skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Metals and Methanotrophy

Journal Article · · Applied and Environmental Microbiology
DOI:https://doi.org/10.1128/aem.02289-17· OSTI ID:1503609
 [1];  [2];  [1];  [3];  [4]
  1. Univ. of Michigan, Ann Arbor, MI (United States)
  2. Iowa State Univ., Ames, IA (United States)
  3. Korea Advanced Inst. Science and Technology (KAIST), Daejeon (South Korea)
  4. Univ. of Illinois, Urbana-Champaign, IL (United States)

ABSTRACTAerobic methanotrophs have long been known to play a critical role in the global carbon cycle, being capable of converting methane to biomass and carbon dioxide. Interestingly, these microbes exhibit great sensitivity to copper and rare-earth elements, with the expression of key genes involved in the central pathway of methane oxidation controlled by the availability of these metals. That is, these microbes have a “copper switch” that controls the expression of alternative methane monooxygenases and a “rare-earth element switch” that controls the expression of alternative methanol dehydrogenases. Further, it has been recently shown that some methanotrophs can detoxify inorganic mercury and demethylate methylmercury; this finding is remarkable, as the canonical organomercurial lyase does not exist in these methanotrophs, indicating that a novel mechanism is involved in methylmercury demethylation. Here, we review recent findings on methanotrophic interactions with metals, with a particular focus on these metal switches and the mechanisms used by methanotrophs to bind and sequester metals.

Research Organization:
Univ. of Michigan, Ann Arbor, MI (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF)
Grant/Contract Number:
SC0018059
OSTI ID:
1503609
Alternate ID(s):
OSTI ID: 1691494
Journal Information:
Applied and Environmental Microbiology, Vol. 84, Issue 6; ISSN 0099-2240
Publisher:
American Society for MicrobiologyCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 89 works
Citation information provided by
Web of Science

References (168)

A methanotroph-based biorefinery: Potential scenarios for generating multiple products from a single fermentation journal September 2016
Fenton-like copper redox chemistry revisited: Hydrogen peroxide and superoxide mediation of copper-catalyzed oxidant production journal May 2013
One millimetre makes the difference: high-resolution analysis of methane-oxidizing bacteria and their specific activity at the oxic–anoxic interface in a flooded paddy soil journal June 2012
Methanotrophs and copper journal July 2010
The Biochemistry of Methane Oxidation journal June 2007
An Oxidized Tryptophan Facilitates Copper Binding in Methylococcus capsulatus -secreted Protein MopE journal March 2008
Mixed Pollutant Degradation by Methylosinus trichosporium OB3b Expressing either Soluble or Particulate Methane Monooxygenase: Can the Tortoise Beat the Hare? journal September 2006
The soluble methane mono-oxygenase of Methylococcus capsulatus (Bath). Its ability to oxygenate n-alkanes, n-alkenes, ethers, and alicyclic, aromatic and heterocyclic compounds journal August 1977
The Metal Centers of Particulate Methane Monooxygenase from Methylosinus trichosporium OB3b journal July 2008
Mutagenesis of the "Leucine Gate" To Explore the Basis of Catalytic Versatility in Soluble Methane Monooxygenase journal August 2007
Measurement and modeling of multiple substrate oxidation by methanotrophs at 20°C journal October 2008
Enrichment, Isolation and Some Properties of Methane-utilizing Bacteria journal May 1970
The structure and mechanism of methanol dehydrogenase journal April 2003
Biochemistry of the Soluble Methane Monooxygenase journal October 1994
Quantitative Transcriptomics Reveals the Growth- and Nutrient-Dependent Response of a Streamlined Marine Methylotroph to Methanol and Naturally Occurring Dissolved Organic Matter journal November 2016
Isolation, sequencing, and mutagenesis of the gene encoding cytochrome c553i of Paracoccus denitrificans and characterization of the mutant strain. journal November 1991
