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Enzymatic Manganese(II) Oxidation By Metabolically Dormant Spores Of Diverse Bacillus Species

Chris A. Francis, B. Tebo
Published 2002 · Biology, Medicine

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ABSTRACT Bacterial spores are renowned for their longevity, ubiquity, and resistance to environmental insults, but virtually nothing is known regarding whether these metabolically dormant structures impact their surrounding chemical environments. In the present study, a number of spore-forming bacteria that produce dormant spores which enzymatically oxidize soluble Mn(II) to insoluble Mn(IV) oxides were isolated from coastal marine sediments. The highly charged and reactive surfaces of biogenic metal oxides dramatically influence the oxidation and sorption of both trace metals and organics in the environment. Prior to this study, the only known Mn(II)-oxidizing sporeformer was the marine Bacillus sp. strain SG-1, an extensively studied bacterium in which Mn(II) oxidation is believed to be catalyzed by a multicopper oxidase, MnxG. Phylogenetic analysis based on 16S rRNA and mnxG sequences obtained from 15 different Mn(II)-oxidizing sporeformers (including SG-1) revealed extensive diversity within the genus Bacillus, with organisms falling into several distinct clusters and lineages. In addition, active Mn(II)-oxidizing proteins of various sizes, as observed in sodium dodecyl sulfate-polyacrylamide electrophoresis gels, were recovered from the outer layers of purified dormant spores of the isolates. These are the first active Mn(II)-oxidizing enzymes identified in spores or gram-positive bacteria. Although extremely resistant to denaturation, the activities of these enzymes were inhibited by azide and o-phenanthroline, consistent with the involvement of multicopper oxidases. Overall, these studies suggest that the commonly held view that bacterial spores are merely inactive structures in the environment should be revised.
This paper references
16S/23S rRNA sequencing, p.115–175
D. J. Lane (1991)
Preservation records of micro-organisms: evidence of the tenacity of life.
M. Kennedy (1994)
Virgibacillus : a new genus to accommodate Bacillus pantothenticus (Proom and Knight 1950). Emended description of Virgibacillus pantothenticus
M. Heyndrickx (1998)
The interaction of metal ions at the manganese dioxide-solution interface
J. Murray (1973)
Bacillus from marine habitats: allocation to phena established by numerical techniques
G J Bonde (1981)
Bacillus subtilis spore coat. Microbiol
A Driks (1999)
Manganese oxidation by Leptothrix discophora SS-1
F. C. Boogerd (1987)
The Aerobic Endospore-Forming Bacteria: Classification and Identification
R. Berkeley (1981)
Bacillus jeotgali sp. nov., isolated from jeotgal, Korean traditional fermented seafood.
J. Yoon (2001)
Multicopper Oxidases and Oxygenases.
E. Solomon (1996)
Marine Bacillus spores as catalysts for oxidative precipitation and sorption of metals.
C. A. Francis (1999)
Bacterially mediated mineral formation; insights into manganese(II) oxidation from molecular genetic and biochemical studies
B. Tebo (1997)
II) OXIDATION BY DORMANT BACILLUS SPORES diversity of an agricultural soil in Wisconsin
Phylogeny of the Main Bacterial 16S rRNA Sequences in Drentse A Grassland Soils (The Netherlands)
A. Felske (1998)
Bacillus thuringiensis and Its Pesticidal Crystal Proteins
E. Schnepf (1998)
Microbial oxidation of cobalt: characterization and its significance in marine environments
Y. Lee (1994)
Genetic analysis of the marine manganese-oxidizing Bacillus sp. strain SG-1: protoplast transformation, Tn917 mutagenesis, and identification of chromosomal loci involved in manganese oxidation.
L. V. van Waasbergen (1993)
In Situ Characterization of Mn(II) Oxidation by Spores of the Marine Bacillus sp. strain SG-1
J. Bargar (2000)
Reclassification of Bacillus marismortui as Salibacillus marismortui comb. nov.
D. R. Arahal (2000)
Partial purification and characterization of manganese-oxidizing factors of Pseudomonas fluorescens GB-1.
M. Okazaki (1997)
The interaction of metal ions at the manganese dioxidesolution interface
J. W. Murray (1975)
Desiccation tolerance of prokaryotes.
M. Potts (1994)
cumA, a Gene Encoding a Multicopper Oxidase, Is Involved in Mn2+ Oxidation in Pseudomonas putida GB-1
G. Brouwers (1999)
Survey of metal tolerance in moderately halophilic eubacteria.
