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The gram-positive bacterium Deinococcus radiodurans can survive under extreme ionizing radiation environment. This study aims to rationalize the role of redox balance, antioxidant status, and metabolite content on the radiation survival of D. radiodurans. We found that the TrxR inhibitors, i.e., ebselen, auranofin, and epigallocatechin gallate (EGCG) (10 µM) treatment affects the radiation survival of D. radiodurans. The TrxR inhibitors treatment affects the redox status, activities of antioxidant enzymes, increases the intracellular ROS levels and protein carbonylation upon 4 kGy ionizing radiation treatments. Moreover, the alteration in cellular redox status affects the metabolites content of the organism. In addition, we noticed differential metabolomic profiles in sham control, radiation control (4 kGy), and TrxR inhibitors plus radiation-treated D. radiodurans. The TrxR inhibitors plus radiation treated groups exhibit more variation compare to sham control and 4 kGy radiation-exposed D. radiodurans. Further, some novel metabolites can possess the high antioxidant property and involved in vital cellular metabolism were found in sham control and radiation treated cells of D. radiodurans. Thus, the results illustrate the role of intracellular redox status in the survival and metabolomic profile of D. radiodurans. [ABSTRACT FROM AUTHOR]