Autotrophic Methanotrophy in Verrucomicrobia: Methylacidiphilum fumariolicumSolV Uses the Calvin-Benson-Bassham Cycle for Carbon Dioxide Fixation journal July 2011
Acetylene as a suicide substrate and active site probe for methane monooxygenase from Methylococcus capsulatus (Bath) journal August 1985
Copper-Binding Properties and Structures of Methanobactins from Methylosinus trichosporium OB3b journal February 2011
Spectral, Kinetic, and Thermodynamic Properties of Cu(I) and Cu(II) Binding by Methanobactin from Methylosinus trichosporium OB3b journal February 2006
Characterization of a Novel Methanol Dehydrogenase in Representatives of Burkholderiales: Implications for Environmental Detection of Methylotrophy and Evidence for Convergent Evolution journal April 2008
Genome mining for methanobactins journal February 2013
Methanobactin, a Copper-Acquisition Compound from Methane-Oxidizing Bacteria journal September 2004
Chemical Plausibility of Cu(III) with Biological Ligation in pMMO journal May 2015
The Phyre2 web portal for protein modeling, prediction and analysis journal May 2015
Expression of the PitA phosphate/metal transporter of Escherichia coli is responsive to zinc and inorganic phosphate levels journal December 2008
The role of copper in the pMMO of Methylococcus capsulatus Bath: A structural vs. catalytic function journal June 1995
Nucleotide metabolism and its control in lactic acid bacteria journal August 2005
Modularity of methylotrophy, revisited: Modularity of methylotrophy, revisited journal March 2011
Methanotrophs and methylobacteria are found in woody plant tissues within the winter period journal November 2004
Draft Genome Sequence of Methyloferula stellata AR4, an Obligate Methanotroph Possessing Only a Soluble Methane Monooxygenase journal March 2015
Growth of methanotrophs in methane and oxygen counter gradients journal March 1995
A Catalytic Role of XoxF1 as La3+-Dependent Methanol Dehydrogenase in Methylobacterium extorquens Strain AM1 journal November 2012
Molecular structure of La3+-induced methanol dehydrogenase-like protein in Methylobacterium radiotolerans journal May 2011
Culturable Facultative Methylotrophic Bacteria from the Cactus <i>Neobuxbaumia macrocephala</i> Possess the Locus <i>xoxF</i> and Consume Methanol in the Presence of Ce<sup>3+</sup> and Ca<sup>2+</sup> journal January 2017
Investigation of XoxF methanol dehydrogenases reveals new methylotrophic bacteria in pelagic marine and freshwater ecosystems journal August 2015
Aquatic plant surface as a niche for methanotrophs journal January 2014
Purification and Physical−Chemical Properties of Methanobactin:  A Chalkophore from Methylosinus trichosporium OB3b journal April 2005
Diversity and Habitat Preferences of Cultivated and Uncultivated Aerobic Methanotrophic Bacteria Evaluated Based on pmoA as Molecular Marker journal December 2015
The small genome of an abundant coastal ocean methylotroph journal July 2008
Spectral and copper binding properties of methanobactin from the facultative methanotroph Methylocystis strain SB2 journal May 2012
Methane oxidation by an extremely acidophilic bacterium of the phylum Verrucomicrobia journal November 2007
Rare earth metals are essential for methanotrophic life in volcanic mudpots: Rare earth metals essential for methanotrophic life journal September 2013
Sulfur oxidizers dominate carbon fixation at a biogeochemical hot spot in the dark ocean journal July 2013
Genome Characteristics of Two Novel Type I Methanotrophs Enriched from North Sea Sediments Containing Exclusively a Lanthanide-Dependent XoxF5-Type Methanol Dehydrogenase journal July 2016
Psychrophilic methanotroph from tundra soil journal November 1993
Siderophore−Manganese(III) Interactions II. Manganite Dissolution Promoted by Desferrioxamine B journal August 2005
Combining metagenomics with metaproteomics and stable isotope probing reveals metabolic pathways used by a naturally occurring marine methylotroph: Metagenomics, metaproteomics and methylotrophy journal July 2015
