No metrics data to plot.
The attempt to load metrics for this article has failed.
The attempt to plot a graph for these metrics has failed.

Skin Fungi from Colonization to Infection

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.
  • PDF
    4.49 MB
  • XML
    133.67 Kb
  • HTML
    122.52 Kb
  • Authors: Sybren de Hoog1, Michel Monod2, Tom Dawson3, Teun Boekhout4, Peter Mayser5, Yvonne Gräser6
  • Editor: Joseph Heitman7
    Affiliations: 1: Westerdijk Fungal Biodiversity Institute, 3584 CT Utrecht, The Netherlands; 2: Department of Dermatology, Centre Hospitalier Universitaire Vaudois, 1011 Lausanne, Switzerland; 3: Institute of Medical Biology, Agency for Science, Technology, and Research, Singapore 138648; 4: Westerdijk Fungal Biodiversity Institute, 3584 CT Utrecht, The Netherlands; 5: Universitätsklinikum Giessen Hautklinik, 35392 Giessen, Germany; 6: Nationales Konsiliarlabor für Dermatophyten, Institut für Mikrobiologie und Hygiene, 12203 Berlin, Germany; 7: Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, NC 27710
  • Source: microbiolspec July 2017 vol. 5 no. 4 doi:10.1128/microbiolspec.FUNK-0049-2016
  • Received 03 June 2016 Accepted 12 May 2017 Published 14 July 2017
  • Sybren de Hoog, [email protected]
image of Skin Fungi from Colonization to Infection
    Preview this microbiology spectrum article:
    Zoom in

    Skin Fungi from Colonization to Infection, Page 1 of 2

    | /docserver/preview/fulltext/microbiolspec/5/4/FUNK-0049-2016-1.gif /docserver/preview/fulltext/microbiolspec/5/4/FUNK-0049-2016-2.gif
  • Abstract:

    Humans are exceptional among vertebrates in that their living tissue is directly exposed to the outside world. In the absence of protective scales, feathers, or fur, the skin has to be highly effective in defending the organism against the gamut of opportunistic fungi surrounding us. Most (sub)cutaneous infections enter the body by implantation through the skin barrier. On intact skin, two types of fungal expansion are noted: (A) colonization by commensals, i.e., growth enabled by conditions prevailing on the skin surface without degradation of tissue, and (B) infection by superficial pathogens that assimilate epidermal keratin and interact with the cellular immune system. In a response-damage framework, all fungi are potentially able to cause disease, as a balance between their natural predilection and the immune status of the host. For this reason, we will not attribute a fixed ecological term to each species, but rather describe them as growing in a commensal state (A) or in a pathogenic state (B).

  • Citation: de Hoog S, Monod M, Dawson T, Boekhout T, Mayser P, Gräser Y. 2017. Skin Fungi from Colonization to Infection. Microbiol Spectrum 5(4):FUNK-0049-2016. doi:10.1128/microbiolspec.FUNK-0049-2016.


