The Extremely Halotolerant Black Yeast Hortaea Werneckii

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The Extremely Halotolerant Black Yeast Hortaea Werneckii Zalar et al. IMA Fungus (2019) 10:10 https://doi.org/10.1186/s43008-019-0007-5 IMA Fungus RESEARCH Open Access The extremely halotolerant black yeast Hortaea werneckii - a model for intraspecific hybridization in clonal fungi Polona Zalar1* , Jerneja Zupančič1, Cene Gostinčar1,2, Janja Zajc3, G. Sybren de Hoog4,5, Filomena De Leo6, Armando Azua-Bustos7,8 and Nina Gunde-Cimerman1 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. Keywords: Morphology, Clustering, NaCl tolerant enyzmes, ITS, D1/D2 rDNA, MCM7, BTB, Genomes INTRODUCTION environments worldwide. It has been isolated from The ascomycetous black yeast Hortaea werneckii (Capno- thalasso-haline brines in salterns on three continents, with diales, Teratosphaeriaceae) is the most extremely halotoler- numerous locations ranging from temperate (Mediterra- ant fungus known, and as such, it has become an important nean) (Gunde-Cimerman et al. 2000, Cabañes et al. 2012, model organism for the study of halotolerance in Eukarya Gunde-Cimerman & Zalar 2014, Elsayed et al. 2016)tosub- (Plemenitaš et al. 2008, 2014, Gunde-Cimerman et al. 2018). tropical and tropical (Mexico, Puerto Rico) (Díaz-Muñoz & Its primary ecological niche are natural hypersaline Montalvo-Rodríguez 2005, Cantrell et al. 2006) climate zones, although never in subpolar and polar regions. Hor- * Correspondence: [email protected] taea werneckii is more frequently found in eutrophic 1Department of Biology, Biotechnical Faculty, University of Ljubljana, Večna thalasso-haline waters at moderate temperatures, while pot 111, SI-1000 Ljubljana, Slovenia it is not known to occur in oligotrophic or Full list of author information is available at the end of the article © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Zalar et al. IMA Fungus (2019) 10:10 Page 2 of 27 athalasso-haline hypersaline waters, and only rarely in Under extremely saline conditions, H. werneckii has an hypersaline waters with elevated temperatures (Plemenitaš extremophilic ecotype, which is characterised by en- &Gunde-Cimerman2005). Occasionally, H. werneckii has hanced melanization, changes in cell size and meristem- been found in seawater (Iwatsu & Udagawa 1988), on atic growth, and changes in colony appearance (Kogej et rocks adjacent to seawater (Ruibal et al. 2009), and inhabit- al. 2007). At the molecular level, the responses of H. ing sea sponges (Brauers et al. 2001), corals (Amend et al. werneckii to high concentrations of toxic sodium ions 2012,Xuetal.2014), marine fish (Todaro et al. 1983), have involved changes in the expression of genes associ- salted freshwater fish (Mok et al. 1981), beach soil (de ated with the synthesis of compatible solutes, regulation Hoog & Guého 1998), saltern microbial mats (Cantrell of intracellular alkali-metal cation concentrations, modi- et al. 2006), and salt marsh plants (Formoso et al. 2015), fications of cell membrane lipid composition, and and as an endophyte in mangrove plants (Chen et al. changes in cell-wall ultrastructure and morphology (Ple- 2012). Recently, it was discovered in an indoor dust sample menitaš et al. 2014). Due to these adaptations, H. wer- collected in Hawaii (Humphries et al. 2017). In agreement neckii has an outstanding ability to overcome the turgor with the extremotolerant nature, it was isolated from 2500 loss and sodium toxicity that are typical of hypersaline m in depth in the Mediterranean Sea (De Leo et al. 2018), environments (Gostinčar et al. 2011). from sediments 5000 m below sea level in the Central Genome sequencing of the H. werneckii strain Indian Basin (Singh et al. 2012), and in sediments 4000 m EXF-2000 (Lenassi et al. 2013, Sinha et al. 2017) has re- below sea level in the East India Ocean (Zhang et al. 2014). vealed that with almost 50 Mb, the H. werneckii genome Using internal transcribed spacer (ITS) clone libraries, H. is larger than the genomes of other sequenced represen- werneckii operational taxonomic units were detected in the tatives of Capnodiales. The H. werneckii genome con- South China Sea in methane-hydrate-bearing deep-sea tained close to 16,000 genes, of which 90% were present sediments (Lai et al. 2007). In spite of the wide distribution in two copies, with an average of 5% amino-acid se- in marine environments, brines in solar salterns are con- quence divergence between the predicted proteins. sidered the primary ecological niche, where at salinities Genomic data fit well with the molecular studies on in- above 20% (w/v) NaCl, H. werneckii represents from 70 to dividual genes performed earlier, as all of the genes stud- 80% of all fungal isolates (Gunde-Cimerman et al. 2000; ied to this point were duplicated and coded for two Butinar et al. 2005), with densities of up to 1400 CFU/L. functionally identical proteins (Vaupotič & Plemenitaš Hortaea werneckii is the only fungus that can grow 2007, Vaupotič et al. 2008). across almost the whole range of NaCl concentrations, Recent analyses of the whole genome sequences of 11 from 0 to 30% NaCl, with a broad optimum between 6 additional strains revealed that two were haploid and the and 14% NaCl (Butinar et al. 2005). As well as NaCl, H. remaining nine were diploid. Differences between the werneckii can also tolerate up to 2 M concentrations of subgenomes of individual strains and their detailed the chaotropic salt MgCl2, and up to 1.7 M CaCl2, and it phylogenetic analyses have shown that the diploid ge- has been isolated from bitterns, i.e. MgCl2-rich leftover nomes were most likely produced by hybridization be- brines after harvesting of NaCl (Zajc et al. 2014). The tween relatively divergent strains (Gostinčar et al. 2018). species also grows on osmotic media with 10% NaCl At the same time, apart from identification of a hetero- with 12% glucose (e.g. malt extract, yeast extract, 10% thallic mating locus, the comparative genomic analyses NaCl, 12% glucose agar) and with 50% glucose (e.g., malt have failed to find any traits that can be linked to sexual extract, yeast extract, 50% glucose agar) (Gunde-Cimer- reproduction. man et al. 2000, Humphries et al. 2017). In summary, the global presence of H. werneckii in Until 2000, H. werneckii was primarily known as the hypersaline environments, its role as the most important aetiological agent of a skin disorder known as tinea model for halotolerance in Eukarya, its extensive physio- nigra, a superficial infection of the human hands and logical plasticity and adaptability, the availability of feet that can occur in warmer climates (de Hoog et al. numerous strains collected from various osmotic environ- 2000, Perez et al. 2005, Bonifaz et al. 2008). Infections ments, and its particular combination of hybridization have been associated with superficially abraded skin ex- with an exclusively or primarily clonal reproduction
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