Crucial Roles of Carotenoids as Bacterial Endogenous Defense System for Bacterial Radioresistance of Deinococcus radiodurans

Abstract

BackgroundThe central dogma of radiation biology is that the cytotoxic and mutagenic effects of radiation are principally the result of biological macromolecules (DNA, RNA, polysaccharides, proteins and lipids) damage caused during the course of irradiation. Previous studies on the radioresistance of the extremely radiation-resistant red-carotenoid-pigmented bacterium Deinococcus radiodurans have been focused on DNA repair system. However, relative little is known about the biochemical basis of the extraordinary recovery capacity of D. radiodurans for ionizing radiation and can include hundreds of DNA double-strand breaks.Methodology/Principal FindingsHere we identified a novel carotenoid in D. radiodurans as ((all-E)-1’-hydroxy-3’,4’-didehydro-1’,2’,2,3-quahydro-β,ψ-carotene-4-one-1) and characterized the intracellular distribution of carotenoids. Following exposure to ionizing radiation, the wild-type parent of D. radiodurans survived much higher compared with radiation-sensitive colorless mutants screened by 60Co irradiation and by knockout of crtB or crtI genes for the carotenoid biosynthesis. Electron paramagnetic resonance spectroscopy analysis showed that two carotenoid can effectively scavenge radicals including superoxide anion (O2.−) and hydroxyl radical (.OH). Consistent results showing the substantial antioxidant abilities of the two carotenoids were obtained by UV-induction of bacteriophage λ method in vivo, and the detectable reaction potentials of two carotenoids with nitric oxide (NO) evaluated by ultraviolet-visible near-infrared ray (UV/vis/NIR) spectra assay.Conclusions/SignificanceOur findings support the idea that the degree of bacterial radioresistance of D. radiodurans is partly related to the levels of carotenoids in the cells. Carotenoids, as an important member of the structural and non-structural components of the cells, are endogenous scavengers of reactive oxygen species and can effectively quench radicals generated during irradiation. The current work suggests that carotenoids play a previously unrecognized protection role in the endogenous defense System (EDS) that facilitates the recovery from radiation injury. And we propose a complete model to elucidate the mechanisms of extreme radioresistance in this remarkable bacterium.