DNA Repair: Lessons from the Evolution of Ionizing- Radiation-Resistant Prokaryotes – Fact and Theory

Abstract

At the outset, I believe that the concept of ionizing-radiation (IR) resistance needs to be clarified in a tangible manner for readers of this chapter. I propose the following general definition adopted in a previous paper (Sghaier et al., 2008): An ionizing-radiation-resistant prokaryotes (IRRP) is any vegetative prokaryote that can thrive after exposure to high, acute IR (generally, with a D10 value the dose necessary to effect a 90% reduction in Colony Forming Units greater than 1 kGy) using efficient physiological, genetic and proteic protection and repair mechanisms to fully amend its DNA DSBs. IR resistance has been observed in a broad range of prokaryotic groups (Kopylov et al., 1993), including hyperthermophilic Archaea (P. abyssi, P. furiosus, Thermococcus marinus, Thermococcus radiotolerans and Thermococcus gammatolerans) (DiRuggiero et al., 1997; Jolivet et al., 2003a; Jolivet et al., 2003b; Jolivet et al., 2004), halophilic Archaea (Halobacterium sp.) (Kottemann et al., 2005), the Deinococcus-Thermus group (many Deinococcus sp. and Truepera radiovictrix) (Albuquerque et al., 2005), Actinobacteria (Rubrobacter radiotolerans, Rubrobacter xylanophilus and Kineococcus radiotolerans) (Yoshinaka et al., 1973; Ferreira et al., 1999; Phillips et al., 2002; Chen et al., 2004), Proteobacteria (Methylobacterium radiotolerans and Acinetobacter radioresistens) (Ito and Iizuka, 1971; Nishimura et al., 1994), Cyanobacteria (Chroococcidiopsis sp.) (Billi et al., 2000), and Sphingobacteria (Hymenobacter actinosclerus) (Collins et al., 2000). However, with the exception of Deinococcus and Pyrococcus, very little information is available regarding the mechanisms of IR resistance and comparative genomics in the above-mentioned prokaryotes. D. radiodurans is the current gold-medallist of IR resistance among prokaryotes with a completely sequenced genome (Liolios et al., 2006; Liolios et al., 2010), and can amend more than 100 DSBs per chromosome, induced by IR, without loss of viability (Moseley, 1983; White et al., 1999). After breaking of its 3.2 Mb genome into 20−30 kb pieces by a high dose of IR, D. radiodurans fascinatingly reassembles its genome such that 3 hr later fully restructured nonrearranged chromosomes are present (Galhardo and Rosenberg, 2009). Nine interrelated explanations for the extreme IR resistance of D. radiodurans have been proposed: (i) the binding of IrrI (DR0171) to genomic repeat sequences that might prevent exhaustive chromosomal degradation after IR exposure irr for IR resistance (Udupa et al., 1994), (ii) the