An integrated study of ecological, genomic, and metabolic factors in radioresistance of black fungi

Abstract

The high levels of ionizing radiation experienced in extraterrestrial environments and in a few places on Earth make the study of the limits and adaptation of life to it a key concern in the fields of astrobiology, bioprotection and bioremediation. Notably, some microorganisms can survive doses of ionizing radiation that are fatal to most known life-forms, becoming potential models for studying the factors that contribute to withstanding hazardous radiation environments. Among them, meristematic black fungi, constituting a polyphyletic and extremophilic guild that displays the ability to thrive in a wide range of extreme environments, is a very promising group. Previous studies have already demonstrated the extraordinary capacity of one of them in particular, Cryomyces antarcticus MNA-CCFEE515, to tolerate high levels of various forms of ionizing radiation. However, several fundamental questions still need to be answered regarding the overall radioresistance limits of the whole group and the evolutionary and genetic factors underlying this trait. From this perspective, the present study comprehensively defined, for the first time, the radioresistance limits of this group and pointed out the potential adaptive and genomic factors that are responsible for this capacity. To reach this goal, we first further tested the ability of the black fungus C. antarcticus MNA-CCFEE515 to tolerate highly damaging accelerated helium and iron ions, which represent part of the spectrum of the cosmic rays pervading the environment beyond Earth. Successively, the survival limits of the broadest set of black fungi ever tested before were defined, and we demonstrated, for the first time, through a machine learning approach how differences in radioresistance among strains may be the consequence of the adaptation to various environmental factors occurring in their natural habitats. Finally, through a comparative genomic analysis among the strains, we showed that radioresistance is driven by a range of different cellular mechanisms that could be correlated to evolutionary and ecological factors. Altogether, the findings of this study showed radioresistance as a factor strictly associated with the extremotolerance capacity of microorganisms, providing novel insights into the ability of life to survive in extreme conditions on Earth and beyond. Additionally, these results may serve as a foundation for future investigations into the molecular mechanisms that underlie the radioresistance of eukaryotic organisms.