Bacterial cytosolic proteins with a high capacity for Cu(I) that protect against copper toxicity journal December 2016
A TonB-Dependent Transporter Is Responsible for Methanobactin Uptake by Methylosinus trichosporium OB3b journal January 2016
The structure and function of the PQQ-containing quinoprotein dehydrogenases journal January 1998
SINA: Accurate high-throughput multiple sequence alignment of ribosomal RNA genes journal May 2012
Characterization of Methanobactin from Methylosinus sp. LW4 journal August 2016
An Aminotransferase is Responsible for the Deamination of the N-terminal Leucine and Required for Formation of Oxazolone Ring A in Methanobactin of Methylosinus trichosporium OB3b journal October 2016
Evidence for a Tryptophan Tryptophylquinone Aminosemiquinone Intermediate in the Physiologic Reaction between Methylamine Dehydrogenase and Amicyanin journal January 1996
The iron-sulfur clusters of dehydratases are primary intracellular targets of copper toxicity journal May 2009
Membrane-associated methane monooxygenase from Methylococcus capsulatus (Bath). journal February 1996
Lanthanide-binding peptides and the enzymes that Might Have Been journal August 2004
Mercury binding by methanobactin from Methylocystis strain SB2 journal December 2014
Light rare earth element depletion during Deepwater Horizon blowout methanotrophy journal September 2017
Methane as a Resource: Can the Methanotrophs Add Value? journal March 2015
Draft Genome Sequence of Methylocapsa palsarum NE2 T , an Obligate Methanotroph from Subarctic Soil journal June 2017
Variations in methanobactin structure influences copper utilization by methane-oxidizing bacteria journal May 2012
Lanthanide-dependent cross-feeding of methane-derived carbon is linked by microbial community interactions journal December 2016
Nitrite-driven anaerobic methane oxidation by oxygenic bacteria journal March 2010
The Membrane-Associated Methane Monooxygenase (pMMO) and pMMO-NADH:Quinone Oxidoreductase Complex from Methylococcus capsulatus Bath journal September 2003
Methanotrophy below pH 1 by a new Verrucomicrobia species journal November 2007
XoxF encoding an alternative methanol dehydrogenase is widespread in coastal marine environments journal June 2015
The genomic landscape of the verrucomicrobial methanotroph Methylacidiphilum fumariolicum SolV journal January 2014
Genomic Insights into Methanotrophy: The Complete Genome Sequence of Methylococcus capsulatus (Bath) journal September 2004
Methane oxidation at 55 C and pH 2 by a thermoacidophilic bacterium belonging to the Verrucomicrobia phylum journal January 2008
MxaY regulates the lanthanide-mediated methanol dehydrogenase switch in Methylomicrobium buryatense journal January 2016
Structure and Spectroscopy of Copper−Dioxygen Complexes journal February 2004
Alkane Oxidation: Methane Monooxygenases, Related Enzymes, and Their Biomimetics journal February 2017
The Particulate Methane Monooxygenase from Methylococcus capsulatus (Bath) Is a Novel Copper-containing Three-subunit Enzyme : ISOLATION AND CHARACTERIZATION journal April 1998
Identification of proteins involved in formaldehyde metabolism by Rhodobacter sphaeroides journal January 2008
Conversion of Methane to Methanol at the Mononuclear and Dinuclear Copper Sites of Particulate Methane Monooxygenase (pMMO):  A DFT and QM/MM Study journal August 2006
The more, the merrier: heterotroph richness stimulates methanotrophic activity journal May 2014
The role of organic acids in mineral weathering journal February 1997
Detoxification of Mercury by Methanobactin from Methylosinus trichosporium OB3b journal July 2013
The Methylococcus capsulatus (Bath) Secreted Protein, MopE*, Binds Both Reduced and Oxidized Copper journal August 2012
A new cofactor in a prokaryotic enzyme: tryptophan tryptophylquinone as the redox prosthetic group in methylamine dehydrogenase journal May 1991
