Role of Mn²⁺and Compatible Solutes in the Radiation Resistance of Thermophilic Bacteria and Archaea

Abstract

Radiation-resistant bacteria have garnered a great deal of attention from scientists seeking to expose the mechanisms underlying their incredible survival abilities. Recent analyses showed that the resistance to ionizing radiation (IR) in the archaeon Halobacterium salinarum is dependent upon Mn-antioxidant complexes responsible for the scavenging of reactive oxygen species (ROS) generated by radiation. Here we examined the role of the compatible solutes trehalose, mannosylglycerate, and di-myo-inositol phosphate in the radiation resistance of aerobic and anaerobic thermophiles. We found that the IR resistance of the thermophilic bacteria Rubrobacter xylanophilus and Rubrobacter radiotolerans was highly correlated to the accumulation of high intracellular concentration of trehalose in association with Mn, supporting the model of Mn2+-dependent ROS scavenging in the aerobes. In contrast, the hyperthermophilic archaea Thermococcus gammatolerans and Pyrococcus furiosus did not contain significant amounts of intracellular Mn, and we found no significant antioxidant activity from mannosylglycerate and di-myo-inositol phosphate in vitro. We therefore propose that the low levels of IR-generated ROS under anaerobic conditions combined with highly constitutively expressed detoxification systems in these anaerobes are key to their radiation resistance and circumvent the need for the accumulation of Mn-antioxidant complexes in the cell.

Protective effect of trehalose-loaded liposomes against UVB-induced photodamage in human keratinocytes

“…In turn, intracellular trehalose may decrease PC by stabilizing proteins and acting as a molecular chaperone (21). In this regard, it is noteworthy that extremophilic bacteria, which are characterized by the ability to resist large amounts of UV radiation, have high intracellular levels of trehalose combined with manganese ions (19,22). The in vitro results of the present study also showed that trehalose may reduce UVB-induced DNA damage to a greater extent than other cytoprotective molecules.…”

“…Trehalose, a naturally occurring non-reducing disaccharide consisting of two glucose units, is found in a large variety of organisms, including bacteria, fungi and invertebrate animals, where it may serve as a stress protectant or resilience factor (21,22). Extremophile bacteria have the ability to achieve a significant UV-radiation resistance via simple non-enzymatic antioxidant mechanisms consisting of trehalose complexed with manganese ions (22).…”

“…Extremophile bacteria have the ability to achieve a significant UV-radiation resistance via simple non-enzymatic antioxidant mechanisms consisting of trehalose complexed with manganese ions (22). Trehalose is known to act as a major protein stabilizer and its topical application to the eye reduces UVB-induced corneal damage (19).…”

Responses of Mn2+speciation inDeinococcus radioduransandEscherichia colito γ-radiation by advanced paramagnetic resonance methods

“…We infer that E. coli is highly susceptible to radiation-induced ROS because it lacks an adequate supply of LMW Mn antioxidants. •-) and hydrogen peroxide (H 2 O 2 ), in addition to enzymatic mechanisms for antioxidant defense (1)(2)(3)(4)(5)(6)(7)(8)(9)(10)(11)(12)(13)(14). The role of nonenzymatic defenses based on Mn is established by such findings as (i) ROS-scavenging enzymes are completely dispensable for extreme radiation resistance in Mn-accumulating prokaryotes (1,2,(6)(7)(8)11) and (ii) limiting Mn 2+ accumulation renders Deinococcus radiodurans cells radiation-sensitive and highly susceptible to protein oxidation (1,9).…”

“…The role of nonenzymatic defenses based on Mn is established by such findings as (i) ROS-scavenging enzymes are completely dispensable for extreme radiation resistance in Mn-accumulating prokaryotes (1,2,(6)(7)(8)11) and (ii) limiting Mn 2+ accumulation renders Deinococcus radiodurans cells radiation-sensitive and highly susceptible to protein oxidation (1,9). This nonenzymatic, Mndependent artillery for combating oxidative stress is manifested in cells that accumulate Mn 2+ together with various inorganic and organic ligands (2,11,13,14), and has been best studied in the extremely radiation-resistant bacterium D. radiodurans (8). D. radiodurans is capable of surviving huge doses of γ-rays (12,000 Gy): 20 times greater than the bacterium Escherichia coli, and 3,000 times greater than most human cells in liquid culture (2).…”