Skip to main content
U.S. Department of Energy
Office of Scientific and Technical Information

Variable Inhibition of Nitrous Oxide Reduction in Denitrifying Bacteria by Different Forms of Methanobactin

Journal Article · · Applied and Environmental Microbiology
DOI:https://doi.org/10.1128/aem.02346-21· OSTI ID:1865104
 [1];  [2];  [3];  [2]
  1. Univ. of Michigan, Ann Arbor, MI (United States); The University of Michigan
  2. Univ. of Michigan, Ann Arbor, MI (United States)
  3. Iowa State Univ., Ames, IA (United States)
Aerobic methanotrophic activity is highly dependent on copper availability, and methanotrophs have developed multiple strategies to collect copper. Specifically, when copper is limiting (ambient concentrations < 1 μM), some methanotrophs produce and secret a small modified peptide (< 1,300 Da) termed methanobactin (MB) that binds copper with high affinity. As MB is secreted into the environment, other microbes that require copper for their metabolism may be inhibited as MB may make copper unavailable; e.g., inhibition of denitrifiers as complete conversion nitrate to dinitrogen involves multiple enzymes, some of which are copper-dependent. Of key concern is inhibition of the copper-dependent nitrous oxide reductase (NosZ), the only known enzyme capable of converting nitrous oxide (N2O) to dinitrogen. Herein, we show that different forms of MB differentially affect copper uptake and N2O reduction by Pseudomonas stutzeri strain DCP-Ps1 (that expresses clade I NosZ) and Dechloromonas aromatica strain RCB (that expresses clade II NosZ). Specifically, in the presence of MB from Methylocystis sp. strain SB2 (SB2-MB), copper uptake and nosZ expression were more significantly reduced than in the presence of MB from Methylosinus trichosporium OB3b (OB3b-MB). Further, N2O accumulation increased more significantly for both P. stutzeri strain DCP-Ps1 and D. aromatica strain RCB in the presence of SB2-MB versus OB3b-MB. These data illustrate that copper competition between methanotrophs and denitrifying bacteria can be significant and that the extent of such competition is dependent on the form of MB that methanotrophs produce.
Research Organization:
Univ. of Michigan, Ann Arbor, MI (United States)
Sponsoring Organization:
USDOE Office of Science (SC)
Grant/Contract Number:
SC0020174
OSTI ID:
1865104
Journal Information:
Applied and Environmental Microbiology, Journal Name: Applied and Environmental Microbiology Journal Issue: 7 Vol. 88; ISSN 0099-2240
Publisher:
American Society for MicrobiologyCopyright Statement
Country of Publication:
United States
Language:
English

References (78)

Structural conservation of the B subunit in the ammonia monooxygenase/particulate methane monooxygenase superfamily: Structure of an Archaeal amoB Domain journal March 2014
The nature of the copper ions in the membranes containing the particulate methane monooxygenase from Methylococcus capsulatus (Bath). journal May 1994
Effects of copper on the abundance and diversity of ammonia oxidizers during dairy cattle manure composting journal December 2016
Organic carbon, and not copper, controls denitrification in oxygen minimum zones of the ocean journal December 2008
Spectral and copper binding properties of methanobactin from the facultative methanotroph Methylocystis strain SB2 journal May 2012
Mercury binding by methanobactin from Methylocystis strain SB2 journal December 2014
Alkane Oxidation: Methane Monooxygenases, Related Enzymes, and Their Biomimetics journal February 2017
Enrichment, Isolation, and Characterization of High-Affinity N 2 O-Reducing Bacteria in a Gas-Permeable Membrane Reactor journal September 2019
Structure of Alcaligenes faecalis Nitrite Reductase and a Copper Site Mutant, M150E, That Contains Zinc journal September 1995
Anaerobic Oxidation of Methane: Mechanisms, Bioenergetics, and the Ecology of Associated Microorganisms journal September 2008
Mössbauer Studies of the Membrane-Associated Methane Monooxygenase from Methylococcus capsulatus Bath:  Evidence for a Diiron Center journal December 2007
