Genomic Insights into the Atopic Eczema-Associated Skin Commensal Yeast <italic toggle="yes">Malassezia sympodialis</italic>

ABSTRACT Malassezia commensal yeasts are associated with a number of skin disorders, such as atopic eczema/dermatitis and dandruff, and they also can cause systemic infections. Here we describe the 7.67-Mbp genome of Malassezia sympodialis, a species associated with atopic eczema, and contrast its g...

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Autores principales: Anastasia Gioti, Björn Nystedt, Wenjun Li, Jun Xu, Anna Andersson, Anna F. Averette, Karin Münch, Xuying Wang, Catharine Kappauf, Joanne M. Kingsbury, Bart Kraak, Louise A. Walker, Henrik J. Johansson, Tina Holm, Janne Lehtiö, Jason E. Stajich, Piotr Mieczkowski, Regine Kahmann, John C. Kennell, Maria E. Cardenas, Joakim Lundeberg, Charles W. Saunders, Teun Boekhout, Thomas L. Dawson, Carol A. Munro, Piet W. J. de Groot, Geraldine Butler, Joseph Heitman, Annika Scheynius
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Publicado: American Society for Microbiology 2013
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spelling oai:doaj.org-article:aee49ae1daf24291ac42a63f4afcf0972021-11-15T15:40:22ZGenomic Insights into the Atopic Eczema-Associated Skin Commensal Yeast <italic toggle="yes">Malassezia sympodialis</italic>10.1128/mBio.00572-122150-7511https://doaj.org/article/aee49ae1daf24291ac42a63f4afcf0972013-03-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00572-12https://doaj.org/toc/2150-7511ABSTRACT Malassezia commensal yeasts are associated with a number of skin disorders, such as atopic eczema/dermatitis and dandruff, and they also can cause systemic infections. Here we describe the 7.67-Mbp genome of Malassezia sympodialis, a species associated with atopic eczema, and contrast its genome repertoire with that of Malassezia globosa, associated with dandruff, as well as those of other closely related fungi. Ninety percent of the predicted M. sympodialis protein coding genes were experimentally verified by mass spectrometry at the protein level. We identified a relatively limited number of genes related to lipid biosynthesis, and both species lack the fatty acid synthase gene, in line with the known requirement of these yeasts to assimilate lipids from the host. Malassezia species do not appear to have many cell wall-localized glycosylphosphatidylinositol (GPI) proteins and lack other cell wall proteins previously identified in other fungi. This is surprising given that in other fungi these proteins have been shown to mediate interactions (e.g., adhesion and biofilm formation) with the host. The genome revealed a complex evolutionary history for an allergen of unknown function, Mala s 7, shown to be encoded by a member of an amplified gene family of secreted proteins. Based on genetic and biochemical studies with the basidiomycete human fungal pathogen Cryptococcus neoformans, we characterized the allergen Mala s 6 as the cytoplasmic cyclophilin A. We further present evidence that M. sympodialis may have the capacity to undergo sexual reproduction and present a model for a pseudobipolar mating system that allows limited recombination between two linked MAT loci. IMPORTANCE Malassezia commensal yeasts are associated with a number of skin disorders. The previously published genome of M. globosa provided some of the first insights into Malassezia biology and its involvement in dandruff. Here, we present the genome of M. sympodialis, frequently isolated from patients with atopic eczema and healthy individuals. We combined comparative genomics with sequencing and functional characterization of specific genes in a population of clinical isolates and in closely related model systems. Our analyses provide insights into the evolution of allergens related to atopic eczema and the evolutionary trajectory of the machinery for sexual reproduction and meiosis. We hypothesize that M. sympodialis may undergo sexual reproduction, which has important implications for the understanding of the life cycle and virulence potential of this medically important yeast. Our findings provide a foundation for the development of genetic and genomic tools to elucidate host-microbe interactions that occur on the skin and to identify potential therapeutic targets.Anastasia GiotiBjörn NystedtWenjun LiJun XuAnna AnderssonAnna F. AveretteKarin MünchXuying WangCatharine KappaufJoanne M. KingsburyBart KraakLouise A. WalkerHenrik J. JohanssonTina HolmJanne LehtiöJason E. StajichPiotr MieczkowskiRegine KahmannJohn C. KennellMaria E. CardenasJoakim LundebergCharles W. SaundersTeun BoekhoutThomas L. DawsonCarol A. MunroPiet W. J. de GrootGeraldine ButlerJoseph HeitmanAnnika ScheyniusAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 4, Iss 1 (2013)
institution DOAJ
collection DOAJ
language EN
topic Microbiology
QR1-502
spellingShingle Microbiology
QR1-502
Anastasia Gioti
Björn Nystedt
Wenjun Li
Jun Xu
Anna Andersson
Anna F. Averette
Karin Münch
Xuying Wang
Catharine Kappauf
Joanne M. Kingsbury
Bart Kraak
Louise A. Walker
Henrik J. Johansson
Tina Holm
Janne Lehtiö
