dependent on the host species, U. cordatus. However, we did not attempt isolation from the marine water, which may represent the pathway of dispersion of the black yeast species between neighbor mangroves.

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References

  1. Boeger WA, Pie MR, Ostrensky A, Patella L. Lethargic crab disease: multidisciplinary evidence supports a mycotic etiology. Mem Inst Oswaldo Cruz. 2005;100:161–7.

    Article  PubMed  Google Scholar 

  2. Boeger WA, Pie MR, Vicente VA, Ostrensky A, Hungria D, Castilho GG. Histopathology of the mangrove land crab Ucides cordatus (Ocypodidae) affected by lethargic crab disease. Dis Aquat Organ. 2007;78:73–81.

    Article  PubMed  Google Scholar 

  3. Orélis-Ribeiro R, Boeger WA, Vicente VA, Chammas M, Ostrensky A. Fulfilling Koch’s postulates confirms the mycotic origin of Lethargic Crab Disease. Antonie Van Leeuwenhoek. 2011;99:601–8.

    Article  PubMed  Google Scholar 

  4. de Hoog GS, Vicente VA, Najafzadeh MJ, Harrak JM, Badali H, Seyedmousavi S. Waterborne Exophiala species causing disease in cold-blooded animals. Persoonia. 2011;27:46–72.

    Article  PubMed  Google Scholar 

  5. Vicente VA, Orélis-Ribeiro R, Najafzadeh MJ, Sun J, Guerra RS, Miesch S, Ostrenky A, Meis JF, Klaassen CH, de Hoog GS, Boeger WA. Black yeast-like fungi associated with Lethargic Crab Disease (LCD) in the mangrove-land crab, Ucides cordatus (Ocypodidae). Vet Microbiol. 2012;158:109–22.

    Article  PubMed  CAS  Google Scholar 

  6. Ferreira CP, Pie MR, Esteva L, Mancera PFA, Boeger WA, Ostrensky A. Modelling the lethargic crab disease. J Biol Dyn. 2009;3:620–34.

    Article  PubMed  CAS  Google Scholar 

  7. de Hoog GS, Göttlich E, Platas G, Genilloud O, Leotta G, van Brummelen J. Evolution taxonomy and ecology of the genus Thelebolus in Antarctica. Stud Mycol. 2005;51:33–76.

    Google Scholar 

  8. Dixon DM, Shadomy HJ, Shadomy S. Dematiaceous fungal pathogens isolated from nature. Mycopathologia. 1980;70:153–61.

    Article  PubMed  CAS  Google Scholar 

  9. Prenafeta-Boldú FX, Summerbell RC, de Hoog GS. Fungi growing on aromatic hydrocarbons: biotechnology’s unexpected encounter with biohazard. FEMS Microbiol Rev. 2006;30:109–30.

    Article  PubMed  Google Scholar 

  10. Satow MM, Attili-Angelis D, de Hoog GS, Angelis DF, Vicente VA. Selective factors involved in oil flotation isolation of black yeasts from the environment. Stud Mycol. 2008;61:157–63.

    Article  PubMed  CAS  Google Scholar 

  11. Zhao J, Zeng J, de Hoog GS, Attili-Angelis D, Prenafeta-Boldú FX. Isolation of black yeasts by enrichment on atmospheres of monoaromatic hydrocarbons. Microb Ecol. 2010;60:149–56.

    Article  PubMed  CAS  Google Scholar 

  12. Sudhadham M, Dorrestein GM, Prakitsin S, Sivichai S, Chaiyarat R, Prakitsin S, Menken SBJ, de Hoog GS. The neurotropic black yeast Exophiala dermatitidis has a possible origin in the tropical rain forest. Stud Mycol. 2008;61:145–55.

    Article  PubMed  CAS  Google Scholar 

  13. Sterflinger K, de Hoog GS, Haase G. Phylogeny and ecology of meristematic ascomycetes. Stud Mycol. 1999;43:5–22.

    Google Scholar 

  14. Wang CJK, Zabel RA. Identification manual for fungi from utility poles in the Eastern United States. Lawrence: Allen Press; 1990.

    Google Scholar 

  15. Lutzoni F, Pagel M, Reeb V. Major fungal lineages are derived from lichen symbiotic ancestors. Nature. 2001;411:937–40.

    Article  PubMed  CAS  Google Scholar 

  16. Iwatsu T, Miyaji M, Okamoto S. Isolation of Phialophora verrucosa and Fonsecaea pedrosoi from nature in Japan. Mycopathologia. 1981;75:149–58.

    Article  Google Scholar 

  17. Vicente VA, Attili-Angelis D, Pie MR, Queiros-Telles F, Cruz LM, Najafzadeh MJ, de Hoog GS, Pizzirani-Kleiner A. Environmental isolation of black yeast-like fungi involved in human infection. Stud Mycol. 2008;61:137–44.

    Article  PubMed  CAS  Google Scholar 

  18. Pie MR, Boeger W, Patella L, Vicente VA, Orélis-Ribeiro R, Ostrensky A. Specific primers for the detection of the black-yeast fungus associated with lethargic crab disease (LCD). Dis Aquat Organ. 2011;94:73–5.

    Article  PubMed  CAS  Google Scholar 

  19. De Hoog GS, Gerrits van den Ende AHG. Molecular diagnostics of clinical strains of filamentous basidiomycetes. Mycoses. 1998;41:183–9.

    Article  PubMed  Google Scholar 

  20. Fijan N. Systemic mycosis in channel catfish. Wildl Dis. 1969;5:109–10.

    PubMed  CAS  Google Scholar 

  21. Richards RH, Holliman A, Helgason S. Exophiala salmonis infection in Atlantic salmon Salmo salar L. J Fish Dis. 1978;1:357–68.

