The extremely halotolerant black yeast Hortaea werneckii - a model for intraspecific hybridization in clonal fungi

Abstract The polymorphic black yeast Hortaea werneckii (Capnodiales, Ascomycota) is extremely halotolerant (growth from 0 to 30% [w/v] NaCl) and has been extensively studied as a model for halotolerance in Eukaryotes for over two decades. Its most frequent sources are hypersaline environments and ad...

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Main Authors: Polona Zalar, Jerneja Zupančič, Cene Gostinčar, Janja Zajc, G. Sybren de Hoog, Filomena De Leo, Armando Azua-Bustos, Nina Gunde-Cimerman
Format: Article
Language:English
Published: BMC 2019-07-01
Series:IMA Fungus
Subjects:
Online Access:http://link.springer.com/article/10.1186/s43008-019-0007-5
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author Polona Zalar
Jerneja Zupančič
Cene Gostinčar
Janja Zajc
G. Sybren de Hoog
Filomena De Leo
Armando Azua-Bustos
Nina Gunde-Cimerman
author_facet Polona Zalar
Jerneja Zupančič
Cene Gostinčar
Janja Zajc
G. Sybren de Hoog
Filomena De Leo
Armando Azua-Bustos
Nina Gunde-Cimerman
author_sort Polona Zalar
collection DOAJ
description Abstract The polymorphic black yeast Hortaea werneckii (Capnodiales, Ascomycota) is extremely halotolerant (growth from 0 to 30% [w/v] NaCl) and has been extensively studied as a model for halotolerance in Eukaryotes for over two decades. Its most frequent sources are hypersaline environments and adjacent sea-water habitats in temperate, subtropical and tropical climates. Although typically saprobic, H. werneckii can also act as a commensal coloniser on human skin, causing tinea nigra on hands and soles. Here, we report that addition of NaCl to culture media expands the growth range of H. werneckii to 37 °C, which explains its colonisation of human skin, with its increased salinity. The morphological and physiological plasticity/ versatility of H. werneckii indicate that a species complex might be involved. This was investigated in this polyphasic taxonomic analysis based on the global diversity of H. werneckii strains collected from hypersaline environments, and from humans and animals. Analysis of D1/D2domains of 28S and internal transcribed spacer rDNA revealed 10 and 17 genotypes, respectively, that were not always compliant. The genotypes have global distributions. Human and environmental strains with the same genotypes are intermingled. Due to the limited number of phylogenetically informative characters in the ribosomal DNA dataset, the partial genes encoding for β-tubulin (BTB) and mini-chromosome maintenance protein (MCM7) were also sequenced. The use of these genes was hampered by ambiguous sequences obtained by Sanger sequencing, as a consequence of the diploid and highly heterozygous genome of many H. werneckii strains. Analysis of the BTB and MCM7 genes showed that in some cases two copies of the gene from the same genome are positioned in distant phylogenetic clusters of the intraspecific gene tree. Analysis of whole-genome sequences of selected H. werneckii strains generally confirmed the phylogenetic distances estimated on the basis of ribosomal genes, but also showed substantial reticulation within the phylogenetic history of the strains. This is in line with the hypothesis that the diploid genomes of H. werneckii were formed by hybridizations, which have sometimes occurred between relatively divergent strains.
