Abstract
BackgroundHortaea werneckii is one of the most salt-tolerant species among microorganisms. It has been isolated from hypersaline waters of salterns as one of the predominant species of a group of halophilic and halotolerant melanized yeast-like fungi, arbitrarily named as "black yeasts". It has previously been shown that H. werneckii has distinct mechanisms of adaptation to high salinity environments that are not seen in salt-sensitive and only moderately salt-tolerant fungi. In H. werneckii, the HOG pathway is important for sensing the changes in environmental osmolarity, as demonstrated by identification of three main pathway components: the mitogen-activated protein kinase (MAPK) HwHog1, the MAPK kinase HwPbs2, and the putative histidine kinase osmosensor HwHhk7.ResultsIn this study, we show that the expression of HwHOG1 in salt-adapted cells depends on the environmental salinity and that HwHOG1 transcription responds rapidly but reciprocally to the acute hyper-saline or hypo-saline stress. Molecular modelling of HwHog1 reveals an overall structural homology with other MAPKs. HwHog1 complements the function of ScHog1 in the Saccharomyces cerevisiae multistress response. We also show that hyper-osmolar, oxidative and high-temperature stresses activate the HwHog1 kinase, although under high-temperature stress the signal is not transmitted via the MAPK kinase Pbs2. Identification of HOG1-like genes from other halotolerant fungi isolated from solar salterns demonstrates a high degree of similarity and excellent phylogenetic clustering with orthologues of fungal origin.ConclusionThe HOG signalling pathway has an important role in sensing and responding to hyper-osmolar, oxidative and high-temperature stresses in the halophilic fungi H. werneckii. These findings are an important advance in our understanding of the HOG pathway response to stress in H. werneckii, a proposed model organism for studying the salt tolerance of halophilic and halotolerant eukaryotes.
Highlights
Hortaea werneckii is one of the most salt-tolerant species among microorganisms
We examined how different NaCl concentrations in the growth media affect the expression of the HwHOG1 gene in cells adapted to 1.0 M, 3.0 M and 4.5 M NaCl and in salt-stressed cells
Following the first acute stress response for both of these stresses, a slow but continous increase in HwHOG1 transcript levels was seen after 90 min, suggesting the starting phase of the adaptive response, which probably contributes to the levels of the transcript seen in the adaptation study (Fig. 1A)
Summary
Hortaea werneckii is one of the most salt-tolerant species among microorganisms. It has been isolated from hypersaline waters of salterns as one of the predominant species of a group of halophilic and halotolerant melanized yeast-like fungi, arbitrarily named as "black yeasts". Solar salterns represent an extreme environment, with high concentrations of NaCl, occasional rapid changes in water activity, low oxygen concentrations and high UV radiation [1]. These environments are inhabited mostly by bacteria and archea, and by certain algal and fungal species [2,3,4]. These extremophilic fungi are represented by a group of melanized fungi, the so-called black yeasts Hortaea werneckii, Phaeotheca triangularis and Aureobasidium pullulans, and by the non-melanized fungi Wallemia sebi, W. muriae and W. ichthyophaga. The most relevant differences studied to date are in plasma membrane composition and properties [7], osmolyte composition and accumulation [5,8], and the maintenance of low intracellular potassium and sodium ion levels [9]
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