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

Chang, Jin; Peng, Peng; DiSpirito, Alan A.; Semrau, Jeremy D.

doi:10.1128/aem.02346-21

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

Journal Article · Mon Mar 14 00:00:00 EDT 2022 · Applied and Environmental Microbiology

DOI:https://doi.org/10.1128/aem.02346-21· OSTI ID:1865104

Chang, Jin ^[1]; Peng, Peng ^[1];

^[2];

^[1]

Univ. of Michigan, Ann Arbor, MI (United States)
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.

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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, Vol. 88, Issue 7; ISSN 0099-2240

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

References (75)

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
Methane emissions from wetlands: biogeochemical, microbial, and modeling perspectives from local to global scales Bridgham, Scott D.; Cadillo-Quiroz, Hinsby; Keller, Jason K. Global Change Biology, Vol. 19, Issue 5 https://doi.org/10.1111/gcb.12131	journal	February 2013
A 3-D model analysis of the slowdown and interannual variability in the methane growth rate from 1988 to 1997: METHANE INTERANNUAL VARIABILITY Wang, James S.; Logan, Jennifer A.; McElroy, Michael B. Global Biogeochemical Cycles, Vol. 18, Issue 3 https://doi.org/10.1029/2003GB002180	journal	August 2004
The global methane cycle: recent advances in understanding the microbial processes involved: Global methane cycle Conrad, Ralf Environmental Microbiology Reports, Vol. 1, Issue 5 https://doi.org/10.1111/j.1758-2229.2009.00038.x	journal	June 2009
A comprehensive quantification of global nitrous oxide sources and sinks Tian, Hanqin; Xu, Rongting; Canadell, Josep G. Nature, Vol. 586, Issue 7828 https://doi.org/10.1038/s41586-020-2780-0	journal	October 2020
Widespread soil bacterium that oxidizes atmospheric methane Tveit, Alexander T.; Hestnes, Anne Grethe; Robinson, Serina L. Proceedings of the National Academy of Sciences, Vol. 116, Issue 17 https://doi.org/10.1073/pnas.1817812116	journal	April 2019
Methane and nitrous oxide fluxes in native, fertilized and cultivated grasslands Mosier, A.; Schimel, D.; Valentine, D. Nature, Vol. 350, Issue 6316 https://doi.org/10.1038/350330a0	journal	March 1991
Conventional methanotrophs are responsible for atmospheric methane oxidation in paddy soils Cai, Yuanfeng; Zheng, Yan; Bodelier, Paul L. E. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms11728	journal	June 2016
Nitrous oxide production and consumption: regulation of gene expression by gas-sensitive transcription factors Spiro, Stephen Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 367, Issue 1593 https://doi.org/10.1098/rstb.2011.0309	journal	May 2012
Intergenomic Comparisons Highlight Modularity of the Denitrification Pathway and Underpin the Importance of Community Structure for N2O Emissions Graf, Daniel R. H.; Jones, Christopher M.; Hallin, Sara PLoS ONE, Vol. 9, Issue 12 https://doi.org/10.1371/journal.pone.0114118	journal	December 2014
Nitrite-driven anaerobic methane oxidation by oxygenic bacteria Ettwig, Katharina F.; Butler, Margaret K.; Le Paslier, Denis Nature, Vol. 464, Issue 7288 https://doi.org/10.1038/nature08883	journal	March 2010
Archaea catalyze iron-dependent anaerobic oxidation of methane Ettwig, Katharina F.; Zhu, Baoli; Speth, Daan Proceedings of the National Academy of Sciences, Vol. 113, Issue 45 https://doi.org/10.1073/pnas.1609534113	journal	October 2016
Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage Haroon, Mohamed F.; Hu, Shihu; Shi, Ying Nature, Vol. 500, Issue 7464 https://doi.org/10.1038/nature12375	journal	July 2013
Anaerobic Oxidation of Methane Coupled to Nitrite Reduction by Halophilic Marine NC10 Bacteria He, Zhanfei; Geng, Sha; Cai, Chaoyang Applied and Environmental Microbiology, Vol. 81, Issue 16 https://doi.org/10.1128/AEM.00984-15	journal	August 2015