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spelling doaj.art-2e3acf2c48e544b4921352c460102e7e2025-02-02T06:02:50ZengBMCIMA Fungus2210-63592019-07-0110112710.1186/s43008-019-0007-5The extremely halotolerant black yeast Hortaea werneckii - a model for intraspecific hybridization in clonal fungiPolona Zalar0Jerneja Zupančič1Cene Gostinčar2Janja Zajc3G. Sybren de Hoog4Filomena De Leo5Armando Azua-Bustos6Nina Gunde-Cimerman7Department of Biology, Biotechnical Faculty, University of LjubljanaDepartment of Biology, Biotechnical Faculty, University of LjubljanaDepartment of Biology, Biotechnical Faculty, University of LjubljanaDepartment of Biotechnology and Systems Biology, National Institute of BiologyWesterdijk Fungal Biodiversity InstituteDepartment of Chemical, Biological, Pharmaceutical and Environmental Sciences (ChiBioFarAm), University of MessinaCentro de Astrobiología (CSIC-INTA)Department of Biology, Biotechnical Faculty, University of LjubljanaAbstract The polymorphic black yeast Hortaea werneckii (Capnodiales, Ascomycota) is extremely halotolerant (growth from 0 to 30% [w/v] NaCl) and has been extensively studied as a model for halotolerance in Eukaryotes for over two decades. Its most frequent sources are hypersaline environments and adjacent sea-water habitats in temperate, subtropical and tropical climates. Although typically saprobic, H. werneckii can also act as a commensal coloniser on human skin, causing tinea nigra on hands and soles. Here, we report that addition of NaCl to culture media expands the growth range of H. werneckii to 37 °C, which explains its colonisation of human skin, with its increased salinity. The morphological and physiological plasticity/ versatility of H. werneckii indicate that a species complex might be involved. This was investigated in this polyphasic taxonomic analysis based on the global diversity of H. werneckii strains collected from hypersaline environments, and from humans and animals. Analysis of D1/D2domains of 28S and internal transcribed spacer rDNA revealed 10 and 17 genotypes, respectively, that were not always compliant. The genotypes have global distributions. Human and environmental strains with the same genotypes are intermingled. Due to the limited number of phylogenetically informative characters in the ribosomal DNA dataset, the partial genes encoding for β-tubulin (BTB) and mini-chromosome maintenance protein (MCM7) were also sequenced. The use of these genes was hampered by ambiguous sequences obtained by Sanger sequencing, as a consequence of the diploid and highly heterozygous genome of many H. werneckii strains. Analysis of the BTB and MCM7 genes showed that in some cases two copies of the gene from the same genome are positioned in distant phylogenetic clusters of the intraspecific gene tree. Analysis of whole-genome sequences of selected H. werneckii strains generally confirmed the phylogenetic distances estimated on the basis of ribosomal genes, but also showed substantial reticulation within the phylogenetic history of the strains. This is in line with the hypothesis that the diploid genomes of H. werneckii were formed by hybridizations, which have sometimes occurred between relatively divergent strains.http://link.springer.com/article/10.1186/s43008-019-0007-5MorphologyClusteringNaCl tolerant enyzmesITSD1/D2 rDNAMCM7
spellingShingle Polona Zalar
Jerneja Zupančič
Cene Gostinčar
Janja Zajc
G. Sybren de Hoog
Filomena De Leo
Armando Azua-Bustos
Nina Gunde-Cimerman
The extremely halotolerant black yeast Hortaea werneckii - a model for intraspecific hybridization in clonal fungi
IMA Fungus
Morphology
Clustering
NaCl tolerant enyzmes
ITS
D1/D2 rDNA
MCM7
title The extremely halotolerant black yeast Hortaea werneckii - a model for intraspecific hybridization in clonal fungi
title_full The extremely halotolerant black yeast Hortaea werneckii - a model for intraspecific hybridization in clonal fungi
title_fullStr The extremely halotolerant black yeast Hortaea werneckii - a model for intraspecific hybridization in clonal fungi
title_full_unstemmed The extremely halotolerant black yeast Hortaea werneckii - a model for intraspecific hybridization in clonal fungi
title_short The extremely halotolerant black yeast Hortaea werneckii - a model for intraspecific hybridization in clonal fungi
title_sort extremely halotolerant black yeast hortaea werneckii a model for intraspecific hybridization in clonal fungi
topic Morphology
Clustering
NaCl tolerant enyzmes
ITS
D1/D2 rDNA
MCM7
url http://link.springer.com/article/10.1186/s43008-019-0007-5
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