Responses of Mn²⁺ Speciation in Deinococcus radiodurans and Escherichia coli to γ-Radiation by Advanced Paramagnetic Resonance Methods

Authors

Ajay Sharma, Northwestern University
Elena K. Gaidamakova, Uniformed Services University of the Health Sciences
Vera Y. Matrosova, Uniformed Services University of the Health Sciences
Brian Bennett, Marquette UniversityFollow
Michael J. Daly, Uniformed Services University of the Health Sciences
Brian M. Hoffman, Northwestern University

Document Type

Article

Language

eng

Format of Original

6 p.

Publication Date

4-9-2013

Publisher

National Academy of Sciences

Source Publication

Proceedings of the National Academy of Sciences

Source ISSN

0027-8424

Original Item ID

doi: 10.1073/pnas.1303376110

Abstract

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” Mn²⁺–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 Mn²⁺ speciation in D. radiodurans and E. coli cells and their responses to 10 kGy γ-irradiation. The Mn²⁺ of D. radiodurans exists predominantly as LMW complexes with nitrogenous metabolites and orthophosphate, with negligible EPR signal from Mn²⁺ 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 Mn²⁺ 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 Mn²⁺ complexes that show negligible coordination by nitrogenous metabolites. Nonetheless, irradiation of E. coli majorly changes LMW Mn²⁺ 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.

Comments

Accepted version. Proceedings of the National Academy of Sciences, Vol. 110, No. 15 (April 9, 2013): 5945-5950. DOI. © 2013 National Academy of Sciences. Used with permission.

Brian Bennett was affiliated with the Medical College of Wisconsin at the time of publication.

Recommended Citation

Sharma, Ajay; Gaidamakova, Elena K.; Matrosova, Vera Y.; Bennett, Brian; Daly, Michael J.; and Hoffman, Brian M., "Responses of Mn²⁺ Speciation in Deinococcus radiodurans and Escherichia coli to γ-Radiation by Advanced Paramagnetic Resonance Methods" (2013). Physics Faculty Research and Publications. 48.
https://epublications.marquette.edu/physics_fac/48