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.
Highlights
The ascomycetous black yeast Hortaea werneckii (Capnodiales, Teratosphaeriaceae) is the most extremely halotolerant fungus known, and as such, it has become an important model organism for the study of halotolerance in Eukarya (Plemenitaš et al 2008, 2014, Gunde-Cimerman et al 2018)
In agreement with the extremotolerant nature, it was isolated from 2500 m in depth in the Mediterranean Sea (De Leo et al 2018), from sediments 5000 m below sea level in the Central Indian Basin (Singh et al 2012), and in sediments 4000 m below sea level in the East India Ocean (Zhang et al 2014)
The variant calling for internal transcribed spacer (ITS) and large subunit (LSU) regions for the strains with sequenced genomes showed that a single genome contained a single variant of the ITS and D1/D2 rDNA sequence (Additional file 1: Table S1)
Summary
The ascomycetous black yeast Hortaea werneckii (Capnodiales, Teratosphaeriaceae) is the most extremely halotolerant fungus known, and as such, it has become an important model organism for the study of halotolerance in Eukarya (Plemenitaš et al 2008, 2014, Gunde-Cimerman et al 2018). H. werneckii has been found in seawater (Iwatsu & Udagawa 1988), on rocks adjacent to seawater (Ruibal et al 2009), and inhabiting sea sponges (Brauers et al 2001), corals (Amend et al 2012, Xu et al 2014), marine fish (Todaro et al 1983), salted freshwater fish (Mok et al 1981), beach soil (de Hoog & Guého 1998), saltern microbial mats (Cantrell et al 2006), and salt marsh plants (Formoso et al 2015), and as an endophyte in mangrove plants (Chen et al 2012). In spite of the wide distribution in marine environments, brines in solar salterns are considered the primary ecological niche, where at salinities above 20% (w/v) NaCl, H. werneckii represents from 70 to 80% of all fungal isolates (Gunde-Cimerman et al 2000; Butinar et al 2005), with densities of up to 1400 CFU/L
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