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Genus-Wide Comparative Genomics of Malassezia Delineates Its Phylogeny, Physiology, and Niche Adaptation on Human Skin.

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 - PLoS Genet. (2015)

Bottom Line: Gene family analysis revealed extensive turnover and underlined the importance of secretory lipases, phospholipases, aspartyl proteases, and other peptidases.Combining genomic analysis with a re-evaluation of culture characteristics, we establish the likely lipid-dependence of all Malassezia.Our phylogenetic analysis sheds new light on the relationship between Malassezia and other members of Ustilaginomycotina, as well as phylogenetic lineages within the genus.

View Article: PubMed Central - PubMed

Affiliation: Computational and Systems Biology, Genome Institute of Singapore, A*STAR, Singapore.

ABSTRACT
Malassezia is a unique lipophilic genus in class Malasseziomycetes in Ustilaginomycotina, (Basidiomycota, fungi) that otherwise consists almost exclusively of plant pathogens. Malassezia are typically isolated from warm-blooded animals, are dominant members of the human skin mycobiome and are associated with common skin disorders. To characterize the genetic basis of the unique phenotypes of Malassezia spp., we sequenced the genomes of all 14 accepted species and used comparative genomics against a broad panel of fungal genomes to comprehensively identify distinct features that define the Malassezia gene repertoire: gene gain and loss; selection signatures; and lineage-specific gene family expansions. Our analysis revealed key gene gain events (64) with a single gene conserved across all Malassezia but absent in all other sequenced Basidiomycota. These likely horizontally transferred genes provide intriguing gain-of-function events and prime candidates to explain the emergence of Malassezia. A larger set of genes (741) were lost, with enrichment for glycosyl hydrolases and carbohydrate metabolism, concordant with adaptation to skin's carbohydrate-deficient environment. Gene family analysis revealed extensive turnover and underlined the importance of secretory lipases, phospholipases, aspartyl proteases, and other peptidases. Combining genomic analysis with a re-evaluation of culture characteristics, we establish the likely lipid-dependence of all Malassezia. Our phylogenetic analysis sheds new light on the relationship between Malassezia and other members of Ustilaginomycotina, as well as phylogenetic lineages within the genus. Overall, our study provides a unique genomic resource for understanding Malassezia niche-specificity and potential virulence, as well as their abundance and distribution in the environment and on human skin.

No MeSH data available.


Related in: MedlinePlus

Lipid specificity and extensive turnover in the lipase gene family.A) Representative lipid assimilation assay images. Letters correspond to lipid wells (S5 Table). White letters indicate no growth, while green letters indicate growth on visual scale. B) Gene gains and losses in phosphoesterase family PF04185, where “+” indicates the number of gene gain events while “-” indicates the number of gene loss events. Shaded numbers indicate the estimated gene copy number in the most recent common ancestor and gene copy numbers in the observed species.
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pgen.1005614.g005: Lipid specificity and extensive turnover in the lipase gene family.A) Representative lipid assimilation assay images. Letters correspond to lipid wells (S5 Table). White letters indicate no growth, while green letters indicate growth on visual scale. B) Gene gains and losses in phosphoesterase family PF04185, where “+” indicates the number of gene gain events while “-” indicates the number of gene loss events. Shaded numbers indicate the estimated gene copy number in the most recent common ancestor and gene copy numbers in the observed species.

Mentions: Malassezia are known to have varying host tropism and highly specific preferences for environmental niches and food sources [3,44]. For example, some highly sebaceous sites such as scalp (including occiput) and back are typically dominated by M. globosa [11]. To further understand niche-specificity in Malassezia, we evaluated their preference for growth in various lipid media using “Lipid Assimilation Assays” (see Methods). These experiments highlight a strong specificity in Malassezia’s preference for lipids (S4 Table) that is not well correlated with their phylogenetic relatedness. For example, M. furfur and M. sympodialis are functionally similar as the most robust of the lipid-dependent species in culture, sharing the broadest range of lipids that support growth (Fig 5A, S5 Table). However, they are not closely related and are placed in different sub-clusters of the Malassezia phylogeny (Fig 3B). Also, the closely related species M. globosa and M. restricta have different lipid assimilation profiles (Fig 5A, S5 Table). To understand the genetic basis of these phenotypes, we reexamined the list of gene family expansions and selection in Malassezia. Strikingly, the most expanded gene family in Malassezia was found to be a phospholipase family, and a secretory lipase family was also among the list of 13 families with a 2-fold increase in median copy number in Malassezia compared to other fungi (S3 Table). Lipase and phospholipase activities have been detected in multiple Malassezia species [45,46]. Their genes are highly expressed in vivo on human scalp [2,45,47], and are thought to play an essential role in supporting their growth. Therefore, we hypothesized that expansion of these gene families might explain Malassezia niche-specificity. Other than lipases, many peptidases in multiple families are found in the most expanded gene families in Malassezia, underlining their importance in Malassezia biology (S3 Table, S8 Text).


