On and Under the Skin: Emerging Basidiomycetous Yeast Infections Caused by Species

1. Sugita T Trichosporon behrend (1890). in: Kurtzman C.P., Fell J.W., Boekhout T. (Eds.) The yeasts: a taxonomic study. 5th ed. Elsevier Science, Amsterdam. 2004; 2011:2015–2061.

2. Ageitos JM, Vallejo JA, Veiga-Crespo P, Villa TG Oily yeasts as oleaginous cell factories. Appl Microbiol Biotechnol 2011; 90: 1219–1227. doi: 10.1007/s00253-011-3200-z 21465305

3. Xiong L, Huang C, Li XM, Chen XF, Wang B, Wang C,et al. Acetone-Butanol-Ethanol (ABE) Fermentation Wastewater Treatment by oleaginous yeast Trichosporon cutaneum. Appl Biochem Biotechnol 2015. In press.

4. Tamis J, Sorokin DY, Jiang Y, van Loosdrecht MC, Kleerebezem R Lipid recovery from a vegetable oil emulsion using microbial enrichment cultures. Biotechnol Biofuels 2015; 8:39. doi: 10.1186/s13068-015-0228-9 25798194

5. Nhi Cong le T, Ngoc Mai CT, Thanh VT, Nga le P, Minh NN Application of a biofilm formed by a mixture of yeasts isolated in Vietnam to degrade aromatic hydrocarbon polluted wastewater collected from petroleum storage. Water Sci Technol 2014; 70: 329–336. doi: 10.2166/wst.2014.233 25051481

6. Middelhoven WJ, Scorzetti G, Fell JW Systematics of the anamorphic basidiomycetous yeast genus Trichosporon Behrend with the description of five novel species: Trichosporon vadense, T. smithiae, T. dehoogii, T. scarabaeorum and T. gamsii. Int J Syst Evol Microbiol 2004; 54: 975–986. 15143052

7. Zhang E, Sugita T, Tsuboi R, Yamazaki T, Makimura K The opportunistic yeast pathogen Trichosporon asahii colonizes the skin of healthy individuals: analysis of 380 healthy individuals by age and gender using a nested polymerase chain reaction assay. Microbiol Immunol 2011; 55: 483–4888. doi: 10.1111/j.1348-0421.2011.00341.x 21707737

8. Zhang E, Tanaka T, Tajima M, Tsuboi R, Nishikawa A, Sugita T Characterization of the skin fungal microbiota in patients with atopic dermatitis and in healthy subjects. Microbiol Immunol 2011; 55: 625–632. doi: 10.1111/j.1348-0421.2011.00364.x 21699559

9. Hamad I, Sokhna C, Raoult D, Bittar F Molecular detection of eukaryotes in a single human stool sample from Senegal. PLoS One 2012; 7: e40888. doi: 10.1371/journal.pone.0040888 22808282

10. Gouba N, Raoult D, Drancourt M Eukaryote culturomics of the gut reveals new species. PLoS One 2014; 9: e106994. doi: 10.1371/journal.pone.0106994 25210972

11. Silvestre AM Jr, Miranda MAR, Camargo ZP Trichosporon species isolated from the perigenital region, urine and catheters of a Brazilian population. Braz J Microbiol 2010; 41: 628–634. doi: 10.1590/S1517-83822010000300013 24031538

12. Colombo AL, Padovan ACB, Chaves GM Current knowledge of Trichosporon spp. and trichosporonosis. Clin Microbiol Rev 2011; 24: 682–700. doi: 10.1128/CMR.00003-11 21976604

13. Gueho E, de Hoog GS, Smith MT Neotypification of the genus Trichosporon. Antonie Van Leeuwenhoek 1992; 61: 285–288 1497333

14. Motaung TE, Albertyn J, Kock JL, Lee CF, Suh SO, et al. Trichosporon vanderwaltii sp. nov., an asexual basidiomycetous yeast isolated from soil and beetles. Antonie Van Leeuwenhoek 2013; 103: 313–319. doi: 10.1007/s10482-012-9811-2 22996387

15. Girmenia C, Pagano L, Martino B, D’Antonio D, Fanci R, Blackweel M, et al. Invasive infections caused by Trichosporon species and Geotrichum capitatum in patients with hematological malignancies: a retrospective multicenter study from Italy and review of the literature. J Clin Microbiol 2005; 43: 1818–1828. 15815003