1. Casadevall A, Pirofski LA. 2015. What is a host? Incorporating the microbiota into the damage-response framework. Infect Immun 83:2–7 http://dx.doi.org/10.1128/IAI.02627-14.
2. Agosta SJ, Janz N, Brooks DR. 2010. How specialists can be generalists: resolving the “parasite paradox” and implications for emerging infectious disease. Zoologia Curitiba 27:151–162 http://dx.doi.org/10.1590/S1984-46702010000200001.
3. Bonifaz A, Badali H, de Hoog GS, Cruz M, Araiza J, Cruz MA, Fierro L, Ponce RM. 2008. Tinea nigra by Hortaea werneckii, a report of 22 cases from Mexico. Stud Mycol 61:77–82 http://dx.doi.org/10.3114/sim.2008.61.07.
4. Gunde-Cimermana N, Zalarb P, de Hoog S, Plemenitaš A. 2000. Hypersaline waters in salterns - natural ecological niches for halophilic black yeasts. FEMS Microbiol Ecol 32:235–240.
5. Kejžar A, Cibic M, Grøtli M, Plemenitaš A, Lenassi M. 2015. The unique characteristics of HOG pathway MAPKs in the extremely halotolerant Hortaea werneckii. FEMS Microbiol Lett 362:fnv046 http://dx.doi.org/10.1093/femsle/fnv046.
6. Batra R, Boekhout T, Guého E, Cabañes FJ, Dawson TL Jr, Gupta AK. 2005. Malassezia Baillon, emerging clinical yeasts. FEMS Yeast Res 5:1101–1113 http://dx.doi.org/10.1016/j.femsyr.2005.05.006.
7. Gupta AK, Batra R, Bluhm R, Boekhout T, Dawson TL Jr. 2004. Skin diseases associated with Malassezia species. J Am Acad Dermatol 51:785–798 http://dx.doi.org/10.1016/j.jaad.2003.12.034. [PubMed]
8. Gaitanis G, Magiatis P, Hantschke M, Bassukas ID, Velegraki A. 2012. The Malassezia genus in skin and systemic diseases. Clin Microbiol Rev 25:106–141 http://dx.doi.org/10.1128/CMR.00021-11.
9. Wu G, Zhao H, Li C, Rajapakse MP, Wong WC, Xu J, Saunders CW, Reeder NL, Reilman RA, Scheynius A, Sun S, Billmyre BR, Li W, Averette AF, Mieczkowski P, Heitman J, Theelen B, Schröder MS, De Sessions PF, Butler G, Maurer-Stroh S, Boekhout T, Nagarajan N, Dawson TL Jr. 2015. Genus-wide comparative genomics of Malassezia delineates its phylogeny, physiology, and niche adaptation on human skin. PLoS Genet 11:e1005614 http://dx.doi.org/10.1371/journal.pgen.1005614.
10. Gräser Y, de Hoog GS, Kuijpers AFA. 2000. Recent advances in the molecular taxonomy of dermatophytes. In Kushwaha RKS, Guarro J (ed), Biology of Dermatophytes and other Keratinophilic Fungi. Rev Iberoam Micol 17:17–21.
11. Rezaei-Matehkolaei A, Mirhendi H, Makimura K, de Hoog GS, Satoh K, Najafzadeh MJ, Shidfar MR. 2014. Nucleotide sequence analysis of beta tubulin gene in a wide range of dermatophytes. Med Mycol 52:674–688 http://dx.doi.org/10.1093/mmy/myu033.
12. Mirhendi H, Makimura K, de Hoog GS, Rezaei-Matehkolaei A, Najafzadeh MJ, Umeda Y, Ahmadi B. 2015. Translation elongation factor 1-α gene as a potential taxonomic and identification marker in dermatophytes. Med Mycol 53:215–224 http://dx.doi.org/10.1093/mmy/myu088.
13. de Hoog GS, Dukik K, Monod M, Packeu A, Stubbe D, Hendrickx M, Kupsch C, Stielow JB, Freeke J, Göker M, Rezaei-Matehkolaei A, Mirhendi H, Gräser Y. 2017. Toward a novel multilocus phylogenetic taxonomy for the dermatophytes. Mycopathologia 182:5–31 http://dx.doi.org/10.1007/s11046-016-0073-9.
14. Sriranganadane D, Waridel P, Salamin K, Feuermann M, Mignon B, Staib P, Neuhaus JM, Quadroni M, Monod M. 2011. Identification of novel secreted proteases during extracellular proteolysis by dermatophytes at acidic pH. Proteomics 11:4422–4433 http://dx.doi.org/10.1002/pmic.201100234.
15. Burmester A, Shelest E, Glöckner G, Heddergott C, Schindler S, Staib P, Heidel A, Felder M, Petzold A, Szafranski K, Feuermann M, Pedruzzi I, Priebe S, Groth M, Winkler R, Li W, Kniemeyer O, Schroeckh V, Hertweck C, Hube B, White TC, Platzer M, Guthke R, Heitman J, Wöstemeyer J, Zipfel PF, Monod M, Brakhage AA. 2011. Comparative and functional genomics provide insights into the pathogenicity of dermatophytic fungi. Genome Biol 12:R7 http://dx.doi.org/10.1186/gb-2011-12-1-r7. [PubMed]
16. Jousson O, Léchenne B, Bontems O, Capoccia S, Mignon B, Barblan J, Quadroni M, Monod M. 2004. Multiplication of an ancestral gene encoding secreted fungalysin preceded species differentiation in the dermatophytes Trichophyton and Microsporum. Microbiology 150:301–310 http://dx.doi.org/10.1099/mic.0.26690-0.
17. Jousson O, Léchenne B, Bontems O, Mignon B, Reichard U, Barblan J, Quadroni M, Monod M. 2004. Secreted subtilisin gene family in Trichophyton rubrum. Gene 339:79–88 http://dx.doi.org/10.1016/j.gene.2004.06.024.
18. Giddey K, Favre B, Quadroni M, Monod M. 2007. Closely related dermatophyte species produce different patterns of secreted proteins. FEMS Microbiol Lett 267:95–101 http://dx.doi.org/10.1111/j.1574-6968.2006.00541.x.
19. Zaugg C, Monod M, Weber J, Harshman K, Pradervand S, Thomas J, Bueno M, Giddey K, Staib P. 2009. Gene expression profiling in the human pathogenic dermatophyte Trichophyton rubrum during growth on proteins. Eukaryot Cell 8:241–250 http://dx.doi.org/10.1128/EC.00208-08.
20. Monod M, Léchenne B, Jousson O, Grand D, Zaugg C, Stöcklin R, Grouzmann E. 2005. Aminopeptidases and dipeptidyl-peptidases secreted by the dermatophyte Trichophyton rubrum. Microbiology 151:145–155 http://dx.doi.org/10.1099/mic.0.27484-0.
21. Zaugg C, Jousson O, Léchenne B, Staib P, Monod M. 2008. Trichophyton rubrum secreted and membrane-associated carboxypeptidases. Int J Med Microbiol 298:669–682 http://dx.doi.org/10.1016/j.ijmm.2007.11.005.
