Ringlike Structure of the Deinococcus radiodurans Genome: A Key to Radioresistance?

Abstract

The bacterium Deinococcus radiodurans survives ionizing irradiation and other DNA-damaging assaults at doses that are lethal to all other organisms. How D. radiodurans accurately reconstructs its genome from hundreds of radiation-generated fragments in the absence of an intact template is unknown. Here we show that the D. radiodurans genome assumes an unusual toroidal morphology that may contribute to its radioresistance. We propose that, because of restricted diffusion within the tightly packed and laterally ordered DNA toroids, radiation-generated free DNA ends are held together, which may facilitate template-independent yet error-free joining of DNA breaks.

Underlying Structural Aspects of DNA Repair

“…Within the tightly packed ringlike DNA morphology, ends of DNA fragments generated by DSBs are continuously held in close physical proximity, due to the restricted diffusion that is imposed by the tight packaging. We propose that the physical proximity of DNA ends enables accurate repair of DSBs in a templateindependent pathway, which is likely to proceed through nonhomologous DNA end-joining, as well as via homologous annealing of protruding DNA single strands, which might be present at the ends of DNA fragments [3,4,6].The notion that nonhomologous DNA end-joining within tightly-packed toroidal chromatin structures is operative in bacteria is substantiated by biochemical studies. DNA-binding proteins such as HU in D. radiodurans and SASP in bacterial spores were shown to specifically stabilize toroidal DNA structures both in-vitro and within bacterial cells.…”

“…Consequently, germinating spores lack the template required for homologous recombination-mediated accurate repair of DSBs. These and other considerations imply that the unique ability of both D. radiodurans and germinating spores to effectively repair double strand DNA breaks must depend upon novel strategies, which do not rely on RecA-dependent homologous recombination [2].Structural studies conducted on D. radiodurans demonstrate that the chromatin in this organism adopts a ring-like toroidal morphology [3]. A similar toroidal organization of the chromatin is detected in mature as well as in germinating bacterial spores [4,5].…”

Coherent X-ray diffractive imaging on the single-cell-level of microbial samples

“…3.29). The images of the sample regions A and B show typical shapes of D. radiodurans aggregates, as known from light and electron microscopy [77,169,342] and a previous ptychographic study [97]). Importantly, scanning di raction with the four observables transmission, phase shift DPC-x, DPC-y and dark eld allows for fast, robust visualisation of biological cells without staining and with the additional bene t of a large FOV that can be easily adapted.…”

“…As a hypothesis, it has been proposed that protein oxidation caused by reactive oxygen species such as hydroxyl radicals (OH ) that arise due to radiolysis of H 2 O is sign cantly reduced by the manganese content [56]. A somewhat controversial, discussion has been raised by indications that a toroidal shape of the nucleoid plays a role for its resistance to ionizing radiation [169] (cf. [202,203,342] for discussion).…”

“…The bacterium is nonpathogenic, nonmotile, red-pigmented, Grampositive and well-known due to its outstanding resistance to ionizing-radiation and oxidative stress [7,51,55,56,164,169,180,184,277]. For instance, D. radiodurans R1 reaches a D 10 value of 10 kGy [51], i.e.…”