Yeasts Inhabiting Extreme Environments and Their Biotechnological Applications

Abstract

Yeasts are microscopic fungi inhabiting all Earth environments, including those inhospitable for most life forms, considered extreme environments. According to their habitats, yeasts could be extremotolerant or extremophiles. Some are polyextremophiles, depending on their growth capacity, tolerance, and survival in the face of their habitat's physical and chemical constitution. The extreme yeasts are relevant for the industrial production of value-added compounds, such as biofuels, lipids, carotenoids, recombinant proteins, enzymes, among others. This review calls attention to the importance of yeasts inhabiting extreme environments, including metabolic and adaptive aspects to tolerate conditions of cold, heat, water availability, pH, salinity, osmolarity, UV radiation, and metal toxicity, which are relevant for biotechnological applications. We explore the habitats of extreme yeasts, highlighting key species, physiology, adaptations, and molecular identification. Finally, we summarize several findings related to the industrially-important extremophilic yeasts and describe current trends in biotechnological applications that will impact the bioeconomy.

Keywords: extreme habitats; extremophilic yeasts; stress response; yeast biotechnology; yeast identification.

Figure 1

Representative scheme of yeasts in atmospheric, aquatic, and terrestrial environments. (A) In the atmospheric environment, yeasts have been found in the air of the highest mountains on Earth, the troposphere (T), even in the stratosphere (S), an environment of conditions of extreme cold, dryness, low atmospheric pressure, and high ultraviolet (UV) radiation. Yeasts are unlikely to proliferate in the air, viability is lost as height increases, but spores of some species can remain dormant and germinate later in favorable conditions. (B) In saltwater aquatic environments, yeasts can be found in the depths of the oceans, on the sea surface, in aquatic plants, in animals, etc. The conditions in this environment include combinations of temperature, atmospheric pressure, salinity or UV radiation. (C,D) In freshwater aquatic environments, yeasts have been found in rivers, lagoons, lakes, estuaries, glaciers, aquifers, geysers, etc. These environments may present combinations of conditions of cold, heat, dryness, acidic, alkaline, salinity, osmolarity, UV radiation, or toxicity (sites contaminated with industrial waste; e.g., heavy metals, chemicals, etc.). (E,F) In the terrestrial environment, yeasts have been isolated from soils, rocks, plants, animals, mountains, deserts, etc. The terrestrial environment presents combined conditions of cold, heat, dryness, acidic, alkaline, salinity, or UV radiation. Symbols for different extreme conditions are shown at the bottom of panels (A–F). Panel (C), based from Buzzini et al., 2018 [15]. Created using BioRender.com, accessed on 10 February 2022.

Figure 2

Representative scheme of the metabolic pathways activated under different stress conditions in non-Saccharomyces or oleaginous yeasts. The abbreviations correspond to reactive oxygen species (ROS), triacylglycerols (TAG), diacylglycerols (DAG), inorganic phosphate (Pi), nicotinamide-adenine dinucleotide phosphate (NADPH or NADP), NADPH oxidases (NOX), mitogen-activated protein kinases (MAPK, MAPKK, and MAPKKK), dihydroxyacetone phosphate (DHAP), transcription factors (TF), endoplasmic reticulum (ER), malic enzyme (ME), ATP-citrate lyase or synthase (ACL), acetyl-CoA carboxylase (ACC), malate dehydrogenase (MHD), and isocitrate dehydrogenase (ICDH). ROS accumulation generates oxidative stress, which increases secondary metabolites, the pentose phosphate pathway, glutamate catabolism, and ER stress. Low-temperature conditions increase neutral fatty acid synthesis from triacylglycerols (TAG), whereas at high temperatures, TAG desaturation increases. In oleaginous yeasts, oligotrophic conditions, such as nitrogen-limitation, induce lipogenesis and TAG accumulation in lipid drops (LD), alleviating lipotoxicity. Based from Patel, et al., 2016 and Shi et al., 2017 [43,44]. Adapted from “TAG synthesis”, by BioRender.com (2022). Retrieved from https://app.biorender.com/biorender-templates (accessed on 1 February 2022).