title: Exploring the genomic diversity of black yeasts and relatives (Chaetothyriales,Ascomycota).
abstract: The orderChaetothyriales(Pezizomycotina,Ascomycetes) harbours obligatorily melanised fungi and includes numerous etiologic agents of chromoblastomycosis, phaeohyphomycosis and other diseases of vertebrate hosts. Diseases range from mild cutaneous to fatal cerebral or disseminated infections and affect humans and cold-blooded animals globally. In addition,Chaetothyrialescomprise species with aquatic, rock-inhabiting, ant-associated, and mycoparasitic life-styles, as well as species that tolerate toxic compounds, suggesting a high degree of versatile extremotolerance. To understand their biology and divergent niche occupation, we sequenced and annotated a set of 23 genomes of main the human opportunists within theChaetothyrialesas well as related environmental species. Our analyses included fungi with diverse life-styles, namely opportunistic pathogens and closely related saprobes, to identify genomic adaptations related to pathogenesis. Furthermore, ecological preferences ofChaetothyrialeswere analysed, in conjuncture with the order-level phylogeny based on conserved ribosomal genes. General characteristics, phylogenomic relationships, transposable elements, sex-related genes, protein family evolution, genes related to protein degradation (MEROPS), carbohydrate-active enzymes (CAZymes), melanin synthesis and secondary metabolism were investigated and compared between species. Genome assemblies varied from 25.81 Mb (Capronia coronata) to 43.03 Mb (Cladophialophora immunda). The bantiana-clade contained the highest number of predicted genes (12 817 on average) as well as larger genomes. We found a low content of mobile elements, with DNA transposons from Tc1/Mariner superfamily being the most abundant across analysed species. Additionally, we identified a reduction of carbohydrate degrading enzymes, specifically many of the Glycosyl Hydrolase (GH) class, while most of the Pectin Lyase (PL) genes were lost in etiological agents of chromoblastomycosis and phaeohyphomycosis. An expansion was found in protein degrading peptidase enzyme families S12 (serine-type D-Ala-D-Ala carboxypeptidases) and M38 (isoaspartyl dipeptidases). Based on genomic information, a wide range of abilities of melanin biosynthesis was revealed; genes related to metabolically distinct DHN, DOPA and pyomelanin pathways were identified. TheMAT(MAtingType) locus and other sex-related genes were recognized in all 23 black fungi. Members of the asexual generaFonsecaeaandCladophialophoraappear to be heterothallic with a single copy of eitherMAT-1-1orMAT-1-2in each individual. AllCaproniaspecies are homothallic as bothMAT1-1andMAT1-2genes were found in each single genome. The genomic synteny of theMAT-locus flanking genes (SLA2-APN2-COX13) is not conserved in black fungi as is commonly observed inEurotiomycetes, indicating a unique genomic context forMATin those species. The heterokaryon (het) genes expansion associated with the low selective pressure at theMAT-locus suggests that a parasexual cycle may play an important role in generating diversity among those fungi.
authors.affiliation: Division of Pathogen Genomics, Translational Genomics Research Institute (TGen), Flagstaff, AZ, USA; Department of Cell Biology, University of Brasília, Brasilia, Brazil.
authors.forename: M M
authors.initials: MM
authors.lastname: Teixeira
authors.affiliation: Westerdijk Fungal Biodiversity Institute, Utrecht, The Netherlands; Department of Basic Pathology, Federal University of Paraná State, Curitiba, PR, Brazi1; Institute of Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam, The Netherlands.
authors.forename: L F
authors.initials: LF
authors.lastname: Moreno
authors.affiliation: Westerdijk Fungal Biodiversity Institute, Utrecht, The Netherlands.
authors.forename: B J
authors.initials: BJ
authors.lastname: Stielow
authors.affiliation: Institute of Biochemistry and Biophysics, Polish Academy of Sciences, Warsaw, Poland.
authors.forename: A
authors.initials: A
authors.lastname: Muszewska
authors.affiliation: Université Aix-Marseille (CNRS), Marseille, France.
authors.forename: M
authors.initials: M
authors.lastname: Hainaut
authors.affiliation: The National Laboratory for Scientific Computing (LNCC), Petropolis, Brazil.
authors.forename: L
authors.initials: L
authors.lastname: Gonzaga
authors.affiliation: Broad Institute of MIT and Harvard, Cambridge, USA.