22. Byun T, Kofod L, Blinkovsky A. 2001. Synergistic action of an X-prolyl dipeptidyl aminopeptidase and a non-specific aminopeptidase in protein hydrolysis. J Agric Food Chem 49:2061–2063 http://dx.doi.org/10.1021/jf001091m.
23. Sriranganadane D, Waridel P, Salamin K, Reichard U, Grouzmann E, Neuhaus JM, Quadroni M, Monod M. 2010. Aspergillus protein degradation pathways with different secreted protease sets at neutral and acidic pH. J Proteome Res 9:3511–3519 http://dx.doi.org/10.1021/pr901202z.
24. Staib P, Zaugg C, Mignon B, Weber J, Grumbt M, Pradervand S, Harshman K, Monod M. 2010. Differential gene expression in the pathogenic dermatophyte Arthroderma benhamiae in vitro versus during infection. Microbiology 156:884–895 http://dx.doi.org/10.1099/mic.0.033464-0.
25. Méhul B, Gu Z, Jomard A, Laffet G, Feuilhade M, Monod M. 2016. Sub6 (Tri r 2), an onychomycosis marker revealed by proteomics analysis of Trichophyton rubrum secreted proteins in patient nail samples. J Invest Dermatol 136:331–333 http://dx.doi.org/10.1038/JID.2015.367.
26. Woodfolk JA, Wheatley LM, Piyasena RV, Benjamin DC, Platts-Mills TA. 1998. Trichophyton antigens associated with IgE antibodies and delayed type hypersensitivity. Sequence homology to two families of serine proteinases. J Biol Chem 273:29489–29496 http://dx.doi.org/10.1074/jbc.273.45.29489.
27. Lorenz MC, Fink GR. 2001. The glyoxylate cycle is required for fungal virulence. Nature 412:83–86 http://dx.doi.org/10.1038/35083594.
28. McKinney JD, Höner zu Bentrup K, Muñoz-Elías EJ, Miczak A, Chen B, Chan WT, Swenson D, Sacchettini JC, Jacobs WR Jr, Russell DG. 2000. Persistence of Mycobacterium tuberculosis in macrophages and mice requires the glyoxylate shunt enzyme isocitrate lyase. Nature 406:735–738 http://dx.doi.org/10.1038/35021074.
29. Grumbt M, Defaweux V, Mignon B, Monod M, Burmester A, Wöstemeyer J, Staib P. 2011. Targeted gene deletion and in vivo analysis of putative virulence gene function in the pathogenic dermatophyte Arthroderma benhamiae. Eukaryot Cell 10:842–853 http://dx.doi.org/10.1128/EC.00273-10.
30. Veien NK, Hattel T, Laurberg G. 1994. Plantar Trichophyton rubrum infections may cause dermatophytids on the hands. Acta Derm Venereol 74:403–404. [PubMed]
31. Gianni C, Betti R, Crosti C. 1996. Psoriasiform id reaction in tinea corporis. Mycoses 39:307–308 http://dx.doi.org/10.1111/j.1439-0507.1996.tb00144.x. [PubMed]
32. Liu ZH, Shen H, Xu AE. 2011. Severe kerion with dermatophytid reaction presenting with diffuse erythema and pustules. Mycoses 54:e650–e652 http://dx.doi.org/10.1111/j.1439-0507.2010.01973.x.
33. Cheng N, Rucker Wright D, Cohen BA. 2011. Dermatophytid in tinea capitis: rarely reported common phenomenon with clinical implications. Pediatrics 128:e453–e457 http://dx.doi.org/10.1542/peds.2010-2757.
34. Ilkit M, Durdu M, Karakaş M. 2012. Cutaneous id reactions: a comprehensive review of clinical manifestations, epidemiology, etiology, and management. Crit Rev Microbiol 38:191–202 http://dx.doi.org/10.3109/1040841X.2011.645520.
35. Slunt JB, Taketomi EA, Woodfolk JA, Hayden ML, Platts-Mills TA. 1996. The immune response to Trichophyton tonsurans: distinct T cell cytokine profiles to a single protein among subjects with immediate and delayed hypersensitivity. J Immunol 157:5192–5197. [PubMed]
36. Woodfolk JA, Platts-Mills TA. 2001. Diversity of the human allergen-specific T cell repertoire associated with distinct skin test reactions: delayed-type hypersensitivity-associated major epitopes induce Th1- and Th2-dominated responses. J Immunol 167:5412–5419 http://dx.doi.org/10.4049/jimmunol.167.9.5412.
37. Woodfolk JA. 2005. Allergy and dermatophytes. Clin Microbiol Rev 18:30–43 http://dx.doi.org/10.1128/CMR.18.1.30-43.2005.
38. Martinez DA, Oliver BG, Gräser Y, Goldberg JM, Li W, Martinez-Rossi NM, Monod M, Shelest E, Barton RC, Birch E, Brakhage AA, Chen Z, Gurr SJ, Heiman D, Heitman J, Kosti I, Rossi A, Saif S, Samalova M, Saunders CW, Shea T, Summerbell RC, Xu J, Young S, Zeng Q, Birren BW, Cuomo CA, White TC. 2012. Comparative genome analysis of Trichophyton rubrum and related dermatophytes reveals candidate genes involved in infection. MBio 3:e00259-12 http://dx.doi.org/10.1128/mBio.00259-12.
39. Li W, Metin B, White TC, Heitman J. 2010. Organization and evolutionary trajectory of the mating type ( MAT) locus in dermatophyte and dimorphic fungal pathogens. Eukaryot Cell 9:46–58 http://dx.doi.org/10.1128/EC.00259-09.
40. Symoens F, Jousson O, Packeu A, Fratti M, Staib P, Mignon B, Monod M. 2013. The dermatophyte species Arthroderma benhamiae: intraspecies variability and mating behaviour. J Med Microbiol 62:377–385 http://dx.doi.org/10.1099/jmm.0.053223-0.
41. Anzawa K, Kawasaki M, Mochizuki T, Ishizaki H. 2010. Successful mating of Trichophyton rubrum with Arthroderma simii. Med Mycol 48:629–634 http://dx.doi.org/10.3109/13693780903437884.
42. Kawasaki M. 2011. Verification of a taxonomy of dermatophytes based on mating results and phylogenetic analyses. Med Mycol J 52:291–295 http://dx.doi.org/10.3314/mmj.52.291.
43. Kano R, Yoshida E, Yaguchi T, Hubka V, Anzawa K, Mochizuki T, Hasegawa A, Kamata H. 2014. Mating type gene (MAT1-2) of Trichophyton verrucosum. Mycopathologia 177:87–90 http://dx.doi.org/10.1007/s11046-013-9722-4.
44. Gräser Y, De Hoog S, Summerbell RC. 2006. Dermatophytes: recognizing species of clonal fungi. Med Mycol 44:199–209 http://dx.doi.org/10.1080/13693780600606810.