Jason E. Stajich
Piotr Mieczkowski
Regine Kahmann
John C. Kennell
Maria E. Cardenas
Joakim Lundeberg
Charles W. Saunders
Teun Boekhout
Thomas L. Dawson
Carol A. Munro
Piet W. J. de Groot
Geraldine Butler
Joseph Heitman
Annika Scheynius
Genomic Insights into the Atopic Eczema-Associated Skin Commensal Yeast <italic toggle="yes">Malassezia sympodialis</italic>
description ABSTRACT Malassezia commensal yeasts are associated with a number of skin disorders, such as atopic eczema/dermatitis and dandruff, and they also can cause systemic infections. Here we describe the 7.67-Mbp genome of Malassezia sympodialis, a species associated with atopic eczema, and contrast its genome repertoire with that of Malassezia globosa, associated with dandruff, as well as those of other closely related fungi. Ninety percent of the predicted M. sympodialis protein coding genes were experimentally verified by mass spectrometry at the protein level. We identified a relatively limited number of genes related to lipid biosynthesis, and both species lack the fatty acid synthase gene, in line with the known requirement of these yeasts to assimilate lipids from the host. Malassezia species do not appear to have many cell wall-localized glycosylphosphatidylinositol (GPI) proteins and lack other cell wall proteins previously identified in other fungi. This is surprising given that in other fungi these proteins have been shown to mediate interactions (e.g., adhesion and biofilm formation) with the host. The genome revealed a complex evolutionary history for an allergen of unknown function, Mala s 7, shown to be encoded by a member of an amplified gene family of secreted proteins. Based on genetic and biochemical studies with the basidiomycete human fungal pathogen Cryptococcus neoformans, we characterized the allergen Mala s 6 as the cytoplasmic cyclophilin A. We further present evidence that M. sympodialis may have the capacity to undergo sexual reproduction and present a model for a pseudobipolar mating system that allows limited recombination between two linked MAT loci. IMPORTANCE Malassezia commensal yeasts are associated with a number of skin disorders. The previously published genome of M. globosa provided some of the first insights into Malassezia biology and its involvement in dandruff. Here, we present the genome of M. sympodialis, frequently isolated from patients with atopic eczema and healthy individuals. We combined comparative genomics with sequencing and functional characterization of specific genes in a population of clinical isolates and in closely related model systems. Our analyses provide insights into the evolution of allergens related to atopic eczema and the evolutionary trajectory of the machinery for sexual reproduction and meiosis. We hypothesize that M. sympodialis may undergo sexual reproduction, which has important implications for the understanding of the life cycle and virulence potential of this medically important yeast. Our findings provide a foundation for the development of genetic and genomic tools to elucidate host-microbe interactions that occur on the skin and to identify potential therapeutic targets.
format article
author Anastasia Gioti
Björn Nystedt
Wenjun Li
Jun Xu
Anna Andersson
Anna F. Averette
Karin Münch
Xuying Wang
Catharine Kappauf
Joanne M. Kingsbury
Bart Kraak
Louise A. Walker
Henrik J. Johansson
Tina Holm
Janne Lehtiö
Jason E. Stajich
Piotr Mieczkowski
Regine Kahmann
John C. Kennell
Maria E. Cardenas
Joakim Lundeberg
Charles W. Saunders
Teun Boekhout
Thomas L. Dawson
Carol A. Munro
Piet W. J. de Groot
Geraldine Butler
Joseph Heitman
Annika Scheynius
author_facet Anastasia Gioti
Björn Nystedt
Wenjun Li
Jun Xu
Anna Andersson
Anna F. Averette
Karin Münch
Xuying Wang
Catharine Kappauf
Joanne M. Kingsbury
Bart Kraak
Louise A. Walker
Henrik J. Johansson
Tina Holm
Janne Lehtiö
Jason E. Stajich
Piotr Mieczkowski
Regine Kahmann
John C. Kennell
Maria E. Cardenas
Joakim Lundeberg
Charles W. Saunders
Teun Boekhout
Thomas L. Dawson
Carol A. Munro
Piet W. J. de Groot
Geraldine Butler
Joseph Heitman
Annika Scheynius
author_sort Anastasia Gioti
title Genomic Insights into the Atopic Eczema-Associated Skin Commensal Yeast <italic toggle="yes">Malassezia sympodialis</italic>
title_short Genomic Insights into the Atopic Eczema-Associated Skin Commensal Yeast <italic toggle="yes">Malassezia sympodialis</italic>
title_full Genomic Insights into the Atopic Eczema-Associated Skin Commensal Yeast <italic toggle="yes">Malassezia sympodialis</italic>
title_fullStr Genomic Insights into the Atopic Eczema-Associated Skin Commensal Yeast <italic toggle="yes">Malassezia sympodialis</italic>
title_full_unstemmed Genomic Insights into the Atopic Eczema-Associated Skin Commensal Yeast <italic toggle="yes">Malassezia sympodialis</italic>
title_sort genomic insights into the atopic eczema-associated skin commensal yeast <italic toggle="yes">malassezia sympodialis</italic>
publisher American Society for Microbiology
publishDate 2013
url https://doaj.org/article/aee49ae1daf24291ac42a63f4afcf097
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