Whole genome duplication and enrichment of metal cation transporters revealed by de novo genome sequencing of extremely halotolerant black yeast Hortaea werneckii

• Published in: PloS one 2013-08, Vol.8 (8), p.e71328
• Main Authors: Lenassi, Metka, Gostinčar, Cene, Jackman, Shaun, Turk, Martina, Sadowski, Ivan, Nislow, Corey, Jones, Steven, Birol, Inanc, Cimerman, Nina Gunde, Plemenitaš, Ana
• Format: Article
• Language: English
• Subjects: Adaptability; Adenosine triphosphatase; Amino Acid Sequence; Analysis; ATPases; Baking yeast; Biochemistry; Bioenergetics; Biology; Cancer; Cation Transport Proteins - classification; Cation Transport Proteins - genetics; Cation Transport Proteins - metabolism; Cations; Deoxyribonucleic acid; DNA; DNA sequencing; Ethanol; Fungal Proteins - classification; Fungal Proteins - genetics; Fungal Proteins - metabolism; Fungi; Gene Dosage; Gene Duplication; Gene Expression Regulation, Fungal; Gene sequencing; Genes; Genetic aspects; Genetic engineering; Genome Size; Genome, Fungal; Genomes; Genomics; Homeostasis; Hydrogen; Ion Transport; Mating; Metals; Microorganisms; Molecular Sequence Data; Osmotic Pressure; Phylogeny; Plants (botany); Proteins; Redundancy; Reproduction (copying); Saccharomyces cerevisiae; Saccharomycetales - classification; Saccharomycetales - genetics; Saccharomycetales - metabolism; Salinity; Salinity tolerance; Salt; Salt Tolerance - genetics; Salts; Salts - metabolism; Sequence Alignment; Sequence Analysis, DNA; Signal transduction; Sodium Chloride; Target recognition; Transcription; Yeast
• ISSN: 1932-6203; 1932-6203
• DOI: 10.1371/journal.pone.0071328

Hortaea werneckii, ascomycetous yeast from the order Capnodiales, shows an exceptional adaptability to osmotically stressful conditions. To investigate this unusual phenotype we obtained a draft genomic sequence of a H. werneckii strain isolated from hypersaline water of solar saltern. Two of its most striking characteristics that may be associated with a halotolerant lifestyle are the large genetic redundancy and the expansion of genes encoding metal cation transporters. Although no sexual state of H. werneckii has yet been described, a mating locus with characteristics of heterothallic fungi was found. The total assembly size of the genome is 51.6 Mb, larger than most phylogenetically related fungi, coding for almost twice the usual number of predicted genes (23333). The genome appears to have experienced a relatively recent whole genome duplication, and contains two highly identical gene copies of almost every protein. This is consistent with some previous studies that reported increases in genomic DNA content triggered by exposure to salt stress. In hypersaline conditions transmembrane ion transport is of utmost importance. The analysis of predicted metal cation transporters showed that most types of transporters experienced several gene duplications at various points during their evolution. Consequently they are present in much higher numbers than expected. The resulting diversity of transporters presents interesting biotechnological opportunities for improvement of halotolerance of salt-sensitive species. The involvement of plasma P-type H⁺ ATPases in adaptation to different concentrations of salt was indicated by their salt dependent transcription. This was not the case with vacuolar H⁺ ATPases, which were transcribed constitutively. The availability of this genomic sequence is expected to promote the research of H. werneckii. Studying its extreme halotolerance will not only contribute to our understanding of life in hypersaline environments, but should also identify targets for improving the salt- and osmotolerance of economically important plants and microorganisms.