Black yeasts in hypersaline conditions

Abstract

Extremotolerant and extremophilic fungi are an important part of microbial communities that thrive in extreme environments. Among them, the black yeasts are particularly adaptable. They use their melanized cell walls and versatile morphology, as well as a complex set of molecular adaptations, to survive in conditions that are lethal to most other species. In contrast to extremophilic bacteria and archaea, these fungi are typically extremotolerant rather than extremophilic and exhibit an unusually wide ecological amplitude. Some extremely halotolerant black yeasts can grow in near-saturated NaCl solutions, but can also grow on normal mycological media. They adapt to the low water activity caused by high salt concentrations by sensing their environment, balancing osmotic pressure by accumulating compatible solutes, removing toxic salt ions from the cell using membrane transporters, altering membrane composition and remodelling the highly melanized cell wall. As protection against extreme conditions, halotolerant black yeasts also develop different morphologies, from yeast-like to meristematic. Genomic studies of black yeasts have revealed a variety of reproductive strategies, from clonality to intense recombination and the formation of stable hybrids. Although a comprehensive understanding of the ecological role and molecular adaptations of halotolerant black yeasts remains elusive and the application of many experimental methods is challenging due to their slow growth and recalcitrant cell walls, much progress has been made in deciphering their halotolerance. Advances in molecular tools and genomics are once again accelerating the research of black yeasts, promising further insights into their survival strategies and the molecular basis of their adaptations. KEY POINTS: • Black yeasts show remarkable adaptability to environmental stress • Black yeasts are part of microbial communities in hypersaline environments • Halotolerant black yeasts utilise various molecular and morphological adaptations.

Keywords: Adaptation; Black yeast; Extremophile; Halotolerant; Hypersaline.

Fig. 1

Selected environments in which halotolerant black fungi are commonly found (A–C) and the typical representative species of each environment below them (D–F). (A) A hypersaline lake in the Kalahari Desert, South Africa. (B) Evaporation ponds of solar saltern Sečovlje, Slovenia. (C) Household dishwasher. (D) Aureobasidium melanogenum. (E) Hortaea werneckii. (F) Exophiala dermatitidis

Fig. 2

Major adaptations of black yeasts to growth at high salinity. The cells sense the osmolarity of the medium by membrane sensors and convey the information through the high-osmolarity glycerol and other signalling pathways, triggering a complex network of responses. The energy metabolism of the cell is accelerated to power the increased energy expenditure used for the synthesis of compatible solutes, membrane transporters and other adaptations. The resulting increase in oxidative stress is countered by enzymatic and non-enzymatic antioxidants. Accumulation of compatible solutes balances the osmotic pressure, while membrane transporters powered by the transmembrane proton gradient or ATP maintain physiological intracellular concentrations of Na⁺, K⁺ and other ions as well as retrieve compatible solutes that leak from the cell. Cellular membranes and the melanized cell wall are remodelled to provide structural stability, maintain appropriate membrane fluidity and reduce the leakage of compatible solutes