45. Shiraki Y, Ishibashi Y, Hiruma M, Nishikawa A, Ikeda S. 2006. Cytokine secretion profiles of human keratinocytes during Trichophyton tonsurans and Arthroderma benhamiae infections. J Med Microbiol 55:1175–1185 http://dx.doi.org/10.1099/jmm.0.46632-0.
46. Nakamura Y, Kano R, Hasegawa A, Watanabe S. 2002. Interleukin-8 and tumor necrosis factor alpha production in human epidermal keratinocytes induced by Trichophyton mentagrophytes. Clin Diagn Lab Immunol 9:935–937.
47. Tani K, Adachi M, Nakamura Y, Kano R, Makimura K, Hasegawa A, Kanda N, Watanabe S. 2007. The effect of dermatophytes on cytokine production by human keratinocytes. Arch Dermatol Res 299:381–387 http://dx.doi.org/10.1007/s00403-007-0780-7.
48. Jensen JM, Pfeiffer S, Akaki T, Schröder JM, Kleine M, Neumann C, Proksch E, Brasch J. 2007. Barrier function, epidermal differentiation, and human beta-defensin 2 expression in tinea corporis. J Invest Dermatol 127:1720–1727 http://dx.doi.org/10.1038/sj.jid.5700788.
49. López-García B, Lee PH, Gallo RL. 2006. Expression and potential function of cathelicidin antimicrobial peptides in dermatophytosis and tinea versicolor. J Antimicrob Chemother 57:877–882 http://dx.doi.org/10.1093/jac/dkl078.
50. Fritz P, Beck-Jendroschek V, Brasch J. 2012. Inhibition of dermatophytes by the antimicrobial peptides human β-defensin-2, ribonuclease 7 and psoriasin. Med Mycol 50:579–584 http://dx.doi.org/10.3109/13693786.2012.660203.
51. Hein KZ, Takahashi H, Tsumori T, Yasui Y, Nanjoh Y, Toga T, Wu Z, Grötzinger J, Jung S, Wehkamp J, Schroeder BO, Schroeder JM, Morita E. 2015. Disulphide-reduced psoriasin is a human apoptosis-inducing broad-spectrum fungicide. Proc Natl Acad Sci USA 112:13039–13044 http://dx.doi.org/10.1073/pnas.1511197112.
52. Nenoff P, Uhrlaß S, Krüger C, Erhard M, Hipler U-C, Seyfarth F, Herrmann J, Wetzig T, Schroedl W, Gräser Y. 2014. Trichophyton species of Arthroderma benhamiae - a new infectious agent in dermatology. J Dtsch Dermatol Ges 12:571–581. [PubMed]
53. da Silva BC, Paula CR, Auler ME, Ruiz LS, Dos Santos JI, Yoshioka MC, Fabris A, Castro LG, Duarte AJ, Gambale W. 2014. Dermatophytosis and immunovirological status of HIV-infected and AIDS patients from Sao Paulo city, Brazil. Mycoses 57:371–376.
54. Wu LC, Sun PL, Chang YT. 2013. Extensive deep dermatophytosis cause by Trichophyton rubrum in a patient with liver cirrhosis and chronic renal failure. Mycopathologia 176:457–462 http://dx.doi.org/10.1007/s11046-013-9696-2.
55. Lanternier F, Pathan S, Vincent QB, Liu L, Cypowyj S, Prando C, Migaud M, Taibi L, Ammar-Khodja A, Boudghene Stambouli O, Guellil B, Jacobs F, Goffard JC, Schepers K, del Marmol V, Boussofara L, Denguezli M, Larif M, Bachelez H, Michel L, Lefranc G, Hay R, Jouvion G, Chretien F, Fraitag S, Bougnoux ME, Boudia M, Abel L, Lortholary O, Casanova JL, Picard C, Grimbacher B, Puel A. 2013. Deep dermatophytosis and inherited CARD9 deficiency. N Engl J Med 369:1704–1714 http://dx.doi.org/10.1056/NEJMoa1208487.
56. Grumach AS, de Queiroz-Telles F, Migaud M, Lanternier F, Filho NR, Palma SM, Constantino-Silva RN, Casanova JL, Puel A. 2015. A homozygous CARD9 mutation in a Brazilian patient with deep dermatophytosis. J Clin Immunol 35:486–490 http://dx.doi.org/10.1007/s10875-015-0170-4.
57. Jachiet M, Lanternier F, Rybojad M, Bagot M, Ibrahim L, Casanova JL, Puel A, Bouaziz JD. 2015. Posaconazole treatment of extensive skin and nail dermatophytosis due to autosomal recessive deficiency of CARD9. JAMA Dermatol 151:192–194 http://dx.doi.org/10.1001/jamadermatol.2014.2154.
58. Cambier L, Weatherspoon A, Defaweux V, Bagut ET, Heinen MP, Antoine N, Mignon B. 2014. Assessment of the cutaneous immune response during Arthroderma benhamiae and A. vanbreuseghemii infection using an experimental mouse model. Br J Dermatol 170:625–633 http://dx.doi.org/10.1111/bjd.12673.
59. Mignon B, Tabart J, Baldo A, Mathy A, Losson B, Vermout S. 2008. Immunization and dermatophytes. Curr Opin Infect Dis 21:134–140 http://dx.doi.org/10.1097/QCO.0b013e3282f55de6.
60. Oh J, Byrd AL, Deming C, Conlan S, NISC Comparative Sequencing Program, Kong HH, Segre JA. 2014. Biogeography and individuality shape function in the human skin metagenome. Nature 514:59–64 http://dx.doi.org/10.1038/nature13786.
61. Boekhout T, Mayser P, Guého-Kellermann E, Velegraki A (ed). 2010. Malassezia and the Skin. Springer, Berlin. http://dx.doi.org/10.1007/978-3-642-03616-3
62. Porro MN, Passi S, Caprill F, Nazzaro P, Morpurgo G. 1976. Growth requirements and lipid metabolism of Pityrosporum orbiculare. J Invest Dermatol 66:178–182 http://dx.doi.org/10.1111/1523-1747.ep12481919.
63. Wang QM, Theelen B, Groenewald M, Bai FY, Boekhout T. 2014. Moniliellomycetes and Malasseziomycetes, two new classes in Ustilaginomycotina. Persoonia 33:41–47 http://dx.doi.org/10.3767/003158514X682313. [PubMed]
64. Guého-Kellermann E, Boekhout T, Begerow D. 2010. Biodiversity, phylogeny and ultrastructure, p 17–63. In Boekhout T, Mayser P, Guého-Kellermann E, Velegraki A (ed), Malassezia and the Skin. Springer Verlag, Berlin.
65. Cabañes FJ. 2014. Malassezia yeasts: how many species infect humans and animals? PLoS Pathog 10:e1003892 http://dx.doi.org/10.1371/journal.ppat.1003892.
66. Cabañes FJ, Vega S, Castellá G. 2011. Malassezia cuniculi sp. nov., a novel yeast species isolated from rabbit skin. Med Mycol 49:40–48 http://dx.doi.org/10.3109/13693786.2010.493562.
