Biology of Extreme Radiation Resistance: The Way of Deinococcus radiodurans

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.Several recent reviews comprehensively present the extraordinary bacterium Deinococcus radiodurans, best known for its biological robustness involving an extremely efficient DNA repair system (Cox and Battista 2005; Blasius et al. 2008; Daly 2009; Slade and Radman 2011). The aim of this short review of the biology of D. radiodurans is to single out a general concept of the primacy of biological function (proteome) over information (genome) in the maintenance of life. A cell dies when its vital functions performed by the proteome cease, for example, because of the direct loss of proteome functionality or via the loss of membrane integrity, whereas genome integrity is required (in addition to an active proteome) for the perpetuation of cells that have survived. But survival itself depends primarily on the proteome rather than the genome. A cell that instantly loses its genome can function for some time, unlike one that loses its proteome. In other words, the proteome sustains and maintains life, whereas the genome ensures the perpetuation of life by renewing the proteome, a process contingent on a preexisting proteome that repairs, replicates, and expresses the genome. In addition to the functional integrity of the proteome, small metabolites and other cofactors for catalysis and protein interactions are equally important for proteome functionality. However, chemical damage to cofactors is not a likely primary bottleneck in survival because of their high molar concentrations, compared with proteins. And, finally, it is the proteome that synthesizes metabolites and imports vital metal cofactors and ions. Although obvious, the concept that the prime target in cell degeneracy and death is proteome activity—ensuring all vital functions including genome integrity—is conspicuously absent in biological and medical sciences. This overview of the biology of a prokaryotic cell that survives conditions lethal to other species is to define and elaborate a general concept of sustainability of life that applies to all living cells.