Abstract
The basidiomycetous fungus Wallemia ichthyophaga grows between 1.7 and 5.1 M NaCl and is the most halophilic eukaryote described to date. Like other fungi, W. ichthyophaga detects changes in environmental salinity mainly by the evolutionarily conserved high-osmolarity glycerol (HOG) signaling pathway. In Saccharomyces cerevisiae, the HOG pathway has been extensively studied in connection to osmotic regulation, with a valuable knock-out strain collection established. In the present study, we reconstructed the architecture of the HOG pathway of W. ichthyophaga in suitable S. cerevisiae knock-out strains, through heterologous expression of the W. ichthyophaga HOG pathway proteins. Compared to S. cerevisiae, where the Pbs2 (ScPbs2) kinase of the HOG pathway is activated via the SHO1 and SLN1 branches, the interactions between the W. ichthyophaga Pbs2 (WiPbs2) kinase and the W. ichthyophaga SHO1 branch orthologs are not conserved: as well as evidence of poor interactions between the WiSho1 Src-homology 3 (SH3) domain and the WiPbs2 proline-rich motif, the absence of a considerable part of the osmosensing apparatus in the genome of W. ichthyophaga suggests that the SHO1 branch components are not involved in HOG signaling in this halophilic fungus. In contrast, the conserved activation of WiPbs2 by the S. cerevisiae ScSsk2/ScSsk22 kinase and the sensitivity of W. ichthyophaga cells to fludioxonil, emphasize the significance of two-component (SLN1-like) signaling via Group III histidine kinase. Combined with protein modeling data, our study reveals conserved and non-conserved protein interactions in the HOG signaling pathway of W. ichthyophaga and therefore significantly improves the knowledge of hyperosmotic signal processing in this halophilic fungus.
Highlights
The hypersaline environments of salterns are inhabited by fungal species that are well adapted to these extreme environmental conditions (Gostincar et al, 2011)
We searched for a homolog of the histidine kinase Tco1 (CnNik1) as it has been shown to be involved in the high-osmolarity glycerol (HOG) pathway of C. neoformans (Bahn et al, 2006)
We analyzed the genome of W. ichthyophaga, heterologously expressed the selected W. ichthyophaga HOG signaling proteins, and studied their functions and interactions to further illucidate the architecture of the HOG pathway in this halophilic basidiomycetous fungus
Summary
The hypersaline environments of salterns are inhabited by fungal species that are well adapted to these extreme environmental conditions (Gostincar et al, 2011). The basidiomycete Wallemia ichthyophaga, which was originally isolated from the solar salterns of Secovlje, Slovenia, is the most halophilic eukaryote (Zalar et al, 2005) This obligate halophilic fungus forms multicellular clumps in liquid media, has a coccoid, sarcina-like, morphology (Kralj Kuncicet al., 2010), and grows in media enriched with NaCl concentrations from 1.7 to 5.1 M. This phenotype is unusual in the fungal kingdom, and makes W. ichthyophaga an interesting model organism
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