67. Guého E, Midgley G, Guillot J. 1996. The genus Malassezia with description of four new species. Antonie van Leeuwenhoek 69:337–355 http://dx.doi.org/10.1007/BF00399623.
68. Gupta AK, Boekhout T, Theelen B, Summerbell R, Batra R. 2004. Identification and typing of Malassezia species by amplified fragment length polymorphism and sequence analyses of the internal transcribed spacer and large-subunit regions of ribosomal DNA. J Clin Microbiol 42:4253–4260 http://dx.doi.org/10.1128/JCM.42.9.4253-4260.2004.
69. Guého-Kellermann E, Batra R, Boekhout T. 2011. Malassezia Baillon (1889), p 1807–1836. In Kurtzman C, Fell JW, Boekhout T (ed), The Yeasts, a Taxonomic Study, 5th ed. Elsevier, Amsterdam, The Netherlands.
70. Castellá G, Coutinho SDA, Cabañes FJ. 2014. Phylogenetic relationships of Malassezia species based on multilocus sequence analysis. Med Mycol 52:99–105. [PubMed]
71. Theelen B, Silvestri M, Guého E, van Belkum A, Boekhout T. 2001. Identification and typing of Malassezia yeasts using amplified fragment length polymorphism (AFLP), random amplified polymorphic DNA (RAPD) and denaturing gradient gel electrophoresis (DGGE). FEMS Yeast Res 1:79–86 http://dx.doi.org/10.1111/j.1567-1364.2001.tb00018.x.
72. Saunders CW, Scheynius A, Heitman J. 2012. Malassezia fungi are specialized to live on skin and associated with dandruff, eczema, and other skin diseases. PLoS Pathog 8:e1002701 http://dx.doi.org/10.1371/journal.ppat.1002701.
73. Nagata R, Nagano H, Ogishima D, Nakamura Y, Hiruma M, Sugita T. 2012. Transmission of the major skin microbiota, Malassezia, from mother to neonate. Pediatr Int 54:350–355 http://dx.doi.org/10.1111/j.1442-200X.2012.03563.x.
74. Findley K, Grice EA. 2014. The skin microbiome: a focus on pathogens and their association with skin disease. PLoS Pathog 10:e1004436 http://dx.doi.org/10.1371/journal.ppat.1004436.
75. Tanaka A, Cho O, Saito M, Tsuboi R, Kurakado S, Sugita T. 2014. Molecular characterization of the skin fungal microbiota in patients with seborrheic dermatitis. J Clin Exp Dermatol Res 5:239 http://dx.doi.org/10.4172/2155-9554.1000239.
76. Clavaud C, Jourdain R, Bar-Hen A, Tichit M, Bouchier C, Pouradier F, El Rawadi C, Guillot J, Ménard-Szczebara F, Breton L, Latgé JP, Mouyna I. 2013. Dandruff is associated with disequilibrium in the proportion of the major bacterial and fungal populations colonizing the scalp. PLoS One 8:e58203 http://dx.doi.org/10.1371/journal.pone.0058203.
77. DeAngelis YM, Gemmer CM, Kaczvinsky JR, Kenneally DC, Schwartz JR, Dawson TL Jr. 2005. Three etiologic facets of dandruff and seborrheic dermatitis: Malassezia fungi, sebaceous lipids, and individual sensitivity. J Investig Dermatol Symp Proc 10:295–297 http://dx.doi.org/10.1111/j.1087-0024.2005.10119.x.
78. Gemmer CM, DeAngelis YM, Theelen B, Boekhout T, Dawson TL Jr. 2002. Fast, noninvasive method for molecular detection and differentiation of Malassezia yeast species on human skin and application of the method to dandruff microbiology. J Clin Microbiol 40:3350–3357 http://dx.doi.org/10.1128/JCM.40.9.3350-3357.2002.
79. Sugita T, Takashima M, Kodama M, Tsuboi R, Nishikawa A. 2003. Description of a new yeast species, Malassezia japonica, and its detection in patients with atopic dermatitis and healthy subjects. J Clin Microbiol 41:4695–4699 http://dx.doi.org/10.1128/JCM.41.10.4695-4699.2003.
80. Crespo Erchiga V, Ojeda Martos A, Vera Casaño A, Crespo Erchiga A, Sanchez Fajardo F. 2000. Malassezia globosa as the causative agent of pityriasis versicolor. Br J Dermatol 143:799–803 http://dx.doi.org/10.1046/j.1365-2133.2000.03779.x.
81. Sugita T, Tajima M, Tsubuku H, Tsuboi R, Nishikawa A. 2006. Quantitative analysis of cutaneous malassezia in atopic dermatitis patients using real-time PCR. Microbiol Immunol 50:549–552 http://dx.doi.org/10.1111/j.1348-0421.2006.tb03825.x.
82. Oh BH, Song YC, Lee YW, Choe YB, Ahn KJ. 2009. Comparison of nested PCR and RFLP for identification and classification of Malassezia yeasts from healthy human skin. Ann Dermatol 21:352–357 http://dx.doi.org/10.5021/ad.2009.21.4.352.
83. Gioti A, Nystedt B, Li W, Xu J, Andersson A, Averette AF, Münch K, Wang X, Kappauf C, Kingsbury JM, Kraak B, Walker LA, Johansson HJ, Holm T, Lehtiö J, Stajich JE, Mieczkowski P, Kahmann R, Kennell JC, Cardenas ME, Lundeberg J, Saunders CW, Boekhout T, Dawson TL, Munro CA, de Groot PWJ, Butler G, Heitman J, Scheynius A. 2013. Genomic insights into the atopic eczema-associated skin commensal yeast Malassezia sympodialis. MBio 4:e00572-12 http://dx.doi.org/10.1128/mBio.00572-12.
84. Simmons RB. 1990. A new species of Malassezia. Mycol Res 94:1146–1149 http://dx.doi.org/10.1016/S0953-7562(09)81349-X.
85. Jagielski T, Rup E, Ziółkowska A, Roeske K, Macura AB, Bielecki J. 2014. Distribution of Malassezia species on the skin of patients with atopic dermatitis, psoriasis, and healthy volunteers assessed by conventional and molecular identification methods. BMC Dermatol 14:3 http://dx.doi.org/10.1186/1471-5945-14-3.
86. Cabañes FJ, Theelen B, Castellá G, Boekhout T. 2007. Two new lipid-dependent Malassezia species from domestic animals. FEMS Yeast Res 7:1064–1076 http://dx.doi.org/10.1111/j.1567-1364.2007.00217.x.
87. Boekhout T, Bosboom RW. 1994. Karyotyping of Malassezia yeasts: taxonomic and epidemiological implications. Syst Appl Microbiol 17:146–153 http://dx.doi.org/10.1016/S0723-2020(11)80043-3.
