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.IMPORTANCE Studies of eukaryotic microorganisms under conditions of astrobiological relevance, as well as the aerial dispersion potential of extremophilic yeasts, are still lacking in the literature compared to works with bacteria. Using stratospheric balloon flights and a simulation chamber, we demonstrate that yeasts isolated from an extreme environment are capable of surviving all stressors found in the stratosphere, including intense UV irradiation, scoring an even higher survival than B. subtilis spores. Notably, the yeast N. friedmannii, which displayed one of the highest tolerances to the stratospheric environment in the experiments, was recently proposed to be adapted to airborne transportation, although such a hypothesis had not yet been tested. Our results strengthen such an assumption and can help explain the observed distribution and ecology of this particular yeast species.
Highlights
The high-altitude atmosphere is a harsh environment with extremely low temperatures, low pressure, and high UV irradiation
In order to endure atmospheric transportation, microorganisms must deal with intense UV, dehydration, reduced pressures, and low temperatures [12, 18]
Desiccation is the first challenge faced by these yeasts, but not for metabolically inert B. subtilis spores, which are extremely resistant to this type of stress [34]
Summary
The high-altitude atmosphere is a harsh environment with extremely low temperatures, low pressure, and high UV irradiation. Microorganisms suspended in the air can impact important meteorological and atmospheric processes, such as cloud formation, precipitation, and cloud water chemistry [4, 5] Due to their importance, airborne microbial communities at different environments and altitudes are widely studied using molecular and cultivation-based methods [6,7,8,9,10,11]. Airborne microbial communities at different environments and altitudes are widely studied using molecular and cultivation-based methods [6,7,8,9,10,11] To complement these aerobiological investigations on the ecology of airborne microbes, it is important to study the survival potential of microorganisms under actual atmospheric conditions in order to better understand how living organisms adapt to air transportation and exposure to high altitudes [12, 13]. The study of organisms under Mars-like extreme conditions is relevant to planetary protection research [13, 24]
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