Responses of Mn2+ speciation in Deinococcus radiodurans and Escherichia coli to γ-radiation by advanced paramagnetic resonance methods. Proc Natl Acad Sci U S A 2013 Apr 09;110(15):5945-50
Date
03/29/2013Pubmed ID
23536297Pubmed Central ID
PMC3625348DOI
10.1073/pnas.1303376110Scopus ID
2-s2.0-84876040028 (requires institutional sign-in at Scopus site) 66 CitationsAbstract
The remarkable ability of bacterium Deinococcus radiodurans to survive extreme doses of γ-rays (12,000 Gy), 20 times greater than Escherichia coli, is undiminished by loss of Mn-dependent superoxide dismutase (SodA). D. radiodurans radiation resistance is attributed to the accumulation of low-molecular-weight (LMW) "antioxidant" Mn(2+)-metabolite complexes that protect essential enzymes from oxidative damage. However, in vivo information about such complexes within D. radiodurans cells is lacking, and the idea that they can supplant reactive-oxygen-species (ROS)-scavenging enzymes remains controversial. In this report, measurements by advanced paramagnetic resonance techniques [electron-spin-echo (ESE)-EPR/electron nuclear double resonance/ESE envelope modulation (ESEEM)] reveal differential details of the in vivo Mn(2+) speciation in D. radiodurans and E. coli cells and their responses to 10 kGy γ-irradiation. The Mn(2+) of D. radiodurans exists predominantly as LMW complexes with nitrogenous metabolites and orthophosphate, with negligible EPR signal from Mn(2+) of SodA. Thus, the extreme radiation resistance of D. radiodurans cells cannot be attributed to SodA. Correspondingly, 10 kGy irradiation causes no change in D. radiodurans Mn(2+) speciation, despite the paucity of holo-SodA. In contrast, the EPR signal of E. coli is dominated by signals from low-symmetry enzyme sites such as that of SodA, with a minority pool of LMW Mn(2+) complexes that show negligible coordination by nitrogenous metabolites. Nonetheless, irradiation of E. coli majorly changes LMW Mn(2+) speciation, with extensive binding of nitrogenous ligands created by irradiation. We infer that E. coli is highly susceptible to radiation-induced ROS because it lacks an adequate supply of LMW Mn antioxidants.
Author List
Sharma A, Gaidamakova EK, Matrosova VY, Bennett B, Daly MJ, Hoffman BMAuthor
Brian Bennett D.Phil. Professor and Chair in the Physics department at Marquette UniversityMESH terms used to index this publication - Major topics in bold
AntioxidantsBacterial Proteins
Deinococcus
Electron Spin Resonance Spectroscopy
Escherichia coli
Gamma Rays
Ligands
Manganese
Reactive Oxygen Species
Spectrophotometry
Superoxide Dismutase