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

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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.

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Most cited references 48

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Substrate profile and metal-ion selectivity of human divalent metal-ion transporter-1.

Anthony C Illing, Ali Shawki, Christopher L Cunningham … (2012)

Divalent metal-ion transporter-1 (DMT1) is a H(+)-coupled metal-ion transporter that plays essential roles in iron homeostasis. DMT1 exhibits reactivity (based on evoked currents) with a broad range of metal ions; however, direct measurement of transport is lacking for many of its potential substrates. We performed a comprehensive substrate-profile analysis for human DMT1 expressed in RNA-injected Xenopus oocytes by using radiotracer assays and the continuous measurement of transport by fluorescence with the metal-sensitive PhenGreen SK fluorophore. We provide validation for the use of PhenGreen SK fluorescence quenching as a reporter of cellular metal-ion uptake. We determined metal-ion selectivity under fixed conditions using the voltage clamp. Radiotracer and continuous measurement of transport by fluorescence assays revealed that DMT1 mediates the transport of several metal ions that were ranked in selectivity by using the ratio I(max)/K(0.5) (determined from evoked currents at -70 mV): Cd(2+) > Fe(2+) > Co(2+), Mn(2+) ≫ Zn(2+), Ni(2+), VO(2+). DMT1 expression did not stimulate the transport of Cr(2+), Cr(3+), Cu(+), Cu(2+), Fe(3+), Ga(3+), Hg(2+), or VO(+). (55)Fe(2+) transport was competitively inhibited by Co(2+) and Mn(2+). Zn(2+) only weakly inhibited (55)Fe(2+) transport. Our data reveal that DMT1 selects Fe(2+) over its other physiological substrates and provides a basis for predicting the contribution of DMT1 to intestinal, nasal, and pulmonary absorption of metal ions and their cellular uptake in other tissues. Whereas DMT1 is a likely route of entry for the toxic heavy metal cadmium, and may serve the metabolism of cobalt, manganese, and vanadium, we predict that DMT1 should contribute little if at all to the absorption or uptake of zinc. The conclusion in previous reports that copper is a substrate of DMT1 is not supported.

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Biology of iron- and manganese-depositing bacteria.

W C Ghiorse (1984)

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Battles with iron: manganese in oxidative stress protection.

J Aguirre R, Valeria Culotta (2012)

The redox-active metal manganese plays a key role in cellular adaptation to oxidative stress. As a cofactor for manganese superoxide dismutase or through formation of non-proteinaceous manganese antioxidants, this metal can combat oxidative damage without deleterious side effects of Fenton chemistry. In either case, the antioxidant properties of manganese are vulnerable to iron. Cellular pools of iron can outcompete manganese for binding to manganese superoxide dismutase, and through Fenton chemistry, iron may counteract the benefits of non-proteinaceous manganese antioxidants. In this minireview, we highlight ways in which cells maximize the efficacy of manganese as an antioxidant in the midst of pro-oxidant iron.

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Author and article information

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Adam Driks: Role: Editor

Journal

Journal ID (nlm-ta): PLoS One

Journal ID (iso-abbrev): PLoS ONE

Journal ID (publisher-id): plos

Journal ID (pmc): plosone

Title: PLoS ONE

Publisher: Public Library of Science (San Francisco, USA )

ISSN (Electronic): 1932-6203

Publication date Collection: 2013

Publication date (Electronic): 17 October 2013

Volume: 8

Issue: 10

Electronic Location Identifier: e77835

Affiliations

[1]Center for Applied Biotechnology Studies, Department of Biological Science, California State University Fullerton, Fullerton, California, United States of America

Loyola University Medical Center, United States of America

Author notes

* E-mail: hajohnson@ 123456fullerton.edu

Competing Interests: The authors have declared that no competing interests exist.

Conceived and designed the experiments: AB HAJ. Performed the experiments: AB VC JD AN SH VH PJ FE HAJ. Analyzed the data: AB VC JD AN SH VH PJ FE HAJ. Contributed reagents/materials/analysis tools: AB VC JD AN SH PJ FE HAJ. Wrote the manuscript: AB VC JD AN SH VH PJ FE HAJ.

Article

Publisher ID: PONE-D-13-29854

DOI: 10.1371/journal.pone.0077835

PMC ID: 3798386

SO-VID: e966adad-efbd-411c-9203-c13719433c2f

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This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

History

Date received : 19 July 2013

Date accepted : 11 September 2013

Funding

Funding for this project was provided by Research Corporation ( http://www.rescorp.org), the National Science Foundation (MCB-1021187), California State University Fullerton Associated Students, Inc research grants to JD, AB, VC, AN, SH, VH, FE, and PJ; and a State Mini Grant to HAJ. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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

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Most cited references 48

Substrate profile and metal-ion selectivity of human divalent metal-ion transporter-1.

Biology of iron- and manganese-depositing bacteria.

Battles with iron: manganese in oxidative stress protection.

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