Siderophores: Structure and Function of Microbial Iron Transport Compounds journal November 1995
Metabolic engineering in methanotrophic bacteria journal May 2015
Autotrophic Carbon Dioxide Fixation via the Calvin-Benson-Bassham Cycle by the Denitrifying Methanotroph “Candidatus Methylomirabilis oxyfera” journal February 2014
Possible Peroxo State of the Dicopper Site of Particulate Methane Monooxygenase from Combined Quantum Mechanics and Molecular Mechanics Calculations journal February 2016
XoxF Acts as the Predominant Methanol Dehydrogenase in the Type I Methanotroph Methylomicrobium buryatense journal February 2016
X-ray Absorption and EPR Studies on the Copper Ions Associated with the Particulate Methane Monooxygenase from Methylococcus capsulatus (Bath). Cu(I) Ions and Their Implications journal January 1996
Lanthanide Chemistry: From Coordination in Chemical Complexes Shaping Our Technology to Coordination in Enzymes Shaping Bacterial Metabolism journal September 2016
Quantum mechanical calculations suggest that lytic polysaccharide monooxygenases use a copper-oxyl, oxygen-rebound mechanism journal December 2013
A four-helix bundle stores copper for methane oxidation journal August 2015
An assay for screening microbial cultures for chalkophore production journal April 2010
Environmental proteomics of microbial plankton in a highly productive coastal upwelling system journal November 2010
Mechanistic studies of a protonolytic organomercurial cleaving enzyme: bacterial organomercurial lyase journal November 1986
Community proteogenomics reveals insights into the physiology of phyllosphere bacteria journal September 2009
Molecular and mutational analysis of a DNA region separating two methylotrophy gene clusters in Methylobacterium extorquens AM1 journal May 1997
Comprehensive proteomics of Methylobacterium extorquens AM1 metabolism under single carbon and nonmethylotrophic conditions journal September 2008
Development of the Tricopper Cluster as a Catalyst for the Efficient Conversion of Methane into MeOH journal September 2013
Methanobactin and MmoD work in concert to act as the ‘copper-switch’ in methanotrophs: Copper-switch in methanotrophy journal May 2013
Outer membrane proteins of Methylococcus capsulatus (Bath) journal August 1997
Mössbauer Studies of the Membrane-Associated Methane Monooxygenase from Methylococcus capsulatus Bath:  Evidence for a Diiron Center journal December 2007
Identification of a Copper-Responsive Two-Component System on the Chromosome of Escherichia coli K-12 journal October 2000
Environmental Geochemistry of Cerium: Applications and Toxicology of Cerium Oxide Nanoparticles journal January 2015
Cell biology and molecular basis of denitrification. journal January 1997
Methanobactin and the Link between Copper and Bacterial Methane Oxidation journal March 2016
Microbial solubilization and immobilization of toxic metals: key biogeochemical processes for treatment of contamination journal July 1997
Insights into the oxidative degradation of cellulose by a copper metalloenzyme that exploits biomass components journal August 2011
TIGRFAMs and Genome Properties in 2013 journal November 2012
Stress resistance and C1 metabolism involved in plant colonization of a methanotroph Methylosinus sp. B4S journal September 2013
Microbes and metals journal December 1997
Cerium Regulates Expression of Alternative Methanol Dehydrogenases in Methylosinus trichosporium OB3b journal August 2015
Electroporation-Based Genetic Manipulation in Type I Methanotrophs journal January 2016
NMR, Mass Spectrometry and Chemical Evidence Reveal a Different Chemical Structure for Methanobactin That Contains Oxazolone Rings journal September 2008
Isolation of Methanobactin from the Spent Media of Methane-Oxidizing Bacteria book January 2011
Marker Exchange Mutagenesis of mxaF , Encoding the Large Subunit of the Mxa Methanol Dehydrogenase, in Methylosinus trichosporium OB3b journal December 2015
