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Background  The extraordinarily resistant bacterium  Deinococcus radiodurans  withstands harsh environmental conditions present in outer space.  Deinococcus radiodurans  was exposed for 1 year outside the International Space Station within Tanpopo orbital mission to investigate microbial survival and space travel. In addition, a ground-based simulation experiment with conditions, mirroring those from low Earth orbit, was performed.    Methods  We monitored  Deinococcus radiodurans  cells during early stage of recovery after low Earth orbit exposure using electron microscopy tools. Furthermore, proteomic, transcriptomic and metabolomic analyses were performed to identify molecular mechanisms responsible for the survival of  Deinococcus radiodurans  in low Earth orbit.    Results   D. radiodurans  cells exposed to low Earth orbit conditions do not exhibit any morphological damage. However, an accumulation of numerous outer-membrane-associated vesicles was observed. On levels of proteins and transcripts, a multi-faceted response was detected to alleviate cell stress. The UvrABC endonuclease excision repair mechanism was triggered to cope with DNA damage. Defense against reactive oxygen species is mirrored by the increased abundance of catalases and is accompanied by the increased abundance of putrescine, which works as reactive oxygen species scavenging molecule. In addition, several proteins and mRNAs, responsible for regulatory and transporting functions showed increased abundances. The decrease in primary metabolites indicates alternations in the energy status, which is needed to repair damaged molecules.    Conclusion  Low Earth orbit induced molecular rearrangements trigger multiple components of metabolic stress response and regulatory networks in exposed microbial cells. Presented results show that the non-sporulating bacterium  Deinococcus radiodurans  survived long-term low Earth orbit exposure if wavelength below 200 nm are not present, which mirrors the UV spectrum of Mars, where CO 2  effectively provides a shield below 190 nm. These results should be considered in the context of planetary protection concerns and the development of new sterilization techniques for future space missions.Video Abstract

Molecular repertoire of Deinococcus radiodurans after 1 year of exposure outside the International Space Station within the Tanpopo mission