Variations in Mn(II) speciation among organisms: what makes D. radiodurans different.

Area of Science:

• Biochemistry
• Cell Biology
• Biophysics

Background:

• Manganese is an essential trace element involved in various cellular processes.
• Understanding manganese speciation is crucial for elucidating its biological roles and toxicity.
• Previous studies have not comprehensively compared manganese speciation across diverse organisms like bacteria, yeast, and plants.

Purpose of the Study:

• To investigate and compare the speciation of manganese(II) ions in intact cells of Deinococcus radiodurans, Escherichia coli, Saccharomyces cerevisiae, and Arabidopsis thaliana seeds.
• To identify the primary ligands binding manganese(II) in these organisms.
• To explore the relationship between manganese speciation and the presence of manganese-binding proteins.

Main Methods:

• High-field electron paramagnetic resonance (EPR) spectroscopy was employed to measure manganese(II) speciation.
• Intact cells of D. radiodurans, E. coli, S. cerevisiae, and A. thaliana seeds were analyzed.
• Quantification of different manganese(II) coordination environments and ligand types (water, phosphates, nitrogen) was performed.

Main Results:

• The majority of manganese(II) ions were six-coordinate in all studied organisms.
• Phosphate ligation varied, with monophosphate monoesters dominating in bacteria and yeast, while phytate was prevalent in Arabidopsis seeds.
• Mn(II) was also observed bound to the phosphate backbone of nucleic acids.
• Nitrogen ligation was highest in D. radiodurans and E. coli, attributed to higher concentrations of manganese(II) bound to proteins.
• Manganese superoxide dismutase (MnSOD) was detected only in D. radiodurans, which also showed a unique accumulation of another manganese-containing protein.

Conclusions:

• Manganese(II) speciation is diverse across different organisms, influenced by their unique biochemical compositions.
• The high concentration of protein-bound manganese(II) is a distinctive characteristic of D. radiodurans.
• Understanding these speciation differences can provide insights into manganese's role in cellular protection and function, particularly in extremophiles like D. radiodurans.