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 Curtobacterium aetherium 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 C. aetherium 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 C. aetherium. 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, C. aetherium can modulate its metabolism through transcriptional regulation at very low moisture levels (Xw < 0.25 g H2O per gram dry weight). Uncovering the genetic underpinnings of desiccation and UVR resistance in C. aetherium provides new insights into how bacterial DNA repair and antioxidant mechanisms function to exhibit traits at the extreme ends of phenotypic distributions.
Keywords: DNA repair; UV radiation; bioaerosols; desiccation; oxidative stress; stratosphere.