The Genetic Determinants of Extreme UV Radiation and Desiccation Tolerance in a Bacterium Recovered from the Stratosphere

Microbes that survive transport to and in the stratosphere endure extremes of low temperature, atmospheric pressure, and relative humidity, as well as high fluxes in ultraviolet radiation (UVR). The high atmosphere thus provides an ideal environment to explore the genetic and physiological determinants conveying high tolerance to desiccation and UVR. In this study, we examined <i>Curtobacterium aetherium</i> L6-1, an actinobacterium obtained from stratospheric aerosol sampling that displays high resistance to desiccation and UVR. We found that its phylogenetic relatives are resistant to desiccation, but only <i>C. aetherium</i> displayed a high tolerance to UVR. Comparative genome analysis and directed evolution experiments implicated genes encoding photolyase, DNA nucleases and helicases, and catalases as responsible for UVR resistance in <i>C. aetherium</i>. Differential gene expression analysis revealed the upregulation of DNA repair and stress response mechanisms when cells were exposed to UVR, while genes encoding sugar transporters, sugar metabolism enzymes, and antioxidants were induced upon desiccation. Based on changes in gene expression as a function of water content, <i>C. aetherium</i> can modulate its metabolism through transcriptional regulation at very low moisture levels (<i>X_w</i> < 0.25 g H₂O per gram dry weight). Uncovering the genetic underpinnings of desiccation and UVR resistance in <i>C. aetherium</i> provides new insights into how bacterial DNA repair and antioxidant mechanisms function to exhibit traits at the extreme ends of phenotypic distributions.