Trends in Microbiology
Geomicrobiology of manganese(II) oxidation
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;
References (59)
Characterization of the manganese oxide produced by Pseudomonas putida strain MnB1
Geochim. Cosmochim. Acta
(2003)How radiation kills cells: survival of Deinococcus radiodurans and Shewanella oneidensis under oxidative stress
FEMS Microbiol. Rev.
(2005)The crystal structure of manganese peroxidase from Phanerochaete chrysosporium at 2.06-A resolution
J. Biol. Chem.
(1994)Manganese(III) binding to a pyoverdine siderophore produced by a manganese(II)-oxidizing bacterium
Geochim. Cosmochim. Acta
(2004)Solid phases in the cycling of manganese in eutrophic lakes: new insights from EXAFS spectroscopy
Geochim. Cosmochim. Acta
(1997)Mn, Fe, Zn, and As speciation in a fast-growing ferromanganese marine nodule
Geochim. Cosmochim. Acta
(2004)Structure of heavy metal sorbed birnessite. Part III: results from powder and polarized extended X-ray absorption fine structure spectroscopy
Geochim. Cosmochim. Acta
(2002)Enzymatic formation of manganese oxides by an Acremonium-like hyphomycete fungus, strain KR21-2
FEMS Microbiol. Ecol.
(2004)Biogeochemistry of manganese oxide coatings on pebble surfaces in the Kikukawa River System, Shizuoka, Japan
Appl. Geochem.
(2003)- et al.
Novel enzymatic oxidation of Mn2+ to Mn3+ catalyzed by a fungal laccase
FEBS Lett.
(1999)
Biogenic manganese oxides: properties and mechanisms of formation
Annu. Rev. Earth Planet. Sci.
Biotic and abiotic products of Mn(II) oxidation by spores of the marine Bacillus sp. strain SG-1
Am. Mineral.
The anaerobic degradation of organic matter in Danish coastal sediments: iron reduction, manganese reduction, and sulfate reduction
Geochim. Cosmochim. Acta
Geomicrobiology of the ocean crust: a role for chemoautotrophic Fe-bacteria
Biol. Bull.
Bacterially mediated mineral formation: insights into manganese(II) oxidation from molecular genetic and biochemical studies
Manganese and defenses against oxygen-toxicity in Lactobacillus plantarum
J. Bacteriol.
Manganese, superoxide dismutase, and oxygen tolerance in some lactic acid bacteria
J. Bacteriol.
Accumulation of Mn(II) in, Deinococcus radiodurans facilitates gamma-radiation resistance
Science
FTIR spectroscopic study of biogenic Mn-oxide formation by Pseudomonas putida GB-1
Geomicrobiol. J.
Oxidation of humic substances by manganese oxides yields low-molecular-weight organic substrates
Nature
Manganese oxidation by spores and spore coats of a marine Bacillus species
Appl. Environ. Microbiol.
Partial purification and characterization of manganese-oxidizing factors of Pseudomonas fluorescens GB-1
Appl. Environ. Microbiol.
Characterization of extracellular Mn2+-oxidizing activity and isolation of an Mn2+-oxidizing protein from Leptothrix discophora SS-1
J. Bacteriol.
Caldimonas manganoxidans gen. nov., sp. nov., a poly(3-hydroxybutyrate)-degrading, manganese-oxidizing thermophile
Int. J. Syst. Evol. Microbiol.
Enzymatic manganese(II) oxidation by a marine α–proteobacterium
Appl. Environ. Microbiol.
Manganese(II) adsorption and oxidation by whole cells and a membrane fraction of Pedomicrobium sp. ACM 3067
Arch. Microbiol.
Interaction of inorganic arsenic with biogenic manganese oxide produced by a Mn-oxidizing fungus, strain KR21-2
Environ. Sci. Technol.
Sorption of Co(II), Ni(II), and Zn(II) on biogenic manganese oxides produced by a Mn-oxidizing fungus, strain KR21-2
J. Environ. Sci. Health A Tox. Hazard. Subst. Environ. Eng.
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