Exposure of Deinococcus Radiodurans to 1126 Days in low Earth orbit: Molecular Patterns of Recovery after Tanpopo space Mission
Background: The International Space Station is an orbiting laboratory for microbial research in space, where microorganisms can be exposed to multiple extremes. Dehydrated cell clusters of extremophilic bacterium Deinococcus radiodurans have survived 3-year exposure outside the International Space Station in frames of the Tanpopo mission. We investigated the robust molecular machinery of Deinococcus radiodurans involved in its recovery after long-term space travel. Methods: The space-exposed and ground control cells of Deinococcus radiodurans were recovered in a complex medium for 5 and 15 h and investigated using integrative –omics techniques combined with electron microscopy tools. Consolidative transcriptomic, proteomic, and metabolomic analyses were performed to investigate molecular kinetics of cell recovery after 3-year exposure to low Earth orbit. Results: Ultrastructure analysis showed that Deinococcus radiodurans cells remained intact after low Earth orbit exposure for 3 years. Multiscale molecular analysis revealed significant alterations in response to long-term space travel. Key adaptations included upregulated DNA repair genes,stress response regulators, and oxidative stress scavenging enzymes. Proteins associated with transmembrane processes, cell division, and stress defence were also upregulated. Metabolomic analysis showed that only a few amino acids, sugars, and specific metabolites were more abundant after low Earth orbit exposure, suggesting energy conservation for molecular repair and regulation.Primordial stress molecule spermidine is also involved in cells recovery, helping combat the stress factors after space travel. Conclusion: Comparative –omics profile of extracted mRNA, proteins and metabolites allowed us to propose a multiscale dynamic molecular response of Deinococcus radiodurans after 3 years of space exposure. The kinetic profile with 2 timepoints during post-exposure analysis enabled the identification of foreground molecular targets employed by this microorganism in recovery after a space journey. Altogether, a multi-omics approach towards space-exposed cells revealed a strong focus on repair mechanisms, stress defence, and the utilization of external resources during the initial recovery phase. These findings expand our understanding of the molecular mechanisms employed by extremophiles to survive in space, providing implications for astrobiology and future space exploration.