Trends in Microbiology
Volume 13, Issue 9, September 2005, Pages 421-428
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Geomicrobiology of manganese(II) oxidation

https://doi.org/10.1016/j.tim.2005.07.009Get rights and content

Mn(II)-oxidizing microbes have an integral role in the biogeochemical cycling of manganese, iron, nitrogen, carbon, sulfur, and several nutrients and trace metals. There is great interest in mechanistically understanding these cycles and defining the importance of Mn(II)-oxidizing bacteria in modern and ancient geochemical environments. Linking Mn(II) oxidation to cellular function, although still enigmatic, continues to drive efforts to characterize manganese biomineralization. Recently, complexed-Mn(III) has been shown to be a transient intermediate in Mn(II) oxidation to Mn(IV), suggesting that the reaction might involve a unique multicopper oxidase system capable of a two-electron oxidation of the substrate. In biogenic and abiotic synthesis experiments, the application of synchrotron-based X-ray scattering and spectroscopic techniques has significantly increased our understanding of the oxidation state and relatively amorphous structure (i.e. δ–MnO2-like) of biogenic oxides, providing a new blueprint for the structural signature of biogenic Mn oxides.

Section snippets

Dynamics of Mn biogeochemistry

Manganese (Mn) (II)-oxidizing microorganisms, primarily bacteria and fungi, accelerate the rate of Mn biomineralization several orders of magnitude faster than either abiotic catalysis on mineral surfaces or homogeneous oxygenation in aqueous solution [1]. This biogeochemical process has gained much attention in recent years because Mn(III,IV) oxide minerals are abundant in terrestrial and marine environments. Serving as major sources or sinks for bioavailable Mn, these Mn oxide minerals affect

Why do Mn(II)-oxidizing bacteria oxidize Mn(II)?

Although bacterial Mn(II) oxidation is widespread, we know little about why bacteria oxidize Mn(II). Indeed, Mn(II) oxidation might be an ‘accidental’ occurrence, the result of nonspecific interactions with cellular or extracellular products. It has also been suggested that rather than serving some explicit biological role, metal oxidation in some species might be an evolutionary holdover that no longer has physiological relevance [5]. Yet, because so many different bacteria oxidize Mn(II), and

Which bacteria oxidize Mn(II)?

Mn(II)-oxidizing bacteria have been identified in a growing number of divergent phylogenetic lineages in the bacterial domain, such as Firmicutes, Proteobacteria and Actinobacteria (Figure 1). This broad phylogenetic diversity mirrors the physiological diversity of Mn(II)-oxidizing bacteria, as demonstrated by the well-studied model organisms: the Gram positive spore-forming Bacillus sp. strain SG1 [13], the γ-proteobacteria Pseudomonas putida MnB1 and GB-1 [14], and the β-proteobacterium

How do bacteria oxidize Mn(II)?

The biochemical mechanism of Mn(II) oxidation has not yet been described because neither native purification nor heterologous overexpression of putative Mn(II) oxidases has been successful to date. However, numerous details of a regulated, functional pathway have emerged. Multicopper oxidase (MCO)-type enzymes have an integral role in Mn(II) oxidation in diverse species, and genetic studies indicate that the site of Mn(II) oxidation in vegetative cells, as was shown with Bacillus sp. strain SG1

What is the biogeochemical importance of Mn oxidation?

Recent field studies focused on Mn oxide recycling in the Orca Basin [36], the Black Sea [37] and acid-mine drainage systems [38] have highlighted the fact that net geochemical fluxes and rates of element cycling are mechanistically linked to Mn(II) oxidation. However, despite new information on the diversity of Mn(II)-oxidizing bacteria and the molecular mechanisms likely to be involved in Mn(II) oxidation, factors controlling the distribution, activity and biochemical function of

Acknowledgements

We gratefully acknowledge support from the National Science Foundation: CRAEMS (Collaborative Research Activities in Environmental Molecular Science) grant CHE-0089208 (see http://mnbiooxides.ucsd.edu/) and our collaborators John Bargar, Garrison Sposito and Tom Spiro, who have greatly influenced our thinking on bacterial Mn(II) oxidation. We appreciate the critical comments of five anonymous reviewers. We also acknowledge other funding from NSF (CHE-9910572, MCB-0422232; MCB-0348668;

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    Address as of 1 September, 2005: OGI School of Science and Engineering, Oregon Health and Science University, 20000 NW Walker Road., Beaverton, OR 97006, USA ([email protected]).

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