16. Donnarumma H, Bentubo L, Fischman-Gompertz O Effects of temperature and incubation time on the in vitro expression of proteases, phospholipases, lipases and DNases by different species of Trichosporon. SpringerPlus 2014; 3: 377. doi: 10.1186/2193-1801-3-377 25161862

17. Taj-Aldeen SJ, Al-Ansari N, El Shafei S, Meis JF, Curfs-Breuker I, Theelen B, et al. Molecular identification and susceptibility of Trichosporon species isolated from clinical specimens in Qatar: isolation of Trichosporon dohaense Taj-Aldeen, Meis & Boekhout sp. nov. J Clin Microbiol 2009; 47: 1791–1799. doi: 10.1128/JCM.02222-08 19321719

18. Iturrieta-González IA, Padovan AC, Bizerra FC, Hahn RC, Colombo AL Multiple species of Trichosporon produce biofilms highly resistant to triazoles and amphotericin B. PLoS One 2014; 9: e109553. doi: 10.1371/journal.pone.0109553 25360765

19. Serena C, Pastor FJ, Gilgado F, Mayayo E, Guarro J Efficacy of micafungin in combination with other drugs in a murine model of disseminated trichosporonosis. Antimicrob Agents Chemother 2005; 49: 497–502. 15673724

20. Treviño-Rangel RD, López LJ, Palma-Nicolás JP, Hernández-Bello R, González JG, González GM Therapeutic efficacy of posaconazole in a murine model of disseminated trichosporonosis. J Antimicrob Chemother 2014; 69: 1075–1078. doi: 10.1093/jac/dkt466 24252752

21. Ochsner UA, Glumoff V, Kälin M, Fiechter A, Reiser J Genetic transformation of auxotrophic mutants of the filamentous yeast Trichosporon cutaneum using homologous and heterologous marker genes. Yeast 1991; 7:513–524. 1897316

22. Reiser J, Glumoff V, Ochsner UA, Fiechter A Molecular analysis of the Trichosporon cutaneum DSM 70698 argA gene and its use for DNA-mediated transformations. J Bacteriol 1994; 176: 3021–3032. 8188603

23. Yang RY, Li HT, Zhu H, Zhou GP, Wang M, Wang L. Draft genome sequence of CBS 2479, the standard type strain of Trichosporon asahii. Eukaryot Cell 2012; 11:1415–1416. doi: 10.1128/EC.00237-12 23104369

24. Yang RY, Li HT, Zhu H, Zhou GP, Wang M, Wang L Genome sequence of the Trichosporon asahii environmental strain CBS 8904. Eukaryot Cell 2012; 11: 1586–1587. doi: 10.1128/EC.00264-12 23193141

25. Xu J, Saunders CW, Hu P, Grant RA, Boekhout T, Kuramae EE, et al. Dandruff-associatedMalassezia genomes reveal convergent and divergent virulence traits shared with plant and human fungal pathogens. Proc Natl Acad Sci 2007; 104: 18730–18735. 18000048

26. White TC, Findley K, Dawson TL Jr, Scheynius A, Boekhout T, Cuomo CA et al. Fungi on the skin: dermatophytes and Malassezia. Cold Spring Harb Perspect Med 2014; 4:a019802 doi: 10.1101/cshperspect.a019802 25085959

27. Loftus BJ, Fung E, Roncaglia P, Rowley D, Amedeo P, Bruno D, et al. The genome of the basidiomycetous yeast and human pathogen Cryptococcus neoformans. Science 2005; 307: 1321–1324. 15653466

28. D'Souza CA, Kronstad JW, Taylor G, Warren R, Yuen M, Hu G, et al. Genome variation in Cryptococcus gattii, an emerging pathogen of immunocompetent hosts. MBio 2011; 2: e00342–10. doi: 10.1128/mBio.00342-10 21304167

29. Gold I, Sommer B, Urson S, Schewach-Millet M White piedra. A frequently misdiagnosed infection of hair. Int J Dermatol 1984; 23: 621–623. 6542905

30. Han MH, Choi JH, Sung KJ, Moon KC, Koh JK Onychomycosis and Trichosporon beigelii in Korea. Int J Dermatol 2000; 39: 266–269. 10809974

31. Archer-Dubon C, Orozco-Topete R, Leyva-Santiago J, Arenas R, Carbajosa J, Ysunza A Superficial mycotic infections of the foot in a native pediatric population: a pathogenic role for Trichosporon cutaneum? Pediatr Dermatol 2003; 20: 299–302. 12869147

