4.4 Article

Bacterial Cellulose Retains Robustness but Its Synthesis Declines After Exposure to a Mars-Like Environment Simulated Outside the International Space Station

Journal

ASTROBIOLOGY
Volume 21, Issue 6, Pages 706-717

Publisher

MARY ANN LIEBERT, INC
DOI: 10.1089/ast.2020.2332

Keywords

Bacterial cellulose; Extraterrestrial stressors; Microbial biosignature; Kombucha multimicrobial community; Komagataeibacter oboediens; The bcs operon

Funding

  1. National Academy of Sciences of Ukraine [49/2018-2019]
  2. DLR programatic management (Grant BioSigN PF/FE)

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This study revealed the characteristics of bacterial cellulose after long-term spaceflight and exposure to Mars-like stressors for the first time. The mechanical properties of cellulose-based pellicle films remained similar under Mars-like conditions, while cellulose production decreased, likely due to epigenetic regulation. Therefore, cellulose could serve as a good material to protect microbial communities during space journeys.
Cellulose is a widespread macromolecule in terrestrial environments and a major architectural component of microbial biofilm. Therefore, cellulose might be considered a biosignature that indicates the presence of microbial life. We present, for the first time, characteristics of bacterial cellulose after long-term spaceflight and exposure to simuled Mars-like stressors. The pristine cellulose-based pellicle membranes from a kombucha microbial community (KMC) were exposed outside the International Space Station, and after their return to Earth, the samples were reactivated and cultured for 2.5 years to discern whether the KMC could be restored. Analyses of cellulose polymer integrity and mechanical properties of cellulose-based pellicle films, as well as the cellulose biosynthesis-related genes' structure and expression, were performed. We observed that (i) the cellulose polymer integrity was not significantly changed under Mars-like conditions; (ii) de novo cellulose production was 1.5 times decreased in exposed KMC samples; (iii) the dry cellulose yield from the reisolated Komagataeibacter oboediens was 1.7 times lower than by wild type; (iv) there was no significant change in mechanical properties of the de novo synthesized cellulose-based pellicles produced by the exposed KMCs and K. oboediens; and (v) the gene, encoding biosynthesis of cellulose (bcsA) of the K. oboediens, was downregulated, and no topological change or mutation was observed in any of the bcs operon genes, indicating that the decreased cellulose production by the space-exposed samples was probably due to epigenetic regulation. Our results suggest that the cellulose-based pellicle could be a good material with which to protect microbial communities during space journeys, and the cellulose produced by KMC members could be suitable in the fabrication of consumer goods for extraterrestrial locations.

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