Genomic insights into the atopic eczema-associated skin commensal yeast Malassezia sympodialis

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 Walker, Henrik J Johansson, Tina Holm, Janne Lehtiö, Jason E Stajich, Piotr Mieczkowski, Regine Kahmann, John C Kennell, Maria E Cardenas & 9 others 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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Abstract

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.
Original languageEnglish
Article numbere00572-12
Number of pages16
JournalmBio
Volume4
Issue number1
DOIs
Publication statusPublished - 22 Jan 2013

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Malassezia
Atopic Dermatitis
Dandruff
Yeasts
Skin
Genome
Allergens
Reproduction
Proteins
Fungi
Cell Wall
Genes
Cyclophilin A
Lipids
Fatty Acid Synthases
Glycosylphosphatidylinositols
Basidiomycota
Cryptococcus neoformans
Meiosis
Biofilms

Cite this

Gioti, A., Nystedt, B., Li, W., Xu, J., Andersson, A., Averette, A. F., ... Scheynius, A. (2013). Genomic insights into the atopic eczema-associated skin commensal yeast Malassezia sympodialis. mBio, 4(1), [e00572-12]. https://doi.org/10.1128/mBio.00572-12

Genomic insights into the atopic eczema-associated skin commensal yeast Malassezia sympodialis. / Gioti, Anastasia; Nystedt, Björn; Li, Wenjun; Xu, Jun; Andersson, Anna; Averette, Anna F; Münch, Karin; Wang, Xuying; Kappauf, Catharine; Kingsbury, Joanne M; Kraak, Bart; Walker, Louise; Johansson, Henrik J; Holm, Tina; Lehtiö, Janne; Stajich, Jason E; Mieczkowski, Piotr; Kahmann, Regine; Kennell, John C; Cardenas, Maria E; Lundeberg, Joakim; Saunders, Charles W; Boekhout, Teun; Dawson, Thomas L; Munro, Carol A; de Groot, Piet W J; Butler, Geraldine; Heitman, Joseph; Scheynius, Annika.

In: mBio, Vol. 4, No. 1, e00572-12, 22.01.2013.

Research output: Contribution to journalArticle

Gioti, A, Nystedt, B, Li, W, Xu, J, Andersson, A, Averette, AF, Münch, K, Wang, X, Kappauf, C, Kingsbury, JM, Kraak, B, Walker, L, 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, vol. 4, no. 1, e00572-12. https://doi.org/10.1128/mBio.00572-12
Gioti A, Nystedt B, Li W, Xu J, Andersson A, Averette AF et al. Genomic insights into the atopic eczema-associated skin commensal yeast Malassezia sympodialis. mBio. 2013 Jan 22;4(1). e00572-12. https://doi.org/10.1128/mBio.00572-12
Gioti, Anastasia ; Nystedt, Björn ; Li, Wenjun ; Xu, Jun ; Andersson, Anna ; Averette, Anna F ; Münch, Karin ; Wang, Xuying ; Kappauf, Catharine ; Kingsbury, Joanne M ; Kraak, Bart ; Walker, Louise ; Johansson, Henrik J ; Holm, Tina ; Lehtiö, Janne ; Stajich, Jason E ; Mieczkowski, Piotr ; Kahmann, Regine ; Kennell, John C ; Cardenas, Maria E ; Lundeberg, Joakim ; Saunders, Charles W ; Boekhout, Teun ; Dawson, Thomas L ; Munro, Carol A ; de Groot, Piet W J ; Butler, Geraldine ; Heitman, Joseph ; Scheynius, Annika. / Genomic insights into the atopic eczema-associated skin commensal yeast Malassezia sympodialis. In: mBio. 2013 ; Vol. 4, No. 1.
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title = "Genomic insights into the atopic eczema-associated skin commensal yeast Malassezia sympodialis",
abstract = "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.",
author = "Anastasia Gioti and Bj{\"o}rn Nystedt and Wenjun Li and Jun Xu and Anna Andersson and Averette, {Anna F} and Karin M{\"u}nch and Xuying Wang and Catharine Kappauf and Kingsbury, {Joanne M} and Bart Kraak and Louise Walker and Johansson, {Henrik J} and Tina Holm and Janne Lehti{\"o} and Stajich, {Jason E} and Piotr Mieczkowski and Regine Kahmann and Kennell, {John C} and Cardenas, {Maria E} and Joakim Lundeberg and Saunders, {Charles W} and Teun Boekhout and Dawson, {Thomas L} and Munro, {Carol A} and {de Groot}, {Piet W J} and Geraldine Butler and Joseph Heitman and Annika Scheynius",
note = "ACKNOWLEDGMENTS This work was supported by the Swedish Research Council, the Center for Allergy Research Karolinska Institutet, the Cancer and Allergy Association, through the regional agreement on medical training and clinical research (ALF) between Stockholm County Council and the Karolinska Institutet, and by funds from Procter and Gamble and R01 grant AI50113 and R37 grant AI39115 from the NIH/NIAID to J.H. We acknowledge Science for Life Laboratory, Swedish National Infrastructure for large-Scale DNA Sequencing (SNISS), and the Uppsala Multidisciplinary Center for Advanced Computational Science (UPPMAX) for providing massive parallel sequencing and computational infrastructure. We are also grateful for the computational resources made available through the University of California, Riverside Bioinformatics Core in the Institute for Integrative Genome Biology.",
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T1 - Genomic insights into the atopic eczema-associated skin commensal yeast Malassezia sympodialis

AU - Gioti, Anastasia

AU - Nystedt, Björn

AU - Li, Wenjun

AU - Xu, Jun

AU - Andersson, Anna

AU - Averette, Anna F

AU - Münch, Karin

AU - Wang, Xuying

AU - Kappauf, Catharine

AU - Kingsbury, Joanne M

AU - Kraak, Bart

AU - Walker, Louise

AU - Johansson, Henrik J

AU - Holm, Tina

AU - Lehtiö, Janne

AU - Stajich, Jason E

AU - Mieczkowski, Piotr

AU - Kahmann, Regine

AU - Kennell, John C

AU - Cardenas, Maria E

AU - Lundeberg, Joakim

AU - Saunders, Charles W

AU - Boekhout, Teun

AU - Dawson, Thomas L

AU - Munro, Carol A

AU - de Groot, Piet W J

AU - Butler, Geraldine

AU - Heitman, Joseph

AU - Scheynius, Annika

N1 - ACKNOWLEDGMENTS This work was supported by the Swedish Research Council, the Center for Allergy Research Karolinska Institutet, the Cancer and Allergy Association, through the regional agreement on medical training and clinical research (ALF) between Stockholm County Council and the Karolinska Institutet, and by funds from Procter and Gamble and R01 grant AI50113 and R37 grant AI39115 from the NIH/NIAID to J.H. We acknowledge Science for Life Laboratory, Swedish National Infrastructure for large-Scale DNA Sequencing (SNISS), and the Uppsala Multidisciplinary Center for Advanced Computational Science (UPPMAX) for providing massive parallel sequencing and computational infrastructure. We are also grateful for the computational resources made available through the University of California, Riverside Bioinformatics Core in the Institute for Integrative Genome Biology.

PY - 2013/1/22

Y1 - 2013/1/22

N2 - 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.

AB - 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.

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