Field and laboratory studies of methane oxidation in an anoxic marine sediment: Evidence for a methanogen-sulfate reducer consortium Hoehler, Tori M.; Alperin, Marc J.; Albert, Daniel B. Global Biogeochemical Cycles, Vol. 8, Issue 4 https://doi.org/10.1029/94GB01800	journal	December 1994
Manganese- and Iron-Dependent Marine Methane Oxidation Beal, E. J.; House, C. H.; Orphan, V. J. Science, Vol. 325, Issue 5937 https://doi.org/10.1126/science.1169984	journal	July 2009
Anaerobic Oxidation of Methane: Mechanisms, Bioenergetics, and the Ecology of Associated Microorganisms Caldwell, Sara L.; Laidler, James R.; Brewer, Elizabeth A. Environmental Science & Technology, Vol. 42, Issue 18 https://doi.org/10.1021/es800120b	journal	September 2008
Environmental, genomic and taxonomic perspectives on methanotrophic Verrucomicrobia : Perspectives on methanotrophic Op den Camp, Huub J. M.; Islam, Tajul; Stott, Matthew B. Environmental Microbiology Reports, Vol. 1, Issue 5 https://doi.org/10.1111/j.1758-2229.2009.00022.x	journal	March 2009
Methanotrophs and copper Semrau, Jeremy D.; DiSpirito, Alan A.; Yoon, Sukhwan FEMS Microbiology Reviews, Vol. 34, Issue 4 https://doi.org/10.1111/j.1574-6976.2010.00212.x	journal	July 2010
Diversity and Habitat Preferences of Cultivated and Uncultivated Aerobic Methanotrophic Bacteria Evaluated Based on pmoA as Molecular Marker Knief, Claudia Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.01346	journal	December 2015
Methane oxidation by an extremely acidophilic bacterium of the phylum Verrucomicrobia Dunfield, Peter F.; Yuryev, Anton; Senin, Pavel Nature, Vol. 450, Issue 7171 https://doi.org/10.1038/nature06411	journal	November 2007
Methanotrophy below pH 1 by a new Verrucomicrobia species Pol, Arjan; Heijmans, Klaas; Harhangi, Harry R. Nature, Vol. 450, Issue 7171 https://doi.org/10.1038/nature06222	journal	November 2007
Expanding the Verrucomicrobial Methanotrophic World: Description of Three Novel Species of Methylacidimicrobium gen. nov. van Teeseling, Muriel C. F.; Pol, Arjan; Harhangi, Harry R. Applied and Environmental Microbiology, Vol. 80, Issue 21 https://doi.org/10.1128/AEM.01838-14	journal	August 2014
Methane oxidation at 55 C and pH 2 by a thermoacidophilic bacterium belonging to the Verrucomicrobia phylum Islam, T.; Jensen, S.; Reigstad, L. J. Proceedings of the National Academy of Sciences, Vol. 105, Issue 1, p. 300-304 https://doi.org/10.1073/pnas.0704162105	journal	January 2008
The origin of aerobic methanotrophy within the Proteobacteria Kang, Christina S.; Dunfield, Peter F.; Semrau, Jeremy D. FEMS Microbiology Letters, Vol. 366, Issue 9 https://doi.org/10.1093/femsle/fnz096	journal	May 2019
The nature of the copper ions in the membranes containing the particulate methane monooxygenase from Methylococcus capsulatus (Bath). Nguyen, H. H.; Shiemke, A. K.; Jacobs, S. J. Journal of Biological Chemistry, Vol. 269, Issue 21 https://doi.org/10.1016/S0021-9258(17)36565-1	journal	May 1994
The Particulate Methane Monooxygenase from Methylococcus capsulatus (Bath) Is a Novel Copper-containing Three-subunit Enzyme : ISOLATION AND CHARACTERIZATION Nguyen, Hiep-Hoa T.; Elliott, Sean J.; Yip, John Hon-Kay Journal of Biological Chemistry, Vol. 273, Issue 14 https://doi.org/10.1074/jbc.273.14.7957	journal	April 1998
Oxidation of methane by a biological dicopper centre Balasubramanian, Ramakrishnan; Smith, Stephen M.; Rawat, Swati Nature, Vol. 465, Issue 7294 https://doi.org/10.1038/nature08992	journal	April 2010
Crystal structure of a membrane-bound metalloenzyme that catalyses the biological oxidation of methane Lieberman, Raquel L.; Rosenzweig, Amy C. Nature, Vol. 434, Issue 7030 https://doi.org/10.1038/nature03311	journal	January 2005
Mössbauer Studies of the Membrane-Associated Methane Monooxygenase from Methylococcus capsulatus Bath: Evidence for a Diiron Center Martinho, Marlène; Choi, Dong W.; DiSpirito, Alan A. Journal of the American Chemical Society, Vol. 129, Issue 51 https://doi.org/10.1021/ja077682b	journal	December 2007
