Abstract
BackgroundThe basidomycete Wallemia ichthyophaga from the phylogenetically distinct class Wallemiomycetes is the most halophilic fungus known to date. It requires at least 10% NaCl and thrives in saturated salt solution. To investigate the genomic basis of this exceptional phenotype, we obtained a de-novo genome sequence of the species type-strain and analysed its transcriptomic response to conditions close to the limits of its lower and upper salinity range.ResultsThe unusually compact genome is 9.6 Mb large and contains 1.67% repetitive sequences. Only 4884 predicted protein coding genes cover almost three quarters of the sequence. Of 639 differentially expressed genes, two thirds are more expressed at lower salinity. Phylogenomic analysis based on the largest dataset used to date (whole proteomes) positions Wallemiomycetes as a 250-million-year-old sister group of Agaricomycotina. Contrary to the closely related species Wallemia sebi, W. ichthyophaga appears to have lost the ability for sexual reproduction. Several protein families are significantly expanded or contracted in the genome. Among these, there are the P-type ATPase cation transporters, but not the sodium/ hydrogen exchanger family. Transcription of all but three cation transporters is not salt dependent. The analysis also reveals a significant enrichment in hydrophobins, which are cell-wall proteins with multiple cellular functions. Half of these are differentially expressed, and most contain an unusually large number of acidic amino acids. This discovery is of particular interest due to the numerous applications of hydrophobines from other fungi in industry, pharmaceutics and medicine.ConclusionsW. ichthyophaga is an extremophilic specialist that shows only low levels of adaptability and genetic recombination. This is reflected in the characteristics of its genome and its transcriptomic response to salt. No unusual traits were observed in common salt-tolerance mechanisms, such as transport of inorganic ions or synthesis of compatible solutes. Instead, various data indicate a role of the cell wall of W. ichthyophaga in its response to salt. Availability of the genomic sequence is expected to facilitate further research into this unique species, and shed more light on adaptations that allow it to thrive in conditions lethal to most other eukaryotes.
Highlights
The basidomycete Wallemia ichthyophaga from the phylogenetically distinct class Wallemiomycetes is the most halophilic fungus known to date
The total assembly size of the W. ichthyophaga genome is 9.6 Mb, and it is assembled into 101 contigs and 82 scaffolds (Table 1)
Transcriptome of Wallemia ichthyophaga at limiting salinities Mapping more than 50 million EST sequences to the W. ichthyophaga genome aligned 83.96% and 83.70% of reads (transcriptome grown at 10% and 30% NaCl (w/v), respectively; Additional file 4: Table S3)
Summary
The basidomycete Wallemia ichthyophaga from the phylogenetically distinct class Wallemiomycetes is the most halophilic fungus known to date. It requires at least 10% NaCl and thrives in saturated salt solution. W. ichthyophaga requires at least 1.5 M NaCl for in-vitro growth (or some other osmolyte for an equivalent aw), and it even thrives in saturated NaCl solution It tolerates high concentrations of other salts, such as MgCl2 (Sonjak et al, unpublished data). Such a narrow ecological amplitude is common for specialised archaeal halophiles, but in the fungal kingdom it is an exception. W. ichthyophaga is a rare fungal example of an obligate extremophilic specialist [9], and it is considered to be the most halophilic fungus known to date
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