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Komagataeibacter is the dominant taxon and cellulose-producing bacteria in the Kombucha Microbial Community (KMC). This is the first study to isolate the K. oboediens genome from a reactivated space-exposed KMC sample and comprehensively characterize it. The space-exposed genome was compared with the Earth-based reference genome to understand the genome stability of K. oboediens under extraterrestrial conditions during a long time. Our results suggest that the genomes of K. oboediens IMBG180 (ground sample) and K. oboediens IMBG185 (space-exposed) are remarkably similar in topology, genomic islands, transposases, prion-like proteins, and number of plasmids and CRISPR-Cas cassettes. Nonetheless, there was a difference in the length of plasmids and the location of cas genes. A small difference was observed in the number of protein coding genes. Despite these differences, they do not affect any genetic metabolic profile of the cellulose synthesis, nitrogen-fixation, hopanoid lipids biosynthesis, and stress-related pathways. Minor changes are only observed in central carbohydrate and energy metabolism pathways gene numbers or sequence completeness. Altogether, these findings suggest that K. oboediens maintains its genome stability and functionality in KMC exposed to the space environment most probably due to the protective role of the KMC biofilm. Furthermore, due to its unaffected metabolic pathways, this bacterial species may also retain some promising potential for space applications.

Humankind has entered a new era of space exploration: settlements on other planetary bodies are foreseen in the near future. Advanced technologies are being developed to support the adaptation to extraterrestrial environments and, with a view on the longer term, to support the viability of an independent economy. Biological processes will likely play a key role and lead to the production of life-support consumables, and other commodities, in a way that is cheaper and more sustainable than exclusively abiotic processes. Microbial communities could be used to sustain the crews’ health as well as for the production of consumables, for waste recycling, and for biomining. They can self-renew with little resources from Earth, be highly productive on a per-volume basis, and be highly versatile—all of which will be critical in planetary outposts. Well-defined, semi-open, and stress-resistant microecosystems are particularly promising. An instance of it is kombucha, known worldwide as a microbial association that produces an eponymous, widespread soft drink that could be valuable for sustaining crews’ health or as a synbiotic (i.e., probiotic and prebiotic) after a rational assemblage of defined probiotic bacteria and yeasts with endemic or engineered cellulose producers. Bacterial cellulose products offer a wide spectrum of possible functions, from leather-like to innovative smart materials during long-term missions and future activities in extraterrestrial settlements. Cellulose production by kombucha is zero-waste and could be linked to bioregenerative life support system (BLSS) loops. Another advantage of kombucha lies in its ability to mobilize inorganic ions from rocks, which may help feed BLSS from local resources. Besides outlining those applications and others, we discuss needs for knowledge and other obstacles, among which is the biosafety of microbial producers.

Outer membrane vesicles (OMVs), produced by nonpathogenic Gram-negative bacteria, have potentially useful biotechnological applications in extraterrestrial extreme environments. However, their biological effects under the impact of various stressors have to be elucidated for safety reasons. In the spaceflight experiment, model biofilm kombucha microbial community (KMC) samples, in which Komagataeibacter intermedius was a dominant community-member, were exposed under simulated Martian factors (i.e., pressure, atmosphere, and UV-illumination) outside the International Space Station (ISS) for 1.5 years. In this study, we have determined that OMVs from post-flight K. intermedius displayed changes in membrane composition, depending on the location of the samples and some other factors. Membrane lipids such as sterols, fatty acids (FAs), and phospholipids (PLs) were modulated under the Mars-like stressors, and saturated FAs, as well as both short-chain saturated and trans FAs, appeared in the membranes of OMVs shed by both post-UV-illuminated and “dark” bacteria. The relative content of zwitterionic and anionic PLs changed, producing a change in surface properties of outer membranes, thereby resulting in a loss of interaction capability with polynucleotides. The changed composition of membranes promoted a bigger OMV size, which correlated with changes of OMV fitness. Biochemical characterization of the membrane-associated enzymes revealed an increase in their activity (DNAse, dehydrogenase) compared to wild type. Other functional membrane-associated capabilities of OMVs (e.g., proton accumulation, interaction with linear DNA, or synaptosomes) were also altered after exposure to the spaceflight stressors. Despite alterations in membranes, vesicles did not acquire endotoxicity, cytotoxicity, and neurotoxicity. Altogether, our results show that OMVs, originating from rationally selected nonpathogenic Gram-negative bacteria, can be considered as candidates in the design of postbiotics or edible mucosal vaccines for in situ production in extreme environment. Furthermore, these OMVs could also be used as promising delivery vectors for applications in Astromedicine.