Manganese(III) binding to a pyoverdine siderophore produced by a manganese(II)-oxidizing bacterium

Parker, Dorothy L.; Sposito, Garrison; Tebo, Bradley M.

doi:10.1016/j.gca.2004.05.038

Cited by 127 publications

(104 citation statements)

References 48 publications

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“…First, the putative Mn(II) oxidase is an MCO, a family of enzymes known to be involved in Fe (34) and Cu (55,62) homeostasis and siderophore degradation (30). Second, Mn(III), an intermediate of Mn(II) oxidation (76), is bound by some siderophores with even greater affinity than their intended target, Fe(III); thus, Mn(II) oxidation may influence Fe bioavailability (23,51). Conversely, the formation of Mn oxides is inhibited by siderophores and thus depends on Fe bioavailability (50).…”

Section: Resultsmentioning

confidence: 99%

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Genomic Insights into Mn(II) Oxidation by the Marine Alphaproteobacterium Aurantimonas sp. Strain SI85-9A1

Dick

Podell

Johnson

et al. 2008

Appl Environ Microbiol

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Microbial Mn(II) oxidation has important biogeochemical consequences in marine, freshwater, and terrestrial environments, but many aspects of the physiology and biochemistry of this process remain obscure. Here, we report genomic insights into Mn(II) oxidation by the marine alphaproteobacterium Aurantimonas sp. strain SI85-9A1, isolated from the oxic/anoxic interface of a stratified fjord. The SI85-9A1 genome harbors the genetic potential for metabolic versatility, with genes for organoheterotrophy, methylotrophy, oxidation of sulfur and carbon monoxide, the ability to grow over a wide range of O 2 concentrations (including microaerobic conditions), and the complete Calvin cycle for carbon fixation. Although no growth could be detected under autotrophic conditions with Mn(II) as the sole electron donor, cultures of SI85-9A1 grown on glycerol are dramatically stimulated by addition of Mn(II), suggesting an energetic benefit from Mn(II) oxidation. A putative Mn(II) oxidase is encoded by duplicated multicopper oxidase genes that have a complex evolutionary history including multiple gene duplication, loss, and ancient horizontal transfer events. The Mn(II) oxidase was most abundant in the extracellular fraction, where it cooccurs with a putative hemolysin-type Ca 2؉ -binding peroxidase. Regulatory elements governing the cellular response to Fe and Mn concentration were identified, and 39 targets of these regulators were detected. The putative Mn(II) oxidase genes were not among the predicted targets, indicating that regulation of Mn(II) oxidation is controlled by other factors yet to be identified. Overall, our results provide novel insights into the physiology and biochemistry of Mn(II) oxidation and reveal a genome specialized for life at the oxic/anoxic interface.

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Section: Resultsmentioning

confidence: 99%

“…The siderophore biosynthesis genes are most similar to those of Rhodopseudomonas palustris and are predicted to encode a rhizobactin-like siderophore (41). It will be interesting to determine whether this siderophore has a high affinity for Mn(III) as in other Mn(II)-oxidizing bacteria (23,51).…”

Section: Resultsmentioning

confidence: 99%

Genomic Insights into Mn(II) Oxidation by the Marine Alphaproteobacterium Aurantimonas sp. Strain SI85-9A1

Dick

Podell

Johnson

et al. 2008

Appl Environ Microbiol

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“…Thus, Mn(III) organic complexes produced by bacteria in zones of Mn(II) oxidation may prove to be an important source of this powerful oxidant in many aquatic and terrestrial settings. Mn(III) has also been shown to compete with Fe(III) for complexation by siderophores (16). Speculation has been raised that the production of Mn(III) and the subsequent competition for siderophores may, under Fe-limiting conditions, help a bacterium acquire Fe from a stable complex that it could not use otherwise (4).…”

Section: Resultsmentioning

confidence: 99%

Evidence for the presence of Mn(III) intermediates in the bacterial oxidation of Mn(II)

Webb

Dick

Bargar

et al. 2005

Proc. Natl. Acad. Sci. U.S.A.

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292

199

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Bacterial oxidation of Mn(II) to Mn(IV) is believed to drive the oxidative segment of the global biogeochemical Mn cycle and regulates the concentration of dissolved Mn(II) in the oceanic water column, where it is a critical nutrient for planktonic primary productivity. Mn(II) oxidizing activity is expressed by numerous phylogenetically diverse bacteria and fungi, suggesting that it plays a fundamental and ubiquitous role in the environment. This important redox system is believed to be driven by an enzyme or enzyme complex involving a multicopper oxidase, although the biochemical mechanism has never been conclusively demonstrated. Here, we show that Mn(II) oxidation by spores of the marine Bacillus sp. strain SG-1 is a result of two sequential one-step electron transfer processes, both requiring the putative multicopper oxidase, MnxG, in which Mn(III) is a transient intermediate. A kinetic model of the oxidation pathway is presented, which shows that the Mn(II) to Mn(III) step is the rate-limiting step. Thus, oxidation of Mn(II) appears to involve a unique multicopper oxidase system capable of the overall two-electron oxidation of its substrate. This enzyme system may serve as a source for environmental Mn(III), a strong oxidant and competitor for siderophorebound Fe(III) in nutrient-limited environments. That metabolically dormant spores catalyze an important biogeochemical process intimately linked to the C, N, Fe, and S cycles requires us to rethink the role of spores in the environment.kinetics ͉ multicopper oxidase ͉ spores ͉ x-ray absorption near-edge spectroscopy