88. Iatta R, Cafarchia C, Cuna T, Montagna O, Laforgia N, Gentile O, Rizzo A, Boekhout T, Otranto D, Montagna MT. 2014. Bloodstream infections by Malassezia and Candida species in critical care patients. Med Mycol 52:264–269 http://dx.doi.org/10.1093/mmy/myt004.
89. Jung WH, Croll D, Cho JH, Kim YR, Lee YW. 2015. Analysis of the nasal vestibule mycobiome in patients with allergic rhinitis. Mycoses 58:167–172 http://dx.doi.org/10.1111/myc.12296.
90. Velegraki A, Cafarchia C, Gaitanis G, Iatta R, Boekhout T. 2015. Malassezia infections in humans and animals: pathophysiology, detection, and treatment. PLoS Pathog 11:e1004523 http://dx.doi.org/10.1371/journal.ppat.1004523.
91. Cleland EJ, Bassiouni A, Boase S, Dowd S, Vreugde S, Wormald PJ. 2014. The fungal microbiome in chronic rhinosinusitis: richness, diversity, postoperative changes and patient outcomes. Int Forum Allergy Rhinol 4:259–265 (Erratum, 5:92.) http://dx.doi.org/10.1002/alr.21297.
92. Suhr MJ, Banjara N, Hallen-Adams HE. 2016. Sequence-based methods for detecting and evaluating the human gut mycobiome. Lett Appl Microbiol 62:209–215 http://dx.doi.org/10.1111/lam.12539.
93. Gouba N, Raoult D, Drancourt M. 2014. Eukaryote culturomics of the gut reveals new species. PLoS One 9:e106994 http://dx.doi.org/10.1371/journal.pone.0106994.
94. Willger SD, Grim SL, Dolben EL, Shipunova A, Hampton TH, Morrison HG, Filkins LM, O’Toole GA, Moulton LA, Ashare A, Sogin ML, Hogan DA. 2014. Characterization and quantification of the fungal microbiome in serial samples from individuals with cystic fibrosis. Microbiome 2:40 http://dx.doi.org/10.1186/2049-2618-2-40.
95. Dupuy AK, David MS, Li L, Heider TN, Peterson JD, Montano EA, Dongari-Bagtzoglou A, Diaz PI, Strausbaugh LD. 2014. Redefining the human oral mycobiome with improved practices in amplicon-based taxonomy: discovery of Malassezia as a prominent commensal. PLoS One 9:e90899 http://dx.doi.org/10.1371/journal.pone.0090899.
96. Xu H, Dongari-Bagtzoglou A. 2015. Shaping the oral mycobiota: interactions of opportunistic fungi with oral bacteria and the host. Curr Opin Microbiol 26:65–70 http://dx.doi.org/10.1016/j.mib.2015.06.002.
97. van Woerden HC, Gregory C, Brown R, Marchesi JR, Hoogendoorn B, Matthews IP. 2013. Differences in fungi present in induced sputum samples from asthma patients and non-atopic controls: a community based case control study. BMC Infect Dis 13:69 http://dx.doi.org/10.1186/1471-2334-13-69.
98. Chryssanthou E, Broberger U, Petrini B. 2001. Malassezia pachydermatis fungaemia in a neonatal intensive care unit. Acta Paediatr 90:323–327 http://dx.doi.org/10.1080/080352501300067712.
99. Chang HJ, Miller HL, Watkins N, Arduino MJ, Ashford DA, Midgley G, Aguero SM, Pinto-Powell R, von Reyn CF, Edwards W, McNeil MM, Jarvis WR, Pruitt R. 1998. An epidemic of Malassezia pachydermatis in an intensive care nursery associated with colonization of health care workers’ pet dogs. N Engl J Med 338:706–711 http://dx.doi.org/10.1056/NEJM199803123381102.
100. Amend A. 2014. From dandruff to deep-sea vents: malassezia-like fungi are ecologically hyper-diverse. PLoS Pathog 10:e1004277 http://dx.doi.org/10.1371/journal.ppat.1004277.
101. Guillot J, Guého E, Chévrier G, Chermette R. 1997. Epidemiological analysis of Malassezia pachydermatis isolates by partial sequencing of the large subunit ribosomal RNA. Res Vet Sci 62:22–25 http://dx.doi.org/10.1016/S0034-5288(97)90174-0.
102. Hirai A, Kano R, Makimura K, Duarte ER, Hamdan JS, Lachance MA, Yamaguchi H, Hasegawa A. 2004. Malassezia nana sp. nov., a novel lipid-dependent yeast species isolated from animals. Int J Syst Evol Microbiol 54:623–627 http://dx.doi.org/10.1099/ijs.0.02776-0.
103. Sugita T, Boekhout T, Velegraki A, Guillot J, Hadina S, Cabañes FJ. 2010. Epidemiology of Malassezia-related skin infections, p 65–119. In Boekhout T, Mayser P, Guého-Kellermann E, Velegraki A (ed), Malassezia and the Skin. Springer, Berlin. http://dx.doi.org/10.1007/978-3-642-03616-3_3
104. Duarte ER, Resende JC, Rosa CA, Hamdan JS. 2001. Prevalence of yeasts and mycelial fungi in bovine parasitic otitis in the State of Minas Gerais, Brazil. J Vet Med B Infect Dis Vet Public Health 48:631–635 http://dx.doi.org/10.1046/j.1439-0450.2001.00474.x.
105. Renker C, Alphei J, Buscot F. 2003. Soil nematodes associated with the mammal pathogenic fungal genus Malassezia ( Basidiomycota: Ustilaginomycetes) in Central European forests. Biol Fertil Soils 37:70–72. doi:10.1007/s00374-002-0556-3
106. Fell JW, Scorzetti G, Connell L, Craig S. 2006. Biodiversity of micro-eukaryotes in Antarctic Dry Valley soils with <5% soil moisture. Soil Biol Biochem 38:3107–3119 http://dx.doi.org/10.1016/j.soilbio.2006.01.014.
107. Mayser P, Gaitanis G. 2010. Physiology and biochemistry, p 121–137. In Boekhout T, Guého E, Mayser P, Velegraki A (ed), Malassezia and the Skin. Springer, Berlin. http://dx.doi.org/10.1007/978-3-642-03616-3_4
108. Mexia N, Gaitanis G, Velegraki A, Soshilov A, Denison MS, Magiatis P. 2015. Pityriazepin and other potent AhR ligands isolated from Malassezia furfur yeast. Arch Biochem Biophys 571:16–20 http://dx.doi.org/10.1016/j.abb.2015.02.023.
109. Zuther K, Mayser P, Hettwer U, Wu W, Spiteller P, Kindler BL, Karlovsky P, Basse CW, Schirawski J. 2008. The tryptophan aminotransferase Tam1 catalyses the single biosynthetic step for tryptophan-dependent pigment synthesis in Ustilago maydis. Mol Microbiol 68:152–172 http://dx.doi.org/10.1111/j.1365-2958.2008.06144.x.
