Ecology and molecular adaptations of the halophilic black yeast Hortaea werneckii

Abstract

Molecular studies on halophilic adaptations have focused on prokaryotic microorganisms due to a lack of known appropriate eukaryotic halophilic microorganisms. However, the black yeast Hortaea werneckii has been identified as the dominant fungal species in hypersaline waters on three continents. It represents a new model organism for studying the mechanisms of salt tolerance in eukaryotes. Ultrastructural studies of the H. werneckii cell wall have shown that it synthesizes dihydroxynaphthalene (DHN) melanin under both saline and non-saline growth conditions. However, melanin granules in the cell walls are organized in a salt-dependent way, implying the potential osmoprotectant role of melanin. At the level of membrane structure, H. werneckii maintains a sterol-to-phospholipid ratio significantly lower than the salt-sensitive Saccharomyces cerevisiae. Accordingly, membranes of H. werneckii are more fluid over a wide range of NaCl concentrations, indicating high intrinsic salt stress tolerance. Even H. werneckii grown in high NaCl concentrations maintains very low intracellular amounts of potassium and sodium, demonstrating the sodium-excluder character of this organism. The salt-dependent expressions of two HwENA genes suggest roles for them in the adaptation to changing salt concentrations. The high similarity of these ENA ATPases to other fungal ENA ATPases involved in Na + /K + transport indicates their potential importance in H. werneckii ion homeostasis. Glycerol is the main compatible solute which accumulates in the cytoplasm of H. werneckii at high salinity, although it seems that mycosporines may also act as supplementary compatible solutes. Salt dependent increase in glycerol synthesis is supported by the identification of two copies of a gene putatively coding for glycerol-3-phosphate-dehydrogenase. Expression of only one of these genes is salt dependent.

Overview on the Fungal Metabolites Involved in Mycopathy

“…Fungal melanins are usually found in the cell walls of spores, sclerotia, mycelia or fruiting bodies [198]. Even when not directly involved in pathogenesis, melanins provide structural strength [199] and protect fungi against environmental stresses such as oxygen free radicals [200], UV radiation [201]- [204], wall-degrading enzymes produced by antagonist microbes [205] [206], high salinity [207] and heavy metals toxicity [208]. It has been suggested that due to antioxidant property of melanins they can neutralize oxidants produced by immune effector cells.…”

Global Molecular Diversity of the Halotolerant Fungus Hortaea werneckii

“…Examples are found in the cold [ 1 ], at high temperatures [ 2 ], with toxic hydrocarbons [ 3 ] or ultra-low pH [ 4 ], at high osmolarity [ 5 ], or on rock [ 6 , 7 ]. The halophilic black yeast H. werneckii is one of the most salt tolerant eukaryotic organisms so far described [ 8 ]. It is characterized by melanin production, pleomorphism of yeast and filamentous phases, and meristematic development [ 9 , 10 ]—characters we also observe in numerous rock-inhabiting fungi [ 6 ].…”

A First Record of Obligate Halophilic Aspergilli from the Dead Sea

“…Hypersaline conditions drastically decrease the biodiversity by exerting a strong selective pressure, resulting in the development of halophilic and halotolerant microbes [2], the study of which has drawn much interest [3]. Fungi are known to adapt to certain extreme environments, but isolation and identification of fungi from these habitats have been frequently hindered due to their slow growth and low ability to compete [4].…”