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“…One previously reported reason for the reduction of Mn(II) oxidation under iron-limiting conditions is the presence of a Mn(III)-binding siderophore, such as pyoverdine, which has been shown to preferentially bind Mn(III) and retard Mn(IV) oxide formation (29,30). This did not appear to explain our observations, however, as a common siderophore detection assay did not detect the production of any siderophore (indicating that the siderophore level was Ͻ0.8 M) from L. discophora SS-1 under iron-limited conditions.…”

Section: Discussionmentioning

confidence: 99%

Iron Requirement for Mn(II) Oxidation by Leptothrix discophora SS-1

Gheriany¹,

Bocioaga²,

Hay³

et al. 2009

Appl Environ Microbiol

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The biological catalysis of Mn(II) oxidation is thought to be responsible for the formation of most naturally occurring insoluble Mn(III, IV) oxides (40, 41) and consequently plays a key role in the biogeochemical cycling of Mn. The resulting biogenic Mn oxides have high adsorptive capacities for toxic metals (16, 17) and can oxidize both natural organic compounds (38) and organic contaminants (36). The binding of transition metals to biogenic Mn oxides can, in turn, greatly affect the phase distributions and residence times of these transition metals in many natural systems (16,17). An understanding of environmental conditions that favor or inhibit the production of the extracellular enzyme responsible for Mn(II) oxidation will contribute to insight into this important ecological process and is also a prerequisite for the design of any successful technology that uses microorganisms for the production of Mn oxides.A variety of phylogenetically distinct microorganisms are capable of the extracellular oxidation of Mn(II) (5). Based on the presence of conserved predicted amino acid motifs, the genes that encode putative Mn(II)-oxidizing enzymes (mofA in Leptothrix discophora [9], cumA in Pseudomonas putida GB-1 [7], and moxA in Pedomicrobium sp. strain ACM 3067 [33]) are all thought to produce multicopper oxidases. Recently, further support for the role of putative multicopper oxidases in Mn(II) oxidation has come from the recovery and sequencing of peptides excised from Mn(II)-oxidizing bands in polyacrylamide gel analyses of proteins from three Mn(II)-oxidizing Bacillus species (15). Specifically, Mn(II)-oxidizing bands from the exosporia of two of the three Bacillus species tested were shown by tandem mass spectrometric analyses to contain peptides with homology to the predicted C terminus of the putative multicopper Mn(II) oxidase MnxG.Despite this growing body of evidence regarding the role of multicopper oxidases in Mn(II) oxidation, little is known about how the concentrations of different nutrients (e.g., iron, carbon, and nitrogen) or growth conditions such as pH and the oxygen concentration regulate the production of the enzyme(s) which oxidizes Mn(II). Nelson et al. (26) evaluated the minimal growth conditions needed for Mn(II) oxidation and found that the addition of 0.1 M Fe(II) to the defined minimal mineral salt (MMS) medium used for growth was necessary for the complete oxidation of Mn(II) by L. discophora SS-1; however, adding 0.1 M Fe(II) to stationary-phase cells did not allow complete Mn(II) oxidation.In the present study, we grew L. discophora SS-1 in a controlled-reactor system and evaluated the time courses of Mn(II) oxidation and mofA transcript levels in batch cultures of cells with limited and sufficient iron. Parker et al. (30) observed that retarded Mn(IV) formation by iron-starved P. putida is a consequence of the binding of the Mn(III) intermediate (42) to the siderophore pyoverdine. Therefore, siderophore production was also evaluated as part of this research. MATERIALS AND METHODS...

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Manganese(III) binding to a pyoverdine siderophore produced by a manganese(II)-oxidizing bacterium

Cited by 127 publications

References 48 publications

Genomic Insights into Mn(II) Oxidation by the Marine Alphaproteobacterium Aurantimonas sp. Strain SI85-9A1

Genomic Insights into Mn(II) Oxidation by the Marine Alphaproteobacterium Aurantimonas sp. Strain SI85-9A1

Evidence for the presence of Mn(III) intermediates in the bacterial oxidation of Mn(II)

Iron Requirement for Mn(II) Oxidation by Leptothrix discophora SS-1

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