Genus-Wide Comparative Genomics of Malassezia Delineates Its Phylogeny, Physiology, and Niche Adaptation on Human Skin.

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 - PLoS Genet. (2015)

Lipid specificity and extensive turnover in the lipase gene family.A) Representative lipid assimilation assay images. Letters correspond to lipid wells (S5 Table). White letters indicate no growth, while green letters indicate growth on visual scale. B) Gene gains and losses in phosphoesterase family PF04185, where “+” indicates the number of gene gain events while “-” indicates the number of gene loss events. Shaded numbers indicate the estimated gene copy number in the most recent common ancestor and gene copy numbers in the observed species.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4634964&req=5

pgen.1005614.g005: Lipid specificity and extensive turnover in the lipase gene family.A) Representative lipid assimilation assay images. Letters correspond to lipid wells (S5 Table). White letters indicate no growth, while green letters indicate growth on visual scale. B) Gene gains and losses in phosphoesterase family PF04185, where “+” indicates the number of gene gain events while “-” indicates the number of gene loss events. Shaded numbers indicate the estimated gene copy number in the most recent common ancestor and gene copy numbers in the observed species.
Mentions: Malassezia are known to have varying host tropism and highly specific preferences for environmental niches and food sources [3,44]. For example, some highly sebaceous sites such as scalp (including occiput) and back are typically dominated by M. globosa [11]. To further understand niche-specificity in Malassezia, we evaluated their preference for growth in various lipid media using “Lipid Assimilation Assays” (see Methods). These experiments highlight a strong specificity in Malassezia’s preference for lipids (S4 Table) that is not well correlated with their phylogenetic relatedness. For example, M. furfur and M. sympodialis are functionally similar as the most robust of the lipid-dependent species in culture, sharing the broadest range of lipids that support growth (Fig 5A, S5 Table). However, they are not closely related and are placed in different sub-clusters of the Malassezia phylogeny (Fig 3B). Also, the closely related species M. globosa and M. restricta have different lipid assimilation profiles (Fig 5A, S5 Table). To understand the genetic basis of these phenotypes, we reexamined the list of gene family expansions and selection in Malassezia. Strikingly, the most expanded gene family in Malassezia was found to be a phospholipase family, and a secretory lipase family was also among the list of 13 families with a 2-fold increase in median copy number in Malassezia compared to other fungi (S3 Table). Lipase and phospholipase activities have been detected in multiple Malassezia species [45,46]. Their genes are highly expressed in vivo on human scalp [2,45,47], and are thought to play an essential role in supporting their growth. Therefore, we hypothesized that expansion of these gene families might explain Malassezia niche-specificity. Other than lipases, many peptidases in multiple families are found in the most expanded gene families in Malassezia, underlining their importance in Malassezia biology (S3 Table, S8 Text).

Bottom Line: Gene family analysis revealed extensive turnover and underlined the importance of secretory lipases, phospholipases, aspartyl proteases, and other peptidases.Combining genomic analysis with a re-evaluation of culture characteristics, we establish the likely lipid-dependence of all Malassezia.Our phylogenetic analysis sheds new light on the relationship between Malassezia and other members of Ustilaginomycotina, as well as phylogenetic lineages within the genus.

View Article: PubMed Central - PubMed

Affiliation: Computational and Systems Biology, Genome Institute of Singapore, A*STAR, Singapore.

ABSTRACT
Malassezia is a unique lipophilic genus in class Malasseziomycetes in Ustilaginomycotina, (Basidiomycota, fungi) that otherwise consists almost exclusively of plant pathogens. Malassezia are typically isolated from warm-blooded animals, are dominant members of the human skin mycobiome and are associated with common skin disorders. To characterize the genetic basis of the unique phenotypes of Malassezia spp., we sequenced the genomes of all 14 accepted species and used comparative genomics against a broad panel of fungal genomes to comprehensively identify distinct features that define the Malassezia gene repertoire: gene gain and loss; selection signatures; and lineage-specific gene family expansions. Our analysis revealed key gene gain events (64) with a single gene conserved across all Malassezia but absent in all other sequenced Basidiomycota. These likely horizontally transferred genes provide intriguing gain-of-function events and prime candidates to explain the emergence of Malassezia. A larger set of genes (741) were lost, with enrichment for glycosyl hydrolases and carbohydrate metabolism, concordant with adaptation to skin's carbohydrate-deficient environment. Gene family analysis revealed extensive turnover and underlined the importance of secretory lipases, phospholipases, aspartyl proteases, and other peptidases. Combining genomic analysis with a re-evaluation of culture characteristics, we establish the likely lipid-dependence of all Malassezia. Our phylogenetic analysis sheds new light on the relationship between Malassezia and other members of Ustilaginomycotina, as well as phylogenetic lineages within the genus. Overall, our study provides a unique genomic resource for understanding Malassezia niche-specificity and potential virulence, as well as their abundance and distribution in the environment and on human skin.

No MeSH data available.


Related in: MedlinePlus