Alkane Oxidation: Methane Monooxygenases, Related Enzymes, and Their Biomimetics Wang, Vincent C. -C.; Maji, Suman; Chen, Peter P. -Y. Chemical Reviews, Vol. 117, Issue 13 https://doi.org/10.1021/acs.chemrev.6b00624	journal	February 2017
Spectral and copper binding properties of methanobactin from the facultative methanotroph Methylocystis strain SB2 Bandow, Nathan; Gilles, Valerie S.; Freesmeier, Brittani Journal of Inorganic Biochemistry, Vol. 110 https://doi.org/10.1016/j.jinorgbio.2012.02.002	journal	May 2012
Variations in methanobactin structure influences copper utilization by methane-oxidizing bacteria El Ghazouani, A.; Basle, A.; Gray, J. Proceedings of the National Academy of Sciences, Vol. 109, Issue 22 https://doi.org/10.1073/pnas.1112921109	journal	May 2012
Methanobactin, a Copper-Acquisition Compound from Methane-Oxidizing Bacteria Kim, H. J. Science, Vol. 305, Issue 5690 https://doi.org/10.1126/science.1098322	journal	September 2004
NMR, Mass Spectrometry and Chemical Evidence Reveal a Different Chemical Structure for Methanobactin That Contains Oxazolone Rings Behling, Lee A.; Hartsel, Scott C.; Lewis, David E. Journal of the American Chemical Society, Vol. 130, Issue 38 https://doi.org/10.1021/ja804747d	journal	September 2008
Methanobactin from methanotrophs: genetics, structure, function and potential applications Semrau, Jeremy D.; DiSpirito, Alan A.; Obulisamy, Parthiba Karthikeyan FEMS Microbiology Letters, Vol. 367, Issue 5 https://doi.org/10.1093/femsle/fnaa045	journal	March 2020
Mercury binding by methanobactin from Methylocystis strain SB2 Baral, Bipin S.; Bandow, Nathan L.; Vorobev, Alexy Journal of Inorganic Biochemistry, Vol. 141 https://doi.org/10.1016/j.jinorgbio.2014.09.004	journal	December 2014
The 2.3 angstrom X-ray structure of nitrite reductase from Achromobacter cycloclastes Godden, J.; Turley, S.; Teller, D. Science, Vol. 253, Issue 5018 https://doi.org/10.1126/science.1862344	journal	July 1991
A novel type of catalytic copper cluster in nitrous oxide reductase Cambillau, Christian; Brown, Kieron; Tegoni, Mariella Nature Structural Biology, Vol. 7, Issue 3, p. 191-195 https://doi.org/10.1038/73288	journal	March 2000
Structural conservation of the B subunit in the ammonia monooxygenase/particulate methane monooxygenase superfamily: Structure of an Archaeal amoB Domain Lawton, Thomas J.; Ham, Jungwha; Sun, Tianlin Proteins: Structure, Function, and Bioinformatics, Vol. 82, Issue 9 https://doi.org/10.1002/prot.24535	journal	March 2014
Ecological and physiological implications of nitrogen oxide reduction pathways on greenhouse gas emissions in agroecosystems Yoon, Sukhwan; Song, Bongkeun; Phillips, Rebecca L. FEMS Microbiology Ecology, Vol. 95, Issue 6 https://doi.org/10.1093/femsec/fiz066	journal	May 2019
Unexpected nondenitrifier nitrous oxide reductase gene diversity and abundance in soils Sanford, R. A.; Wagner, D. D.; Wu, Q. Proceedings of the National Academy of Sciences, Vol. 109, Issue 48 https://doi.org/10.1073/pnas.1211238109	journal	November 2012
The unaccounted yet abundant nitrous oxide-reducing microbial community: a potential nitrous oxide sink Jones, Christopher M.; Graf, Daniel RH; Bru, David The ISME Journal, Vol. 7, Issue 2 https://doi.org/10.1038/ismej.2012.125	journal	November 2012
Nitrous Oxide Reduction Kinetics Distinguish Bacteria Harboring Clade I NosZ from Those Harboring Clade II NosZ Yoon, Sukhwan; Nissen, Silke; Park, Doyoung Applied and Environmental Microbiology, Vol. 82, Issue 13 https://doi.org/10.1128/AEM.00409-16	journal	April 2016
Enrichment, Isolation, and Characterization of High-Affinity N ₂ O-Reducing Bacteria in a Gas-Permeable Membrane Reactor Suenaga, Toshikazu; Hori, Tomoyuki; Riya, Shohei Environmental Science & Technology, Vol. 53, Issue 20 https://doi.org/10.1021/acs.est.9b02237	journal	September 2019