J. J. Nieto (1989)
Production of Biogenic Mn Oxides by Leptothrix discophora SS-1 in a Chemically Defined Growth Medium and Evaluation of Their Pb Adsorption Characteristics
Yarrow M. Nelson (1999)
Genes encoding spore coat polypeptides from Bacillus subtilis.
W. Donovan (1987)
Gracilibacillus gen. nov., with description of Gracilibacillus halotolerans gen. nov., sp. nov.; transfer of Bacillus dipsosauri to Gracilibacillus dipsosauri comb. nov., and Bacillus salexigens to the genus Salibacillus gen. nov., as Salibacillus salexigens comb. nov.
M. Wainø (1999)
The Biological Chemistry of the Elements
D. Williams (1991)
Characterization and Identification of Numerically Abundant Culturable Bacteria from the Anoxic Bulk Soil of Rice Paddy Microcosms
K. Chin (1999)
Enzymatic Manganese(II) Oxidation by a Marine α-Proteobacterium
C. A. Francis (2001)
Identification and characterization of a gene cluster involved in manganese oxidation by spores of the marine Bacillus sp. strain SG-1.
L. V. van Waasbergen (1996)
Mosquitocidal toxins of bacilli and their genetic manipulation for effective biological control of mosquitoes.
A. Porter (1993)
Biodiversity in deep-sea sites located near the south part of Japan
H. Takami (1999)
Bacillus from marine habitats: allocation to phena established by numerical techniques, p. 181–215
G. J. Bonde (1981)
Manganese oxidation by spores and spore coats of a marine bacillus species.
J. D. de Vrind (1986)
Halobacillus gen. nov., with Descriptions of Halobacillus litoralis sp. nov. and Halobacillus trueperi sp. nov., and Transfer of Sporosarcina halophila to Halobacillus halophilus comb. nov.
S. Spring (1996)
Bacillus subtilis Spore Coat
A. Driks (1999)
Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4
U. Laemmli (1970)
Characterization of extracellular Mn2+-oxidizing activity and isolation of an Mn2+-oxidizing protein from Leptothrix discophora SS-1.
L. Adams (1987)
The Cytochrome c Maturation Operon Is Involved in Manganese Oxidation in Pseudomonas putidaGB-1
J. D. de Vrind (1998)
Oxidation of manganese by spores of a marine bacillus: Kinetic and thermodynamic considerations
David Hastings (1986)
Diversity and Molecular Mechanisms of Manganese(II)-Oxidizing Bacteria
C. Francis (2000)
Revival and identification of bacterial spores in 25- to 40-million-year-old Dominican amber.
R. Cano (1995)
Resistance of Bacillus Endospores to Extreme Terrestrial and Extraterrestrial Environments
W. Nicholson (2000)
Nucleic acid techniques in bacterial systematics
E. Stackebrandt (1991)
Phylogeny of Marine Bacillus Isolates from the Gulf of Mexico
J. Siefert (2000)
Bacillus marismortui sp. nov., a new moderately halophilic species from the Dead Sea.
D. R. Arahal (1999)
Redox processes at surfaces of manganese oxide and their effects on aqueous metal ions
J. D. Hem (1978)
Molecular microbial diversity of an agricultural soil in Wisconsin.
J. Borneman (1996)
Characterization of spoIVA, a sporulation gene involved in coat morphogenesis in Bacillus subtilis.
S. Roels (1992)
Manganese binding and oxidation by spores of a marine bacillus.
R. Rosson (1982)
Evolution and protein complexity: the blue copper-containing oxidases and related proteins
L. G. Ryden (1993)
CotA of Bacillus subtilis is a copper-dependent laccase.
M. Hullo (2001)
Identification and molecular analysis of the Leptothrix discophora SS‐1 mofA gene, a gene putatively encoding a manganese‐oxidizing protein with copper domains
P. Corstjens (1997)
Comparative analyses of the bacterial diversity on two different biodeteriorated wall paintings by DGGE and 16S rDNA sequence analysis
Claudia Gurtner (2000)
16S/23S rRNA sequencing
D. J. Lane (1991)
Identification and molecular analysis of the Leptothrix discophora SS-1 mofA gene, a gene putatively encoding a manganese-oxidizing protein with copper domains. Geomicrobiol
Corstjens (1997)
Manganese oxidation by Leptothrix discophora.
F. Boogerd (1987)
Isolation of a 250 million-year-old halotolerant bacterium from a primary salt crystal
R. Vreeland (2000)
Surface enhancement of bacterial manganese oxidation: Implications for aquatic environments
K. Nealson (1980)
Longevity of microorganisms in natural environments.