32. Kolecka A, Khayhan K, Groenewald M, Theelen B, Arabatzis M, Velegraki A, et al. Identification of medically relevant species of arthroconidial yeasts by use of matrix-assisted laser desorption ionization-time of flight mass spectrometry. J Clin Microbiol 2013; 51: 2491–2500. doi: 10.1128/JCM.00470-13 23678074

33. de Almeida Júnior JN, Figueiredo DS, Toubas D, Del Negro GM, Motta AL, Rossi F, et al. Usefulness of matrix-assisted laser desorption ionisation-time-of-flight mass spectrometry for identifying clinical Trichosporon isolates. Clin Microbiol Infect 2014; 20: 784–790. doi: 10.1111/1469-0691.12502 24355037

34. Diaz MR, Fell JW High-throughput detection of pathogenic yeasts of the genus Trichosporon. J Clin Microbiol 2004; 42: 3696–3706 15297519

35. Chagas-Neto TC, Chaves GM, Melo AS, Colombo AL Bloodstream infections due to Trichosporon spp.: species distribution, Trichosporon asahii genotypes determined on the basis of ribosomal DNA intergenic spacer 1 sequencing, and antifungal susceptibility testing. J Clin Microbiol 2009; 47: 1074–1081. doi: 10.1128/JCM.01614-08 19225102

36. Baka S, Tsouma I, Kouskouni E Fatal lower limb infection by Trichosporon asahii in an immunocompetent patient. Acta Dermatovenerol Croat 2013; 21: 241–244 24476611

37. Rodriguez-Tudela JL, Diaz-Guerra TM, Mellado E, Cano V, Tapia C, Perkins A, et al. Susceptibility patterns and molecular identification of Trichosporon species. Antimicrob Agents Chemother 2005; 49: 4026–4034. 16189076

38. Rodrigues Gda S, de Faria RR, Guazzelli LS, Oliveira Fde M, Severo LC Nosocomial infection due to Trichosporon asahii: clinical revision of 22 cases. Rev Iberoam Micol. 2006: 23: 85–89. 16854183

39. Pfaller MA, Diekema DJ, Gibbs DL, Newell VA, Bijie H, Dzierzanowska D, et al. Results from the ARTEMIS DISK Global Antifungal Surveillance Study, 1997 to 2007: 10.5-year analysis of susceptibilities of noncandidal yeast species to fluconazole and voriconazole determined by CLSI standardized disk diffusion testing. J Clin Microbiol 2009; 47: 117–123. doi: 10.1128/JCM.01747-08 19005141

40. Caira M, Trecarichi EM, Tumbarello M, Leone G, Pagano L Uncommon yeast infections in hematological patients: from diagnosis to treatment. Expert Rev Anti Infect Ther 2011; 9: 1067–1075. doi: 10.1586/eri.11.124 22029524

41. Fischman O, Bezerra FC, Francisco EC, da Silva FC, Nishikaku AS, Cavalcanti SD Trichosporon inkin: an uncommon agent of scalp white piedra. Report of four cases in brazilian children. Mycopathologia 2014; 178: 85–89. doi: 10.1007/s11046-014-9750-8 24952012

42. Matsue K, Uryu H, Koseki M, Asada N, Takeuchi M Breakthrough trichosporonosis in patients with hematologic malignancies receiving micafungin. Clin Infect Dis 2006; 42: 753–757. 16477548

43. Madariaga MG, Tenorio A, Proia L Trichosporon inkin peritonitis treated with caspofungin. J Clin Microbiol 2003; 41: 5827–5829. 14662994

44. Serena C, Gilgado F, Mariné M, Pastor FJ, Guarro J Efficacy of voriconazole in a guinea pig model of invasive trichosporonosis. Antimicrob Agents Chemother 2006; 50: 2240–2243. 16723595

45. Arendrup MC, Boekhout T, Akova M, Meis JF, Cornely OA, Lortholary O European Society of Clinical Microbiology and Infectious Diseases Fungal Infection Study Group; European Confederation of Medical Mycology. ESCMID and ECMM joint clinical guidelines for the diagnosis and management of rare invasive yeast infections. Clin Microbiol Infect Suppl 2014; 3:76–98.

