Experimental evolution of extremophile resistance to ionizing radiation

Abstract

A growing number of known species possess a remarkable characteristic - extreme resistance to the effects of ionizing radiation (IR). This review examines our current understanding of how organisms can adapt to and survive exposure to IR, one of the most toxic stressors known. The study of natural extremophiles such as Deinococcus radiodurans has revealed much. However, the evolution of Deinococcus was not driven by IR. Another approach, pioneered by Evelyn Witkin in 1946, is to utilize experimental evolution. Contributions to the IR-resistance phenotype affect multiple aspects of cell physiology, including DNA repair, removal of reactive oxygen species, the structure and packaging of DNA and the cell itself, and repair of iron-sulfur centers. Based on progress to date, we overview the diversity of mechanisms that can contribute to biological IR resistance arising as a result of either natural or experimental evolution.

Keywords: DNA repair; evolution; genomics; ionizing radiation; reactive oxygen species.

Figure 1.. Key figure

Trends in experimental evolution of ionizing radiation (IR) resistance in Escherichia coli (A) Loss of the e14 prophage, and mutations affecting RNA polymerase (RNAP), DNA repair, Fe-S cluster repair, ATP synthesis, and cadaverine biosynthesis, have all been confirmed to enhance IR resistance in lineage IR9 [–88]. Where applicable, these general pathways to IR resistance have been highlighted in the evolving lineages (B) IR10, (C) IR11, and (D) IR12. In general, mutations affecting RNAP and DNA repair are common to all four lineages, especially before round 50 of selection. Since that point, genetic parallelism has given way to significant clonal interference and lineage-specific mechanisms of adaptation (e.g., a major variant of SufD and CadA in IR9 but in no other lineage). In each evolving lineage there are sweeps driven by currently unknown factors.

Figure 2.

Radioresistant E. coli generated in separate evolution experiments exhibit different mutation spectra. Single-nucleotide polymorphisms appear at different frequencies in radioresistant E. coli isolates selected for using a Linac electron beam (IR isolates) [87] compared to those generated with a ⁶⁰Co gamma-ray source (CB isolates) [14]. Transversion mutations (i.e., purine to pyrimidine) are more common in the isolates exposed to electron-beam ionizing radiation.