Survival of extremophilic yeasts in the stratospheric environment during balloon flights and in laboratory simulations

Abstract

The high-altitude atmosphere is a harsh environment with extremely low temperatures, low pressure, and high UV irradiation. For this reason, it has been proposed as an analogue for Mars, presenting deleterious factors similar to those on the surface of that planet. We evaluated the survival of extremophilic UV-resistant yeasts isolated from a high-elevation area in the Atacama Desert under stratospheric conditions. As biological controls, intrinsically resistant Bacillus subtilis spores were used. Experiments were performed in two independent stratospheric balloon flights and with an environmental simulation chamber. The three following different conditions were evaluated: (i) desiccation, (ii) desiccation plus exposure to stratospheric low pressure and temperature, and (3) desiccation plus exposure to the full stratospheric environment (UV, low pressure, and temperature). Two strains, Naganishia (Cryptococcus) friedmannii 16LV2 and Exophiala sp. strain 15LV1, survived full exposures to the stratosphere in larger numbers than did B. subtilis spores. Holtermanniella watticus (also known as Holtermanniella wattica) 16LV1, however, suffered a substantial loss in viability upon desiccation and did not survive the stratospheric UV exposure. The remarkable resilience of N. friedmannii and Exophiala sp. 15LV1 under the extreme Mars-like conditions of the stratosphere confirms its potential as a eukaryotic model for astrobiology. Additionally, our results with N. friedmannii strengthen the recent hypothesis that yeasts belonging to the Naganishia genus are fit for aerial dispersion, which might account for the observed abundance of this species in high-elevation soils.