Methylosphaera hansonii gen. nov., sp. nov., a psychrophilic, group I methanotroph from Antarctic marine-salinity, meromictic lakes journal April 1997
Contributions of Five Secondary Metal Uptake Systems to Metal Homeostasis of Cupriavidus metallidurans CH34 journal July 2011
Rare earth elements in soil and plant systems - A review journal December 2004
Highly efficient methane biocatalysis revealed in a methanotrophic bacterium journal December 2013
The relationship between protein structure and function: a comprehensive survey with application to the yeast genome journal April 1999
Transcriptomic profiling of Methylococcus capsulatus (Bath) during growth with two different methane monooxygenases journal December 2015
Oxidation of methane by a biological dicopper centre journal April 2010
Characterization of Fluorescent and Nonfluorescent Peptide Siderophores Produced by Pseudomonas syringae Strains and Their Potential Use in Strain Identification journal April 2001
PQQ-dependent methanol dehydrogenases: rare-earth elements make a difference journal May 2014
The Surface-Associated and Secreted MopE Protein of Methylococcus capsulatus (Bath) Responds to Changes in the Concentration of Copper in the Growth Medium journal April 2003
Environmental, genomic and taxonomic perspectives on methanotrophic Verrucomicrobia : Perspectives on methanotrophic journal March 2009
The TIM-barrel fold: a versatile framework for efficient enzymes journal March 2001
Methylmercury uptake and degradation by methanotrophs journal May 2017
Ore Leaching by Bacteria journal October 1980
Expanding the Verrucomicrobial Methanotrophic World: Description of Three Novel Species of Methylacidimicrobium gen. nov. journal August 2014
Nitrate leaching in an Andisol treated with different types of fertilizers journal March 2003
Copper and cerium-regulated gene expression in Methylosinus trichosporium OB3b journal October 2017
Molecular structure and gene analysis of Ce3+-induced methanol dehydrogenase of Bradyrhizobium sp. MAFF211645 journal June 2011
A Comparison of Methanobactins from Methylosinus trichosporium OB3b and Methylocystis Strain SB2 Predicts Methanobactins Are Synthesized from Diverse Peptide Precursors Modified To Create a Common Core for Binding and Reducing Copper Ions journal November 2010
Taxonomic Characterization of New Alkaliphilic and Alkalitolerant Methanotrophs from Soda Lakes of the Southeastern Transbaikal Region and description of Methylomicrobium buryatense sp.nov. journal January 2001
The membrane-associated form of methane mono-oxygenase from Methylococcus capsulatus (Bath) is a copper/iron protein journal January 2003
Structural and Mechanistic Insights into Methane Oxidation by Particulate Methane Monooxygenase journal July 2007
MauG: a di-heme enzyme required for methylamine dehydrogenase maturation journal January 2013
Uptake and effect of rare earth elements on gene expression in Methylosinus trichosporium OB3b journal May 2016
Mechanisms of siderophore sorption to smectite and siderophore-enhanced release of structural Fe3+ journal July 2008
Stimulation of Methanotrophic Growth in Cocultures by Cobalamin Excreted by Rhizobia journal October 2011
Evidence for the transport of zinc(II) ions via the Pit inorganic phosphate transport system in Escherichia coli journal March 2000
MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets journal March 2016
The quinoprotein dehydrogenases for methanol and glucose journal August 2004
Copper stress underlies the fundamental change in intracellular location of methane mono-oxygenase in methane-oxidizing organisms: Studies in batch and continuous cultures journal July 1983
Crystal structure of a membrane-bound metalloenzyme that catalyses the biological oxidation of methane journal January 2005
Distribution of Methanotrophs in the Phyllosphere journal August 2012
Copper complexation of methanobactin isolated from Methylosinus trichosporium OB3b: pH-dependent speciation and modeling journal November 2012