    Article  Google Scholar 

  22. Reuter RE, Hutchinson W, Ham J, Davis S. Exophiala sp. infection in captured King George whiting (Sillaginodes punctata). Bull Eur Assoc Fish Pathol. 2003;23:128–34.

    Google Scholar 

  23. Manharth A, Lemberger K, Mylniczenko N, Pinkerton M, Pessier AP, Kammeyer P, de Hoog GS. Disseminated phaeohyphomycosis due to Exophiala species in a Galapagos tortoise, Geochelone nigra. J Herpetol Med Surg. 2005;15:20–6.

    Google Scholar 

  24. Nyaoke A, Weber ES, Innis C, Stremme D, Dowd C, Hinckley L, Gorton T, Wickes B, Sutton D, de Hoog S, Frasca S Jr. Disseminated phaeohyphomycosis in weedy, Phyllopteryx taeniolatus, and leafy, Phycodurus eques, seadragons caused by species of Exophiala, including a novel species. J Vet Diagn Invest. 2009;21:69–79.

    Article  PubMed  Google Scholar 

  25. De Hoog GS. Evolution of black yeasts: possible adaptation to the human host. Antonie Van Leeuwenhoek. 1993;63:105–9.

    Article  PubMed  Google Scholar 

  26. Bonifaz A, Badali H, de Hoog GS, Padilla-Desgarennes C, Vázquez-González D, Navarrete G, Meis JF. Severe disseminated phaeohyphomycosis in an immunocompetent patient caused by Veronaea botryosa. Mycopathologia. 2013 (in press).

  27. Li DM, Li RY, de Hoog GS, Wang YX, Wang DL. Exophiala asiatica, a new species from a fatal case in China. Med Mycol. 2009;47:101–9.

    Article  PubMed  CAS  Google Scholar 

  28. De Hoog GS. Significance of fungal evolution for the understanding of their pathogenicity illustrated with agents of phaeohyphomycosis. Mycoses. 1997;40 Suppl 2:5–8. doi:10.1111/j.1439-0507.1997.tb00555.x.

  29. Li DM, de Hoog GS, Lindhardt Saunte DM, Gerrits van den Ende AHG, Chen XR. Coniosporium epidermidis sp. nov., a new species from human skin. Stud Mycol. 2008;61:131–6.

    Article  PubMed  CAS  Google Scholar 

  30. de Hoog GS, Nishikaku AS, Fernández Zeppenfeldt G, Padín-González C, Burger E, Badali H, Gerrits van den Ende AHG. Molecular analysis and pathogenicity of the Cladophialophora carrionii complex, with the description of a novel species. Stud Mycol. 2007;58:219–34.

    Article  PubMed  Google Scholar 

  31. Heinrichs G, Hübner I, Schmidt GK, de Hoog GS, Haase G. Compositional analysis of dark fungal biofilms from water taps using Tag Encoded FLX Amplicon Pyrosequencing. Mycopathologia. 2013 (in press).

  32. Schmidt AJ. Estudo da dinâmica populacional do caranguejo-uçá, Ucides cordatus (Linnaeus, 1763) (Crustacea-Decapoda-Brachyura), e dos efeitos de uma mortalidade em massa desta espécie em manguezais do Sul da Bahia. Dissertation (in Portuguese). Universidade de São Paulo, Brazil. 2006.

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Acknowledgments

Bert Gerrits van de Ende are thanked for technical assistance. The work of Vania A. Vicente was supported by Brazilian Government fellowship from Coordenação de Aperfeiçoamento de Pessoal de Nivel Superior (CAPES) and the work of Mohammad Javad Najafzadeh by Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran. The authors also wish to thank the Brazilian agencies CAPES/Ministério da Educação—Brazil and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for financial support.

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Authors and Affiliations

  1. Department of Basic Pathology, Federal University of Paraná, Curitiba, CEP 81531–980, Brazil

    Raquel Schier Guerra, Mariana Machado Fidelis do Nascimento, Raphael Orélis Ribeiro, Gerrit Sybren de Hoog & Vania Aparecida Vicente

  2. Department of Zoology, Federal University of Paraná, Curitiba, CEP 81531–980, Brazil

    Walter A. Boeger

  3. Grupo Integrado de Aqüicultura e Estudos Ambientais, Federal University of Paraná, Curitiba, Brazil

    Antonio Ostrensky

  4. CBS Fungal Biodiversity Centre, Utrecht, The Netherlands

    Stephanie Miesch & Gerrit Sybren de Hoog

  5. Department of Parasitology and Mycology, Cancer Molecular Pathology Research Center, Ghaem Hospital, School of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran

    Mohammad Javad Najafzadeh

  6. Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Brasília, Brazil

    Walter A. Boeger

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  1. Raquel Schier Guerra
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  2. Mariana Machado Fidelis do Nascimento
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  3. Stephanie Miesch
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  4. Mohammad Javad Najafzadeh
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  5. Raphael Orélis Ribeiro
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  7. Gerrit Sybren de Hoog
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  8. Vania Aparecida Vicente
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  9. Walter A. Boeger
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Corresponding authors

Correspondence to Vania Aparecida Vicente or Walter A. Boeger.

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Guerra, R.S., do Nascimento, M.M.F., Miesch, S. et al. Black Yeast Biota in the Mangrove, in Search of the Origin of the Lethargic Crab Disease (LCD). Mycopathologia 175, 421–430 (2013). https://doi.org/10.1007/s11046-013-9636-1

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  • DOI: https://doi.org/10.1007/s11046-013-9636-1

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