Recently identified microbial guild mediates soil N2O sink capacity Jones, Christopher M.; Spor, Ayme; Brennan, Fiona P. Nature Climate Change, Vol. 4, Issue 9 https://doi.org/10.1038/nclimate2301	journal	July 2014
The diversity of the N2O reducers matters for the N2O:N2 denitrification end-product ratio across an annual and a perennial cropping system Domeignoz-Horta, Luiz A.; Spor, Aymé; Bru, David Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00971	journal	September 2015
Methanobactin from Methylosinus trichosporium OB3b inhibits N2O reduction in denitrifiers Chang, Jin; Gu, Wenyu; Park, Doyoung The ISME Journal, Vol. 12, Issue 8 https://doi.org/10.1038/s41396-017-0022-8	journal	January 2018
Copper control of bacterial nitrous oxide emission and its impact on vitamin B12-dependent metabolism Sullivan, M. J.; Gates, A. J.; Appia-Ayme, C. Proceedings of the National Academy of Sciences, Vol. 110, Issue 49 https://doi.org/10.1073/pnas.1314529110	journal	November 2013
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 Black, Amanda; Hsu, Pei‐Chun L.; Hamonts, Kelly E. Microbial Biotechnology, Vol. 9, Issue 3 https://doi.org/10.1111/1751-7915.12352	journal	March 2016
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 Felgate, Heather; Giannopoulos, Georgios; Sullivan, Matthew J. Environmental Microbiology, Vol. 14, Issue 7 https://doi.org/10.1111/j.1462-2920.2012.02789.x	journal	May 2012
Accumulation of nitrogen oxides in copper-limited cultures of denitrifying bacteria Granger, Julie; Ward, Bess B. Limnology and Oceanography, Vol. 48, Issue 1 https://doi.org/10.4319/lo.2003.48.1.0313	journal	January 2003
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” Peng, Peng; Kang-Yun, Christina S.; Chang, Jin Applied and Environmental Microbiology, Vol. 88, Issue 1 https://doi.org/10.1128/AEM.01793-21	journal	January 2022
Evidence for methanobactin “Theft” and novel chalkophore production in methanotrophs: impact on methanotrophic-mediated methylmercury degradation Kang-Yun, Christina S.; Liang, Xujun; Dershwitz, Philip The ISME Journal https://doi.org/10.1038/s41396-021-01062-1	journal	July 2021
A TonB-Dependent Transporter Is Responsible for Methanobactin Uptake by Methylosinus trichosporium OB3b Gu, Wenyu; Farhan Ul Haque, Muhammad; Baral, Bipin S. Applied and Environmental Microbiology, Vol. 82, Issue 6 https://doi.org/10.1128/AEM.03884-15	journal	January 2016
Potential role of copper availability in nitrous oxide accumulation in a temperate lake Twining, Benjamin S.; Mylon, Steven E.; Benoit, Gaboury Limnology and Oceanography, Vol. 52, Issue 4 https://doi.org/10.4319/lo.2007.52.4.1354	journal	July 2007
Organic carbon, and not copper, controls denitrification in oxygen minimum zones of the ocean Ward, Bess B.; Tuit, Caroline B.; Jayakumar, Amal Deep Sea Research Part I: Oceanographic Research Papers, Vol. 55, Issue 12 https://doi.org/10.1016/j.dsr.2008.07.005	journal	December 2008
Effects of copper on the abundance and diversity of ammonia oxidizers during dairy cattle manure composting Yin, Yanan; Song, Wen; Gu, Jie Bioresource Technology, Vol. 221 https://doi.org/10.1016/j.biortech.2016.09.016	journal	December 2016
Archaeal nitrification is constrained by copper complexation with organic matter in municipal wastewater treatment plants Gwak, Joo-Han; Jung, Man-Young; Hong, Heeji The ISME Journal, Vol. 14, Issue 2 https://doi.org/10.1038/s41396-019-0538-1	journal	October 2019
Structure of Alcaligenes faecalis Nitrite Reductase and a Copper Site Mutant, M150E, That Contains Zinc Murphy, Michael E. P.; Turley, Stewart; Kukimoto, Mutsuko Biochemistry, Vol. 34, Issue 38 https://doi.org/10.1021/bi00038a003	journal	September 1995
Bacterial SBP56 identified as a Cu-dependent methanethiol oxidase widely distributed in the biosphere Eyice, Özge; Myronova, Nataliia; Pol, Arjan The ISME Journal, Vol. 12, Issue 1 https://doi.org/10.1038/ismej.2017.148	journal	October 2017