The structure of bacterial quinoprotein dehydrogenases journal January 1992
Lanthanide-Dependent Regulation of Methanol Oxidation Systems in Methylobacterium extorquens AM1 and Their Contribution to Methanol Growth journal February 2016
Pseudomonas stutzeri N2O reductase contains CuA-type sites. journal June 1989
Mutagenesis of the hydrocarbon monooxygenase indicates a metal centre in subunit-C, and not subunit-B, is essential for copper-containing membrane monooxygenase activity journal March 2014
Functional investigation of methanol dehydrogenase-like protein XoxF in Methylobacterium extorquens AM1 journal May 2010
Methanobactin from Methylosinus trichosporium OB3b inhibits N2O reduction in denitrifiers journal January 2018
Extractive Metallurgy of Rare Earths book December 2015
Complete genome sequence of the extremely acidophilic methanotroph isolate V4, Methylacidiphilum infernorum, a representative of the bacterial phylum Verrucomicrobia journal January 2008
The nature of the copper ions in the membranes containing the particulate methane monooxygenase from Methylococcus capsulatus (Bath). journal May 1994
Phenotypic characterization of copper-resistant mutants of Methylosinus trichosporium OB3b. journal January 1993
Methylosinus trichosporium OB3b Mutants Having Constitutive Expression of Soluble Methane Monooxygenase in the Presence of High Levels of Copper journal January 1992
Cell biology and molecular basis of denitrification journal December 1997
Fission-Product and Cerium Uptake by Bacteria, Yeasts, and Molds1 journal January 1961
Nucleotide metabolism and its control in lactic acid bacteria journal August 2005
Microbes and Metals journal April 1895
An SHR–SCR module specifies legume cortical cell fate to enable nodulation journal December 2020
Community proteogenomics reveals insights into the physiology of phyllosphere bacteria text January 2009
Quantitative Transcriptomics Reveals the Growth- and Nutrient-Dependent Response of a Streamlined Marine Methylotroph to Methanol and Naturally Occurring Dissolved Organic Matter text January 2016
Structure and Spectroscopy of Copper—Dioxygen Complexes journal May 2004
Structural and Mechanistic Insights into Methane Oxidation by Particulate Methane Monooxygenase journal October 2007

Cited By (12)

Similar but Not the Same: First Kinetic and Structural Analyses of a Methanol Dehydrogenase Containing a Europium Ion in the Active Site journal April 2018
Lanthanide-Dependent Methylotrophs of the Family Beijerinckiaceae : Physiological and Genomic Insights journal October 2019
Novel facultative Methylocella strains are active methane consumers at terrestrial natural gas seeps journal October 2019
Rare Earth Elements Alter Redox Balance in Methylomicrobium alcaliphilum 20ZR journal November 2018
Understanding the chemistry of the artificial electron acceptors PES, PMS, DCPIP and Wurster’s Blue in methanol dehydrogenase assays journal February 2020
The Chemistry of Lanthanides in Biology: Recent Discoveries, Emerging Principles, and Technological Applications journal August 2019
Contrasting in vitro and in vivo methanol oxidation activities of lanthanide-dependent alcohol dehydrogenases XoxF1 and ExaF from Methylobacterium extorquens AM1 journal March 2019
Isolation and Genomic Characterization of a Proteobacterial Methanotroph Requiring Lanthanides journal January 2020
The PedS2/PedR2 two-component system is crucial for the rare earth element switch in Pseudomonas putida KT2440 collection January 2018
Rare earth element (REE)-dependent growth of Pseudomonas putida KT2440 relies on the ABC-transporter PedA1A2BC and is influenced by iron availability collection January 2019
Extracellular Electron Transfer via Outer Membrane Cytochromes in a Methanotrophic Bacterium Methylococcus capsulatus (Bath) journal November 2018
Oxidation of L-Ascorbic Acid in the Presence of the Copper-Binding Compound from Methanotrophic Bacteria Methylococcus capsulatus (M) journal October 2020

Figures / Tables (5)