authors.forename: A
authors.initials: A
authors.lastname: Abouelleil
authors.affiliation: Department of Biochemistry, University of São Paulo, Brazil.
authors.forename: J S L
authors.initials: JS
authors.lastname: Patané
authors.affiliation: Broad Institute of MIT and Harvard, Cambridge, USA.
authors.forename: M
authors.initials: M
authors.lastname: Priest
authors.affiliation: The National Laboratory for Scientific Computing (LNCC), Petropolis, Brazil.
authors.forename: R
authors.initials: R
authors.lastname: Souza
authors.affiliation: Broad Institute of MIT and Harvard, Cambridge, USA.
authors.forename: S
authors.initials: S
authors.lastname: Young
authors.affiliation: Department of Biological Sciences, Federal University of São Paulo, Diadema, SP, Brazil.
authors.forename: K S
authors.initials: KS
authors.lastname: Ferreira
authors.affiliation: Broad Institute of MIT and Harvard, Cambridge, USA.
authors.forename: Q
authors.initials: Q
authors.lastname: Zeng
authors.affiliation: Núcleo Multidisciplinar de Pesquisa em Biologia UFRJ-Xerém-NUMPEX-BIO, Federal University of Rio de Janeiro, Rio de Janeiro, Brazil.
authors.forename: M M L
authors.initials: MM
authors.lastname: da Cunha
authors.affiliation: Institute of Biochemistry and Biophysics, Polish Academy of Sciences, Warsaw, Poland.
authors.forename: A
authors.initials: A
authors.lastname: Gladki
authors.affiliation: Division of Pathogen Genomics, Translational Genomics Research Institute (TGen), Flagstaff, AZ, USA.
authors.forename: B
authors.initials: B
authors.lastname: Barker
authors.affiliation: Department of Basic Pathology, Federal University of Paraná State, Curitiba, PR, Brazi1.
authors.forename: V A
authors.initials: VA
authors.lastname: Vicente
authors.affiliation: Department of Biochemistry and Molecular Biology, Federal University of Paraná, Curitiba, PR, Brazil.
authors.forename: E M
authors.initials: EM
authors.lastname: de Souza
authors.affiliation: Department of Clinical and Toxicological Analysis, University of São Paulo, São Paulo, SP, Brazil.
authors.forename: S
authors.initials: S
authors.lastname: Almeida
authors.affiliation: Université Aix-Marseille (CNRS), Marseille, France.
authors.forename: B
authors.initials: B
authors.lastname: Henrissat
authors.affiliation: The National Laboratory for Scientific Computing (LNCC), Petropolis, Brazil.
authors.forename: A T R
authors.initials: AT
authors.lastname: Vasconcelos
authors.affiliation: Shanghai Institute of Medical Mycology, Changzheng Hospital, Second Military Medical University, Shanghai, China.
authors.forename: S
authors.initials: S
authors.lastname: Deng
authors.affiliation: Department of Systematic and Evolutionary Botany, University of Vienna, Vienna, Austria.
authors.forename: H
authors.initials: H
authors.lastname: Voglmayr
authors.affiliation: Biological Sciences Department, Faculty of Science, King Abdulaziz University, Jeddah, Saudi Arabia; Botany and Microbiology Department, Faculty of Science, Cairo University, Giza, Egypt.
authors.forename: T A A
authors.initials: TA
authors.lastname: Moussa
authors.affiliation: Federal Institute for Material Research and Testing (BAM), Berlin, Germany.
authors.forename: A
authors.initials: A
authors.lastname: Gorbushina
authors.affiliation: Department of Cell Biology, University of Brasília, Brasilia, Brazil.
authors.forename: M S S
authors.initials: MS
authors.lastname: Felipe
authors.affiliation: Broad Institute of MIT and Harvard, Cambridge, USA.
authors.forename: C A
authors.initials: CA
authors.lastname: Cuomo
authors.affiliation: Westerdijk Fungal Biodiversity Institute, Utrecht, The Netherlands; Department of Basic Pathology, Federal University of Paraná State, Curitiba, PR, Brazi1; Institute of Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam, The Netherlands; Biological Sciences Department, Faculty of Science, King Abdulaziz University, Jeddah, Saudi Arabia.
authors.forename: G Sybren
authors.initials: GS
authors.lastname: de Hoog
keywords: Black yeast; Chaetothyriales; Comparative genomics; Ecology; Evolution; Herpotrichiellaceae; Phylogeny