Cell biology and molecular basis of denitrification Zumft, W. G. Microbiology and Molecular Biology Reviews, Vol. 61, Issue 4 https://doi.org/10.1128/mmbr.61.4.533-616.1997	journal	December 1997
Redundant roles of Bradyrhizobium oligotrophicum Cu-type (NirK) and cd1-type (NirS) nitrite reductase genes under denitrifying conditions Sánchez, Cristina; Minamisawa, Kiwamu FEMS Microbiology Letters, Vol. 365, Issue 5 https://doi.org/10.1093/femsle/fny015	journal	January 2018
Influence of Volatile Fatty Acids on Nitrite Accumulation by a Pseudomonas stutzeri Strain Isolated from a Denitrifying Fluidized Bed Reactor. van Rijn, J.; Tal, Y.; Barak, Y. Applied and environmental microbiology, Vol. 62, Issue 7 https://doi.org/10.1128/aem.62.7.2615-2620.1996	journal	January 1996
Shewanella spp. Use Acetate as an Electron Donor for Denitrification but Not Ferric Iron or Fumarate Reduction Yoon, Sukhwan; Sanford, Robert A.; Löffler, Frank E. Applied and Environmental Microbiology, Vol. 79, Issue 8 https://doi.org/10.1128/AEM.03872-12	journal	February 2013
Viologen dye Inhibition of Methane Formation by Methanobacillus Omelianskii Wolin, E. A.; Wolfe, R. S.; Wolin, M. J. Journal of Bacteriology, Vol. 87, Issue 5 https://doi.org/10.1128/jb.87.5.993-998.1964	journal	January 1964
Methanobactin from Methylocystis sp. Strain SB2 Affects Gene Expression and Methane Monooxygenase Activity in Methylosinus trichosporium OB3b Farhan Ul-Haque, Muhammad; Kalidass, Bhagyalakshmi; Vorobev, Alexey Applied and Environmental Microbiology, Vol. 81, Issue 7 https://doi.org/10.1128/AEM.03981-14	journal	January 2015
Uptake and effect of rare earth elements on gene expression in Methylosinus trichosporium OB3b Gu, Wenyu; Farhan Ul Haque, Muhammad; DiSpirito, Alan A. FEMS Microbiology Letters, Vol. 363, Issue 13 https://doi.org/10.1093/femsle/fnw129	journal	May 2016
MUSCLE: multiple sequence alignment with high accuracy and high throughput Edgar, R. C. Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797 https://doi.org/10.1093/nar/gkh340	journal	March 2004
The neighbor-joining method: a new method for reconstructing phylogenetic trees. Saitou, N.; Nei, M. Molecular Biology and Evolution, Vol. 4, Issue 4, p. 406-425 https://doi.org/10.1093/oxfordjournals.molbev.a040454	journal	July 1987
MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms Kumar, Sudhir; Stecher, Glen; Li, Michael Molecular Biology and Evolution, Vol. 35, Issue 6 https://doi.org/10.1093/molbev/msy096	journal	May 2018
Concurrent Haloalkanoate Degradation and Chlorate Reduction by Pseudomonas chloritidismutans AW-1 ^T Peng, Peng; Zheng, Ying; Koehorst, Jasper J. Applied and Environmental Microbiology, Vol. 83, Issue 12 https://doi.org/10.1128/AEM.00325-17	journal	June 2017
Analyzing real-time PCR data by the comparative CT method Schmittgen, Thomas D.; Livak, Kenneth J. Nature Protocols, Vol. 3, Issue 6 https://doi.org/10.1038/nprot.2008.73	journal	June 2008
Competition between Metals for Binding to Methanobactin Enables Expression of Soluble Methane Monooxygenase in the Presence of Copper Kalidass, Bhagyalakshmi; Ul-Haque, Muhammad Farhan; Baral, Bipin S. Applied and Environmental Microbiology, Vol. 81, Issue 3 https://doi.org/10.1128/AEM.03151-14	journal	November 2014
Enhanced Nitrous Oxide Production in Denitrifying Dechloromonas aromatica Strain RCB Under Salt or Alkaline Stress Conditions Han, Heejoo; Song, Bongkeun; Song, Min Joon Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.01203	journal	June 2019

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54 ENVIRONMENTAL SCIENCES
59 BASIC BIOLOGICAL SCIENCES
copper
denitrifier
methane
methanobactin
methanotrophy
nitrous oxide

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

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