Biology of extreme radiation resistance: the way of Deinococcus radiodurans

Abstract

The bacterium Deinococcus radiodurans is a champion of extreme radiation resistance that is accounted for by a highly efficient protection against proteome, but not genome, damage. A well-protected functional proteome ensures cell recovery from extensive radiation damage to other cellular constituents by molecular repair and turnover processes, including an efficient repair of disintegrated DNA. Therefore, cell death correlates with radiation-induced protein damage, rather than DNA damage, in both robust and standard species. From the reviewed biology of resistance to radiation and other sources of oxidative damage, we conclude that the impact of protein damage on the maintenance of life has been largely underestimated in biology and medicine.

Figure 1.

Extended synthesis-dependent strand annealing (ESDSA) pathway for reassembly of broken DNA in D. radiodurans. Several genomic copies present in D. radiodurans undergo radiation-induced random DNA double-strand breakage, producing numerous fragments. The end-recessed fragments (step 1) prime synthesis use the homologous regions of partially overlapping fragments as a template (step 2), presumably through a moving D-loop (bracketed intermediate). The strand extension can run to the end of the template, producing fragments with long, newly synthesized (red) single-stranded overhangs (step 3) that can a priori engage in several rounds of extension until they find a complementary partner strand (steps 4 and 5). Hydrogen bonds are indicated only for interfragment associations. Long linear fragments mature into unit-size circular chromosomes by homologous recombination (crossover).

Figure 2.

Single correlation between cell killing and protein carbonylation. A similar correlation is observed for the two bacterial (E. coli and D. radiodurans) and the two animal (bdelloid rotifer Adineta vaga and the worm Caenorhabditis elegans) species of widely different radiation resistance. (Data from Krisko and Radman 2010; Krisko et al. 2012.)

Figure 3.

Correlations between radiation-induced protein carbonylation (filled square), cellular capacity to produce phage λ (open circle), and cell death (filled circle) in E. coli. (A) γ-radiation. (B) UVC radiation. (Data from Krisko and Radman 2010.)