NMR, Mass Spectrometry and Chemical Evidence Reveal a Different Chemical Structure for Methanobactin That Contains Oxazolone Rings journal September 2008
A 3-D model analysis of the slowdown and interannual variability in the methane growth rate from 1988 to 1997: METHANE INTERANNUAL VARIABILITY journal August 2004
Field and laboratory studies of methane oxidation in an anoxic marine sediment: Evidence for a methanogen-sulfate reducer consortium journal December 1994
Methane and nitrous oxide fluxes in native, fertilized and cultivated grasslands journal March 1991
A novel type of catalytic copper cluster in nitrous oxide reductase journal March 2000
The unaccounted yet abundant nitrous oxide-reducing microbial community: a potential nitrous oxide sink journal November 2012
Bacterial SBP56 identified as a Cu-dependent methanethiol oxidase widely distributed in the biosphere journal October 2017
Crystal structure of a membrane-bound metalloenzyme that catalyses the biological oxidation of methane journal January 2005
Methanotrophy below pH 1 by a new Verrucomicrobia species journal November 2007
Methane oxidation by an extremely acidophilic bacterium of the phylum Verrucomicrobia journal November 2007
Nitrite-driven anaerobic methane oxidation by oxygenic bacteria journal March 2010
Oxidation of methane by a biological dicopper centre journal April 2010
Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage journal July 2013
Recently identified microbial guild mediates soil N2O sink capacity journal July 2014
Conventional methanotrophs are responsible for atmospheric methane oxidation in paddy soils journal June 2016
Analyzing real-time PCR data by the comparative CT method journal June 2008
Methanobactin from Methylosinus trichosporium OB3b inhibits N2O reduction in denitrifiers journal January 2018
Archaeal nitrification is constrained by copper complexation with organic matter in municipal wastewater treatment plants journal October 2019
Evidence for methanobactin “Theft” and novel chalkophore production in methanotrophs: impact on methanotrophic-mediated methylmercury degradation journal July 2021
A comprehensive quantification of global nitrous oxide sources and sinks journal October 2020
Methane oxidation at 55 C and pH 2 by a thermoacidophilic bacterium belonging to the Verrucomicrobia phylum journal January 2008
Variations in methanobactin structure influences copper utilization by methane-oxidizing bacteria journal May 2012
Unexpected nondenitrifier nitrous oxide reductase gene diversity and abundance in soils journal November 2012
Copper control of bacterial nitrous oxide emission and its impact on vitamin B12-dependent metabolism journal November 2013
Archaea catalyze iron-dependent anaerobic oxidation of methane journal October 2016
Widespread soil bacterium that oxidizes atmospheric methane journal April 2019
The Particulate Methane Monooxygenase from Methylococcus capsulatus (Bath) Is a Novel Copper-containing Three-subunit Enzyme : ISOLATION AND CHARACTERIZATION journal April 1998
Ecological and physiological implications of nitrogen oxide reduction pathways on greenhouse gas emissions in agroecosystems journal May 2019
Methanobactin from methanotrophs: genetics, structure, function and potential applications journal March 2020
Uptake and effect of rare earth elements on gene expression in Methylosinus trichosporium OB3b journal May 2016
Redundant roles of Bradyrhizobium oligotrophicum Cu-type (NirK) and cd1-type (NirS) nitrite reductase genes under denitrifying conditions journal January 2018
The origin of aerobic methanotrophy within the Proteobacteria journal May 2019
MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms journal May 2018
MUSCLE: multiple sequence alignment with high accuracy and high throughput journal March 2004
The neighbor-joining method: a new method for reconstructing phylogenetic trees. journal July 1987
Nitrous oxide production and consumption: regulation of gene expression by gas-sensitive transcription factors journal May 2012
Biological sources and sinks of nitrous oxide and strategies to mitigate emissions
