Manganese (Mn) Oxidation Increases Intracellular Mn in Pseudomonas putida GB-1

Abstract

Bacterial manganese (Mn) oxidation plays an important role in the global biogeochemical cycling of Mn and other compounds, and the diversity and prevalence of Mn oxidizers have been well established. Despite many hypotheses of why these bacteria may oxidize Mn, the physiological reasons remain elusive. Intracellular Mn levels were determined for Pseudomonas putida GB-1 grown in the presence or absence of Mn by inductively coupled plasma mass spectrometry (ICP-MS). Mn oxidizing wild type P. putida GB-1 had higher intracellular Mn than non Mn oxidizing mutants grown under the same conditions. P. putida GB-1 had a 5 fold increase in intracellular Mn compared to the non Mn oxidizing mutant P. putida GB-1-007 and a 59 fold increase in intracellular Mn compared to P. putida GB-1 ∆2665 ∆2447. The intracellular Mn is primarily associated with the less than 3 kDa fraction, suggesting it is not bound to protein. Protein oxidation levels in Mn oxidizing and non oxidizing cultures were relatively similar, yet Mn oxidation did increase survival of P. putida GB-1 when oxidatively stressed. This study is the first to link Mn oxidation to Mn homeostasis and oxidative stress protection.

Comparative proteomics of Mn(II)‐oxidizing and non‐oxidizing Roseobacter clade bacteria reveal an operative manganese transport system but minimal Mn(II)‐induced expression of manganese oxidation and antioxidant enzymes

“…This is interesting to note, considering that both bacteria produce extracellular superoxide (Diaz et al ., ) and Mn(II) can scavenge superoxide (Archibald and Fridovich, ; Barnese et al ., ; Hansard et al ., ). Further, a recent study has shown a connection between intracellular Mn(II) and oxidative stress in another Mn(II) oxidizing bacterium, Pseudomonas putida GB‐1 (Banh et al ., ).…”

Identification of a Third Mn(II) Oxidase Enzyme in Pseudomonas putida GB-1

“…What function does Mn(II) oxidation play in the bacterial community such that the cost of secreting large oxidase enzymes is evolutionarily affordable? Mn(II) oxidation has been shown to protect P. putida GB-1 from hydrogen peroxide (11). In the closely related plant-beneficial strain P. putida KT2440, deletion of the mopA homolog PP2561 resulted in increased sensitivity to compounds like tert butyl hydroperoxide (43), supporting a role for Mn(II) oxidation in the oxidative stress response.…”

“…The oxidation reaction is thermodynamically favorable, raising the possibility that bacteria could derive energy from Mn(II) oxidation (10). Recent studies have also shown that Mn(II)-oxidizing bacteria exhibit increased resistance to the reactive oxygen species hydrogen peroxide (11). Nonetheless, the physiological function of bacterial Mn(II) oxidation remains unclear.…”

Identification of Mn(II)-Oxidizing Bacteria from a Low-pH Contaminated Former Uranium Mine

“…Although Mn(IV) formation could generate energy for organisms, this has not been definitively shown for any organism (4,5). However, Mn oxidation was shown to increase the survival of Pseudomonas putida GB-1 in the presence of reactive oxygen species (ROS) (18). In addition, Mn oxidation has been speculated to provide other advantages to the cell, such as abiotic oxidation of refractory organic matter by Mn oxides (3) or controlling the availability of toxic metal ions (2,3,19).…”