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Environmental Microbiology

Survival of Extremophilic Yeasts in the Stratospheric Environment during Balloon Flights and in Laboratory Simulations

André Arashiro Pulschen, Gabriel Guarany de Araujo, Ana Carolina Souza Ramos de Carvalho, Maria Fernanda Cerini, Lucas de Mendonça Fonseca, Douglas Galante, Fabio Rodrigues
Robert M. Kelly, Editor
André Arashiro Pulschen
aInstitute of Chemistry, University of São Paulo, São Paulo, Brazil
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Gabriel Guarany de Araujo
bInterunities Graduate Program in Biotechnology, University of São Paulo, São Paulo, Brazil
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Ana Carolina Souza Ramos de Carvalho
bInterunities Graduate Program in Biotechnology, University of São Paulo, São Paulo, Brazil
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Maria Fernanda Cerini
cGraduate Program in Biomolecular Physics, São Carlos Institute of Physics, University of São Paulo, São Paulo, Brazil
dBrazilian Synchrotron Light Laboratory, Brazilian Center for Research in Energy and Materials, Campinas, São Paulo, Brazil
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Lucas de Mendonça Fonseca
eAirvantis P&D Ltda., São Carlos, São Paulo, Brazil
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Douglas Galante
cGraduate Program in Biomolecular Physics, São Carlos Institute of Physics, University of São Paulo, São Paulo, Brazil
dBrazilian Synchrotron Light Laboratory, Brazilian Center for Research in Energy and Materials, Campinas, São Paulo, Brazil
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Fabio Rodrigues
fDepartment of Fundamental Chemistry, Institute of Chemistry, University of São Paulo, São Paulo, Brazil
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Robert M. Kelly
North Carolina State University
Roles: Editor
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DOI: 10.1128/AEM.01942-18
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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.

FOOTNOTES

    • Received 8 August 2018.
    • Accepted 12 September 2018.
    • Accepted manuscript posted online 28 September 2018.
  • Supplemental material for this article may be found at https://doi.org/10.1128/AEM.01942-18.

  • Copyright © 2018 Pulschen et al.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

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Survival of Extremophilic Yeasts in the Stratospheric Environment during Balloon Flights and in Laboratory Simulations
André Arashiro Pulschen, Gabriel Guarany de Araujo, Ana Carolina Souza Ramos de Carvalho, Maria Fernanda Cerini, Lucas de Mendonça Fonseca, Douglas Galante, Fabio Rodrigues
Applied and Environmental Microbiology Nov 2018, 84 (23) e01942-18; DOI: 10.1128/AEM.01942-18

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Survival of Extremophilic Yeasts in the Stratospheric Environment during Balloon Flights and in Laboratory Simulations
André Arashiro Pulschen, Gabriel Guarany de Araujo, Ana Carolina Souza Ramos de Carvalho, Maria Fernanda Cerini, Lucas de Mendonça Fonseca, Douglas Galante, Fabio Rodrigues
Applied and Environmental Microbiology Nov 2018, 84 (23) e01942-18; DOI: 10.1128/AEM.01942-18
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KEYWORDS

yeasts
Naganishia friedmannii
Cryptococcus
aerobiology
astrobiology
Atacama
extremophiles
stratosphere
UV light

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