title: Genus-Wide Comparative Genomics of Malassezia Delineates Its Phylogeny, Physiology, and Niche Adaptation on Human Skin.
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.
authors.affiliation: Computational and Systems Biology, Genome Institute of Singapore, A*STAR, Singapore.
authors.forename: Guangxi
authors.initials: G
authors.lastname: Wu
authors.affiliation: Procter & Gamble Singapore Innovation Center, Singapore.
authors.forename: He
authors.initials: H
authors.lastname: Zhao
authors.affiliation: Computational and Systems Biology, Genome Institute of Singapore, A*STAR, Singapore.
authors.forename: Chenhao
authors.initials: C
authors.lastname: Li
authors.affiliation: Computational and Systems Biology, Genome Institute of Singapore, A*STAR, Singapore.
authors.forename: Menaka Priyadarsani
authors.initials: MP
authors.lastname: Rajapakse
authors.affiliation: Bioinformatics Institute, A*STAR, Singapore.
authors.forename: Wing Cheong
authors.initials: WC
authors.lastname: Wong
authors.affiliation: Procter & Gamble Mason Business Center, Mason, Ohio, United States of America.
authors.forename: Jun
authors.initials: J
authors.lastname: Xu
authors.affiliation: Procter & Gamble Mason Business Center, Mason, Ohio, United States of America.
authors.forename: Charles W
authors.initials: CW
authors.lastname: Saunders
authors.affiliation: Procter & Gamble Mason Business Center, Mason, Ohio, United States of America.
authors.forename: Nancy L
authors.initials: NL
authors.lastname: Reeder
authors.affiliation: Procter & Gamble Mason Business Center, Mason, Ohio, United States of America.
authors.forename: Raymond A
authors.initials: RA
authors.lastname: Reilman
authors.affiliation: Translational Immunology Unit, Department of Medicine Solna, Karolinska Institutet and University Hospital, Stockholm, Sweden.
authors.forename: Annika
authors.initials: A
authors.lastname: Scheynius
authors.affiliation: Duke University Medical Center, Durham, North Carolina, United States of America.
authors.forename: Sheng
authors.initials: S
authors.lastname: Sun
authors.affiliation: Duke University Medical Center, Durham, North Carolina, United States of America.
authors.forename: Blake Robert
authors.initials: BR
authors.lastname: Billmyre
authors.affiliation: National Center for Biotechnology Information, Bethesda, Maryland, United States of America.
authors.forename: Wenjun
authors.initials: W
authors.lastname: Li
authors.affiliation: Duke University Medical Center, Durham, North Carolina, United States of America.
authors.forename: Anna Floyd
authors.initials: AF
authors.lastname: Averette
authors.affiliation: University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America.
authors.forename: Piotr
authors.initials: P
authors.lastname: Mieczkowski
authors.affiliation: Duke University Medical Center, Durham, North Carolina, United States of America.
authors.forename: Joseph
authors.initials: J
authors.lastname: Heitman
authors.affiliation: Fungal Biodiversity Centre, CBS-KNAW, Utrecht, The Netherlands.
authors.forename: Bart
authors.initials: B
authors.lastname: Theelen
authors.affiliation: University College Dublin, Dublin, Ireland.
authors.forename: Markus S
authors.initials: MS
authors.lastname: Schröder
authors.affiliation: Computational and Systems Biology, Genome Institute of Singapore, A*STAR, Singapore.
authors.forename: Paola Florez
authors.initials: PF
authors.lastname: De Sessions
authors.affiliation: University College Dublin, Dublin, Ireland.
authors.forename: Geraldine
authors.initials: G
authors.lastname: Butler
authors.affiliation: Bioinformatics Institute, A*STAR, Singapore.|School of Biological Sciences, Nanyang Technological University (NTU), Singapore.
authors.forename: Sebastian
authors.initials: S
authors.lastname: Maurer-Stroh
authors.affiliation: Fungal Biodiversity Centre, CBS-KNAW, Utrecht, The Netherlands.
authors.forename: Teun
authors.initials: T
authors.lastname: Boekhout
authors.affiliation: Computational and Systems Biology, Genome Institute of Singapore, A*STAR, Singapore.
authors.forename: Niranjan
authors.initials: N
authors.lastname: Nagarajan
authors.affiliation: Institute of Medical Biology, A*STAR, Singapore.
authors.forename: Thomas L
authors.initials: TL
authors.lastname: Dawson
mesh_terms: D000222:Adaptation, Physiological; D022761:Gene Transfer, Horizontal; D005800:Genes, Fungal; D006801:Humans; D008290:Malassezia / Q000145:classification / Q000235:genetics / Q000502:physiology; D010802:Phylogeny; D012867:Skin / Q000382:microbiology*