H. Gest (1987)

This paper is referenced by
Manganese Oxidation by Bacterial Isolates from the Indian Ridge System
S. O. Fernandes (2005)
Promotion of Mn(II) Oxidation and Remediation of Coal Mine Drainage in Passive Treatment Systems by Diverse Fungal and Bacterial Communities
C. Santelli (2010)
Biomineralisation of the ferromanganese crusts in the Western Pacific Ocean
X. Jiang (2017)
Arsenite Oxidation Using Biogenic Manganese Oxides Produced by a Deep-Sea Manganese-Oxidizing Bacterium, Marinobacter sp. MnI7-9
S. Liao (2013)
Cr(OH)3(s) oxidation induced by surface catalyzed Mn(II) oxidation.
Seonyi Namgung (2014)
Characterization of pH dependent Mn(II) oxidation strategies and formation of a bixbyite-like phase by Mesorhizobium australicum T-G1
Tsing Bohu (2015)
Impacts of Ocean Acidification on Shelled Pteropods in the Southern Ocean
N. Blank (2007)
Multiple organic substrates support Mn(II) removal with enrichment of Mn(II)-oxidizing bacteria.
Ahmad Shoiful (2020)
Autotrophic nitrogen conversion process and microbial population distribution in biofilter that simultaneously removes Fe, Mn and ammonia from groundwater
Hang Yang (2018)
Manganese(II)-Oxidizing Bacillus Spores in Guaymas Basin Hydrothermal Sediments and Plumes
G. Dick (2006)
Biological Manganese Removal by Novel Halotolerant Bacteria Isolated from River Water
Van Khanh Nguyen (2020)
Species-level identification of Bacillus strains isolates from marine sediments by conventional biochemical, 16S rRNA gene sequencing and inter-tRNA gene sequence lengths analysis
Cátia Miranda (2007)
The Molecular Geomicrobiology of Bacterial Manganese(II) Oxidation
B. Tebo (2010)
Complex evolutionary dynamics govern the diversity and distribution of biosynthetic gene clusters and their encoded specialized metabolites
Alexander B. Chase (2020)
Microbial Communities Promoting Mn(II) Oxidation in Ashumet Pond, a Historically Polluted Freshwater Pond Undergoing Remediation
C. Santelli (2014)
Evidence for the presence of Mn(III) intermediates in the bacterial oxidation of Mn(II).
S. Webb (2005)
Bacillus rigiliprofundi sp. nov., an endospore-forming, Mn-oxidizing, moderately halophilic bacterium isolated from deep subseafloor basaltic crust.
J. Sylvan (2015)
Microbiological And Electrochemical Evaluation Of Corrosion And Microbiologically Influenced Corrosion Of Steel In Ethanol Fuel Environments
L. Jain (2010)
Microbial diversity within the low-temperature influenced deep marine biosphere along the Mid-Atlantic-Ridge
K. Rathsack (2010)
Further Readings in Geomicrobiology
Production and Characterization of Biogenic Manganese Oxides by Manganese-adapted Pseudomonas putida NRRL B-14878
Semih Cömert (2020)
Isolation and molecular characterization of phenol-degrading gram-positive bacteria from oil-contaminated soil.
R. M. Enan (2006)
Enzymatic microbial Mn(II) oxidation and Mn biooxide production in the Guaymas Basin deep-sea hydrothermal plume
G. Dick (2009)
Microdiversity of Deep-Sea Bacillales Isolated from Tyrrhenian Sea Sediments as Revealed by ARISA , 16 S rRNA Gene Sequencing and BOX-PCR Fingerprinting
Mel (2013)
Phylogenetic Relationships and Functional Genes: Distribution of a Gene (mnxG) Encoding a Putative Manganese-Oxidizing Enzyme in Bacillus Species
L. Mayhew (2008)
Microbially-mediated geochemical cycling of iron and nitrogen within the granite-hosted subsurface of Henderson Mine, CO
E. Swanner (2011)
Adsorption of ferrous ions onto Bacillus subtilis cells
X. Châtellier (2004)
Ornithinibacillus gen. nov., with the species Ornithinibacillus bavariensis sp. nov. and Ornithinibacillus californiensis sp. nov.
R. Mayr (2006)
The Role of Bacterial Spores in Metal Cycling and Their Potential Application in Metal Contaminant Bioremediation.
Cristina N Butterfield (2016)
Bacterial spores, from ecology to biotechnology.
C. Paul (2019)
Manganese Oxide Biomineralization Provides Protection against Nitrite Toxicity in a Cell-Density-Dependent Manner
Christian Zerfass (2018)
Copper Proteins: Oxidases
C. Stoj (2011)
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