110. Hort W, Lang S, Brunke S, Mayser P, Hube B. 2009. Analysis of differentially expressed genes associated with tryptophan-dependent pigment synthesis in M. furfur by cDNA subtraction technology. Med Mycol 47:248–258 http://dx.doi.org/10.1080/13693780802238842.
111. Lang SK, Hort W, Mayser P. 2011. Differentially expressed genes associated with tryptophan-dependent pigment synthesis in Malassezia furfur--a comparison with the recently published genome of Malassezia globosa. Mycoses 54:e69–e83 http://dx.doi.org/10.1111/j.1439-0507.2009.01848.x.
112. Preuss J, Hort W, Lang S, Netsch A, Rahlfs S, Lochnit G, Jortzik E, Becker K, Mayser PA. 2013. Characterization of tryptophan aminotransferase 1 of Malassezia furfur, the key enzyme in the production of indolic compounds by M. furfur. Exp Dermatol 22:736–741 http://dx.doi.org/10.1111/exd.12260.
113. Mayser P, Rieche I. 2009. Rapid reversal of hyperpigmentation in pityriasis versicolor upon short-term topical cycloserine application. Mycoses 52:541–543 http://dx.doi.org/10.1111/j.1439-0507.2009.01784.x.
114. Reed WB, Pidgeon J, Becker SW. 1961. Patients with spinal cord injury. Clinical cutaneous studies. Arch Dermatol 83:379–385 http://dx.doi.org/10.1001/archderm.1961.01580090029002.
115. Barchmann T, Hort W, Krämer HJ, Mayser P. 2011. Glycine as a regulator of tryptophan-dependent pigment synthesis in Malassezia furfur. Mycoses 54:17–22 http://dx.doi.org/10.1111/j.1439-0507.2009.01758.x.
116. Liappis N, Kelderbacher SD, Kesseler K, Bantzer P. 1979. Quantitative study of free amino acids in human eccrine sweat excreted from the forearms of healthy trained and untrained men during exercise. Eur J Appl Physiol Occup Physiol 42:227–234 http://dx.doi.org/10.1007/BF00423292.
117. Ro BI, Dawson TL. 2005. The role of sebaceous gland activity and scalp microfloral metabolism in the etiology of seborrheic dermatitis and dandruff. J Investig Dermatol Symp Proc 10:194–197 http://dx.doi.org/10.1111/j.1087-0024.2005.10104.x.
118. Wisecaver JH, Alexander WG, King SB, Hittinger CT, Rokas A. 2016. Dynamic evolution of nitric oxide detoxifying flavohemoglobins, a family of single-protein metabolic modules in bacteria and eukaryotes. Mol Biol Evol 33:1979–1987 http://dx.doi.org/10.1093/molbev/msw073.
119. Zhu Y, et al. 2017. Proteogenomics produces comprehensive and highly accurate protein-coding gene annotation in a complete genome assembly of Malassezia sympodialis. Nucleic Acids Res 45:2629–2643. doi:10.1093/nar/gkx006.
120. Xu J, Saunders CW, Hu P, Grant RA, Boekhout T, Kuramae EE, Kronstad JW, Deangelis YM, Reeder NL, Johnstone KR, Leland M, Fieno AM, Begley WM, Sun Y, Lacey MP, Chaudhary T, Keough T, Chu L, Sears R, Yuan B, Dawson TL Jr. 2007. Dandruff-associated Malassezia genomes reveal convergent and divergent virulence traits shared with plant and human fungal pathogens. Proc Natl Acad Sci USA 104:18730–18735 http://dx.doi.org/10.1073/pnas.0706756104.
121. Ianiri G, Averette AF, Kingsbury JM, Heitman J, Idnurm A. 2016. Gene function analysis in the ubiquitous human commensal and pathogen Malassezia genus. MBio 7:e01853-16 http://dx.doi.org/10.1128/mBio.01853-16.
122. Celis AM, Vos AM, Triana S, Medina CA, Escobar N, Restrepo S, Wösten HA, de Cock H. 2017. Highly efficient transformation system for Malassezia furfur and Malassezia pachydermatis using Agrobacterium tumefaciens-mediated transformation. J Microbiol Methods 134:1–6 http://dx.doi.org/10.1016/j.mimet.2017.01.001.
123. Coelho MA, Sampaio JP, Gonçalves P. 2010. A deviation from the bipolar-tetrapolar mating paradigm in an early diverged basidiomycete. PLoS Genet 6:e1001052 http://dx.doi.org/10.1371/journal.pgen.1001052.
124. Nielsen K, Heitman J. 2007. Sex and virulence of human pathogenic fungi, p 143–173. In Dunlap JC (ed), Advances in Genetics. Fungal Genomics. Academic Press, Cambridge, MA http://dx.doi.org/10.1016/S0065-2660(06)57004-X
125. Heitman J, Carter DA, Dyer PS, Soll DR. 2014. Sexual reproduction of human fungal pathogens. Cold Spring Harb Perspect Med 4:a019281 http://dx.doi.org/10.1101/cshperspect.a019281.
126. Kesavan S, Holland KT, Ingham E. 2000. The effects of lipid extraction on the immunomodulatory activity of Malassezia species in vitro. Med Mycol 38:239–247 http://dx.doi.org/10.1080/mmy.
127. Buentke E, D’Amato M, Scheynius A. 2004. Malassezia enhances natural killer cell-induced dendritic cell maturation. Scand J Immunol 59:511–516 http://dx.doi.org/10.1111/j.0300-9475.2004.01416.x.
128. Johansson C, Tengvall Linder M, Aalberse RC, Scheynius A. 2004. Elevated levels of IgG and IgG4 to Malassezia allergens in atopic eczema patients with IgE reactivity to Malassezia. Int Arch Allergy Immunol 135:93–100 http://dx.doi.org/10.1159/000080651.
129. Scheynius A, Johansson C, Buentke E, Zargari A, Linder MT. 2002. Atopic eczema/dermatitis syndrome and Malassezia. Int Arch Allergy Immunol 127:161–169 http://dx.doi.org/10.1159/000053860.
130. Kato H, Sugita T, Ishibashi Y, Nishikawa A. 2006. Detection and quantification of specific IgE antibodies against eight Malassezia species in sera of patients with atopic dermatitis by using an enzyme-linked immunosorbent assay. Microbiol Immunol 50:851–856 http://dx.doi.org/10.1111/j.1348-0421.2006.tb03860.x.

