Role of DNA repair pathways in the recovery of a dried, radioresistant cyanobacterium exposed to high-LET radiation: implications for the habitability of Mars

Abstract If life ever appeared on Mars and if it did refuge into sub-superficial environments when surface conditions turned too hostile, then it should have been periodically revived from the frozen, dormant state in order to repair the accumulated damage and reset the survival clock to zero for the next dormant phase. Thus, unravelling how long Earth dormant microorganisms can cope with high-LET radiation mimicking long-term irradiation is fundamental to get insights into the long-term resilience of a dormant microbial life in the Martian subsurface over geological timescales that might have taken advantage of periodically clement conditions that allowed the repair of the accumulated DNA damage. The exposure of dried cells of the radioresistant cyanobacterium Chroococcidiopsis sp. CCMEE 029 to 2 kGy of heavy-ion radiation (Fe ions) did not significantly reduce its survival, although DNA damage was accumulated. Upon rehydration, DNA lesions were repaired as suggested by the over-expression of genes involved in the repair of double strand breaks (DSBs), oxidized bases and apurinic-apyrimidinic sites. Indeed, the monitoring of repair genes upon rehydration suggested a key role of the RecF homologous recombination in repairing DSBs. While the fact that out of the eight genes of the BER system, only one was up-regulated, suggested the absence of DNA lesions generally induced by UV radiation. In conclusion, the non-significantly reduced survival of dried Chroococcidiopsis exposed to 2 kGy of Fe-ion radiation further expanded our appreciation of the resilience of a putative dormant life in the Martian subsurface. Moreover, it is also relevant when searching life on Europa and Enceladus where the radiation environment might critically affect the long-term survival of dormant, frozen life forms.