  • Thomson, Andrew J.; Giannopoulos, Georgios; Pretty, Jules
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 367, Issue 1593 https://doi.org/10.1098/rstb.2011.0415
journal May 2012
Influence of copper on expression of nirS , norB and nosZ and the transcription and activity of NIR , NOR and N 2 OR in the denitrifying soil bacteria Pseudomonas stutzeri journal March 2016
Methane emissions from wetlands: biogeochemical, microbial, and modeling perspectives from local to global scales journal February 2013
The impact of copper, nitrate and carbon status on the emission of nitrous oxide by two species of bacteria with biochemically distinct denitrification pathways: Denitrification and nitrous oxide release journal May 2012
Methanotrophs and copper journal July 2010
Environmental, genomic and taxonomic perspectives on methanotrophic Verrucomicrobia : Perspectives on methanotrophic journal March 2009
The global methane cycle: recent advances in understanding the microbial processes involved: Global methane cycle journal June 2009
Methanobactin, a Copper-Acquisition Compound from Methane-Oxidizing Bacteria journal September 2004
Manganese- and Iron-Dependent Marine Methane Oxidation journal July 2009
The 2.3 angstrom X-ray structure of nitrite reductase from Achromobacter cycloclastes journal July 1991
Concurrent Haloalkanoate Degradation and Chlorate Reduction by Pseudomonas chloritidismutans AW-1 T journal June 2017
Nitrous Oxide Reduction Kinetics Distinguish Bacteria Harboring Clade I NosZ from Those Harboring Clade II NosZ journal April 2016
Nitrite Control over Dissimilatory Nitrate/Nitrite Reduction Pathways in Shewanella loihica Strain PV-4 journal March 2015
Anaerobic Oxidation of Methane Coupled to Nitrite Reduction by Halophilic Marine NC10 Bacteria journal August 2015
Two TonB-Dependent Transporters in Methylosinus trichosporium OB3b Are Responsible for Uptake of Different Forms of Methanobactin and Are Involved in the Canonical “Copper Switch” journal January 2022
Expanding the Verrucomicrobial Methanotrophic World: Description of Three Novel Species of Methylacidimicrobium gen. nov. journal August 2014
Competition between Metals for Binding to Methanobactin Enables Expression of Soluble Methane Monooxygenase in the Presence of Copper journal November 2014
Shewanella spp. Use Acetate as an Electron Donor for Denitrification but Not Ferric Iron or Fumarate Reduction journal February 2013
A TonB-Dependent Transporter Is Responsible for Methanobactin Uptake by Methylosinus trichosporium OB3b journal January 2016
Methanobactin from Methylocystis sp. Strain SB2 Affects Gene Expression and Methane Monooxygenase Activity in Methylosinus trichosporium OB3b journal January 2015
Kinetic Explanation for Accumulation of Nitrite, Nitric Oxide, and Nitrous Oxide During Bacterial Denitrification † journal January 1981
Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. journal January 1993
Influence of Volatile Fatty Acids on Nitrite Accumulation by a Pseudomonas stutzeri Strain Isolated from a Denitrifying Fluidized Bed Reactor. journal January 1996
Viologen dye Inhibition of Methane Formation by Methanobacillus Omelianskii journal January 1964
Cell biology and molecular basis of denitrification journal December 1997
Intergenomic Comparisons Highlight Modularity of the Denitrification Pathway and Underpin the Importance of Community Structure for N2O Emissions journal December 2014
The diversity of the N2O reducers matters for the N2O:N2 denitrification end-product ratio across an annual and a perennial cropping system journal September 2015
Diversity and Habitat Preferences of Cultivated and Uncultivated Aerobic Methanotrophic Bacteria Evaluated Based on pmoA as Molecular Marker journal December 2015
Enhanced Nitrous Oxide Production in Denitrifying Dechloromonas aromatica Strain RCB Under Salt or Alkaline Stress Conditions journal June 2019
Accumulation of nitrogen oxides in copper-limited cultures of denitrifying bacteria journal January 2003
Potential role of copper availability in nitrous oxide accumulation in a temperate lake journal July 2007