Article

Exploring the genomic diversity of black yeasts and relatives (<i>Chaetothyriales</i>,<i>Ascomycota</i>)

Mauro Martins TeixeiraDivision of Pathogen Genomics, Translational Genomics Research Institute (TGen), Flagstaff, AZ, USA; Department of Cell Biology, University of Brasília, Brasilia, BrazilLeandro F. MorenoWesterdijk 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 NetherlandsJ. Benjamin StielowWesterdijk Fungal Biodiversity Institute, Utrecht, The NetherlandsAnna MuszewskaInstitute of Biochemistry and Biophysics, Polish Academy of Sciences, Warsaw, PolandMatthieu HainautUniversité Aix-Marseille (CNRS), Marseille, FranceLuiz GonzagaThe National Laboratory for Scientific Computing (LNCC), Petropolis, BrazilAmr AbouelleilBroad Institute of MIT and Harvard, Cambridge, USAJ.S.L. PatanéDepartment of Biochemistry, University of São Paulo, BrazilMargaret PriestBroad Institute of MIT and Harvard, Cambridge, USARicardo Magela de SouzaThe National Laboratory for Scientific Computing (LNCC), Petropolis, BrazilSarah YoungBroad Institute of MIT and Harvard, Cambridge, USAKaren Spadari FerreiraDepartment of Biological Sciences, Federal University of São Paulo, Diadema, SP, BrazilQing‐Yin ZengBroad Institute of MIT and Harvard, Cambridge, USAMarcel Menezes Lyra da CunhaNúcleo Multidisciplinar de Pesquisa em Biologia UFRJ-Xerém-NUMPEX-BIO, Federal University of Rio de Janeiro, Rio de Janeiro, BrazilArkadiusz GładkiInstitute of Biochemistry and Biophysics, Polish Academy of Sciences, Warsaw, PolandBridget M. BarkerDivision of Pathogen Genomics, Translational Genomics Research Institute (TGen), Flagstaff, AZ, USAVânia Aparecida VicenteDepartment of Basic Pathology, Federal University of Paraná State, Curitiba, PR, Brazi1Emanuel Maltempi de SouzaDepartment of Biochemistry and Molecular Biology, Federal University of Paraná, Curitiba, PR, BrazilLuiz Gonzaga Paula de AlmeidaDepartment of Clinical and Toxicological Analysis, University of São Paulo, São Paulo, SP, BrazilBernard HenrissatUniversité Aix-Marseille (CNRS), Marseille, FranceAna Tereza Ribeiro de VasconcelosThe National Laboratory for Scientific Computing (LNCC), Petropolis, BrazilShuwen DengShanghai Institute of Medical Mycology, Changzheng Hospital, Second Military Medical University, Shanghai, ChinaHermann VoglmayrDepartment of Systematic and Evolutionary Botany, University of Vienna, Vienna, AustriaTarek A. A. MoussaBiological Sciences Department, Faculty of Science, King Abdulaziz University, Jeddah, Saudi Arabia; Botany and Microbiology Department, Faculty of Science, Cairo University, Giza, EgyptAnna A. GorbushinaFederal Institute for Material Research and Testing (BAM), Berlin, GermanyMaria Sueli Soares FelipeDepartment of Cell Biology, University of Brasília, Brasilia, BrazilChristina A. CuomoBroad Institute of MIT and Harvard, Cambridge, USASybren de HoogWesterdijk 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

2017en

ABI

Abstract

The order Chaetothyriales ( 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, Chaetothyriales comprise 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 the Chaetothyriales as 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 of Chaetothyriales were 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. The MAT ( MA ting T ype) locus and other sex-related genes were recognized in all 23 black fungi. Members of the asexual genera Fonsecaea and Cladophialophora appear to be heterothallic with a single copy of either MAT-1-1 or MAT-1-2 in each individual. All Capronia species are homothallic as both MAT1-1 and MAT1-2 genes were found in each single genome. The genomic synteny of the MAT -locus flanking genes (SLA2-APN2-COX13) is not conserved in black fungi as is commonly observed in Eurotiomycetes , indicating a unique genomic context for MAT in those species. The heterokaryon (het) genes expansion associated with the low selective pressure at the MAT -locus suggests that a parasexual cycle may play an important role in generating diversity among those fungi.

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DOI: 10.1016/j.simyco.2017.01.001

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