46. Hatipoglu N, Hatipoglu H Combination antifungal therapy for invasive fungal infections in children and adults. Expert Rev Anti Infect Ther 2013; 11:523–535. doi: 10.1586/eri.13.29 23627858

47. Hosokawa K, Yamazaki H, Mochizuki K, Ohata K, Ishiyama K, Hayashi T, et al. Successful treatment of Trichosporon fungemia in a patient with refractory acute myeloid leukemia using voriconazole combined with liposomal amphotericin B. Transpl Infect Dis 2012; 14:184–187. doi: 10.1111/j.1399-3062.2011.00670.x 22093149

48. Kozubowski L, Heitman J Profiling a killer, the development of Cryptococcus neoformans. FEMS Microbiol Rev 2012; 36: 78–94. doi: 10.1111/j.1574-6976.2011.00286.x 21658085

49. Suarez F, Olivier G, Garcia-Hermoso D, Randriamalala E, Ghez D, Bruneau J, et al. Breakthrough Hormographiella aspergillata infections arising in neutropenic patients treated empirically with caspofungin. J Clin Microbiol 2011; 49: 461–465. doi: 10.1128/JCM.01213-10 21068290

50. Chrenkova V, Kolarik M, Hubacek P, Kolarik J, Simonek J, et al. Possible Tyromyces fissilis (Basidiomycota, Polyporales) co-infection in a lung transplant recipient. Folia Microbiol (Praha) 2015; 60: 33–35.

51. García-Suárez J, Gómez-Herruz P, Cuadros JA, Burgaleta C Epidemiology and outcome of Rhodotorula infection in haematological patients. Mycoses 2011; 54: 318–324. doi: 10.1111/j.1439-0507.2010.01868.x 20337934

52. Iatta R, Cafarchia C, Cuna T, Montagna O, Laforgia N, Gentile O, et al. Bloodstream infections by Malassezia and Candida species in critical care patients. Med Mycol 2014; 52:264–269. doi: 10.1093/mmy/myt004 24576998

53. Tuon FF, Morales HM, Penteado-Filho SR, da-Silva MM, Quadros Id, Hamoui El A Central venous catheter-related bloodstream infection and Cryptococcus neoformans. Braz J Infect Dis 2009; 13: 317–318. 20231999

54. Fonseca FL, Frases S, Casadevall A, Fischman-Gompertz O, Nimrichter L, Rodrigues ML Structural and functional properties of the Trichosporon asahii glucuronoxylomannan. Fungal Genet Biol 2009; 46: 496–505. doi: 10.1016/j.fgb.2009.03.003 19285564

55. Achterman RR, White TC A foot in the door for dermatophyte research. PLoS Pathog 2012; 8:e1002564. doi: 10.1371/journal.ppat.1002564 22479177

56. Giddey K, Favre B, Quadroni M, Monod M Closely related dermatophyte species produce different patterns of secreted proteins. FEMS Microbiol Lett 2007; 267: 95–101. 17156126

57. Mariné M, Pedro Bom VL, de Castro PA, Winkelstroter LK, Ramalho LN, Brown NA, et al. The development of animal infection models and antifungal efficacy assays against clinical isolates of Trichosporon asahii, T. asteroides and T. inkin. Virulence 2015. In press.

58. Tabei Y, Kiryu H, Kin T, Asai K A fast structural multiple alignment method for long RNA sequences. BMC Bioinformatics 2008; 9:33. doi: 10.1186/1471-2105-9-33 18215258

59. Kück P, Meusemann K FASconCAT: Convenient handling of data matrices. Mol Phylogenet Evol 2010; 56:1115–1118. doi: 10.1016/j.ympev.2010.04.024 20416383

60. Stamatakis A RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 2006; 22:2688–2690. 16928733

61. Higgs PG RNA secondary structure: physical and computational aspects. Q Rev Biophys 2000; 33:199–253. 11191843

62. Jow H, Hudelot C, Rattray M, Higgs PG Bayesian phylogenetics using an RNA substitution model applied to early mammalian evolution. Mol Biol Evol 2002; 19:1591–1601. 12200486

63. Hudelot C, Gowri-Shankar V, Jow H, Rattray M, Higgs PG RNA-based phylogenetic methods: application to mammalian mitochondrial RNA sequences. Mol Phylogenet Evol 2003; 28:241–252. 12878461

64. Yang Z Among-site rate variation and its impact on phylogenetic analyses. Trends Ecol Evol 1996; 11:367–372. 21237881