Article metrics loading...



Humans are exceptional among vertebrates in that their living tissue is directly exposed to the outside world. In the absence of protective scales, feathers, or fur, the skin has to be highly effective in defending the organism against the gamut of opportunistic fungi surrounding us. Most (sub)cutaneous infections enter the body by implantation through the skin barrier. On intact skin, two types of fungal expansion are noted: (A) colonization by commensals, i.e., growth enabled by conditions prevailing on the skin surface without degradation of tissue, and (B) infection by superficial pathogens that assimilate epidermal keratin and interact with the cellular immune system. In a response-damage framework, all fungi are potentially able to cause disease, as a balance between their natural predilection and the immune status of the host. For this reason, we will not attribute a fixed ecological term to each species, but rather describe them as growing in a commensal state (A) or in a pathogenic state (B).

Highlighted Text: Show | Hide
Loading full text...

Full text loading...



Image of FIGURE 1

Click to view


Overview of basic types of fungal occurrence on human skin and modes of transmission.

Source: microbiolspec July 2017 vol. 5 no. 4 doi:10.1128/microbiolspec.FUNK-0049-2016
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 2

Click to view


Maximum likelihood phylogenetic tree (RAxML v.8.0.0) based on ITS and partial LSU, TUB, and 60S L10 sequences of species using GTRCAT as model, with 1,000 bootstrap replications, shown as collapsed when bootstrap values >70%. was selected as outgroup. Reprinted from de Hoog et al. ( 13 ).

Source: microbiolspec July 2017 vol. 5 no. 4 doi:10.1128/microbiolspec.FUNK-0049-2016
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 3

Click to view


species tree was constructed using concatenated sequences of 164 core eukaryotic genes that are present in all , , and genomes. Sequences were aligned using MUSCLE and the phylogeny constructed using a maximum likelihood (ML) approach by RAxML. RAxML was run using “–f a –m PROTGAMMAJTT” with 400 bootstraps.

Source: microbiolspec July 2017 vol. 5 no. 4 doi:10.1128/microbiolspec.FUNK-0049-2016
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 4

Click to view


Synthesis of indole-derived pigments by one enzymatic step (TAM1) and possible intervention by TAM inhibitors.

Source: microbiolspec July 2017 vol. 5 no. 4 doi:10.1128/microbiolspec.FUNK-0049-2016
Permissions and Reprints Request Permissions
Download as Powerpoint


Generic image for table

Click to view


Selected Trp-derived indole compounds and their potential relationship to clinical phenomena in PV

Source: microbiolspec July 2017 vol. 5 no. 4 doi:10.1128/microbiolspec.FUNK-0049-2016
Generic image for table

Click to view


genome statistics

Source: microbiolspec July 2017 vol. 5 no. 4 doi:10.1128/microbiolspec.FUNK-0049-2016

Supplemental Material

No supplementary material available for this content.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error