Inhibition of nitrous oxide reduction in forest soil microcosms by different forms of methanobactin

Chang, Jin; Peng, Peng; Farhan Ul‐Haque, Muhammad; Hira, Abid; DiSpirito, Alan A.; Semrau, Jeremy D.

doi:10.1111/1462-2920.16456

Inhibition of nitrous oxide reduction in forest soil microcosms by different forms of methanobactin

Journal Article · Mon Jul 03 00:00:00 EDT 2023 · Environmental Microbiology

DOI:https://doi.org/10.1111/1462-2920.16456· OSTI ID:1991190

^[1]; Peng, Peng ^[2]; Farhan Ul‐Haque, Muhammad ^[3]; Hira, Abid ^[3]; DiSpirito, Alan A. ^[4]; ^[2]

University of Michigan, Ann Arbor, MI (United States); The University of Michigan
University of Michigan, Ann Arbor, MI (United States)
University of the Punjab, Lahore (Pakistan)
Iowa State University, Ames, IA (United States)

Copper plays a critical role in controlling greenhouse gas emissions as it is a key component of the particulate methane monooxygenase and nitrous oxide reductase. Some methanotrophs excrete methanobactin (MB) that has an extremely high copper affinity. As a result, MB may limit the ability of other microbes to gather copper, thereby decreasing their activity as well as impacting microbial community composition. Here, we show using forest soil microcosms that multiple forms of MB; MB from Methylosinus trichosporium OB3b (MB-OB3b) and MB from Methylocystis sp. strain SB2 (MB-SB2) increased nitrous oxide (N₂O) production as well caused significant shifts in microbial community composition. Such effects, however, were mediated by the amount of copper in the soils, with low-copper soil microcosms showing the strongest response to MB. Furthermore, MB-SB2 had a stronger effect, likely due to its higher affinity for copper. The presence of either form of MB also inhibited nitrite reduction and generally increased the presence of genes encoding for the iron-containing nitrite reductase (nirS) over the copper-dependent nitrite reductase (nirK). Lastly, these data indicate the methanotrophic-mediated production of MB can significantly impact multiple steps of denitrification, as well as have broad effects on microbial community composition of forest soils.

View Accepted Manuscript (DOE)

Research Organization:: University of Michigan, Ann Arbor, MI (United States)

Sponsoring Organization:: USDOE; USDOE Office of Science (SC)

Grant/Contract Number:: SC0020174

OSTI ID:: 1991190

Alternate ID(s):: OSTI ID: 1995609

Journal Information:: Environmental Microbiology, Journal Name: Environmental Microbiology Journal Issue: 11 Vol. 25; ISSN 1462-2912

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

References (76)

Insight into Metal Removal from Peptides that Sequester Copper for Methane Oxidation Baslé, Arnaud; El Ghazouani, Abdelnasser; Lee, Jaeick Chemistry – A European Journal, Vol. 24, Issue 18 https://doi.org/10.1002/chem.201706035	journal	February 2018
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
Multicopper oxidases: modular structure, sequence space, and evolutionary relationships Gräff, Maike; Buchholz, Patrick C. F.; Le Roes‐Hill, Marilize Proteins: Structure, Function, and Bioinformatics, Vol. 88, Issue 10 https://doi.org/10.1002/prot.25952	journal	June 2020
Cu, Zn superoxide dismutase structure from a microbial pathogen establishes a class with a conserved dimer interface 1 1Edited by D. C. Rees Forest, Katrina T.; Langford, Paul R.; Kroll, J. Simon Journal of Molecular Biology, Vol. 296, Issue 1 https://doi.org/10.1006/jmbi.1999.3448	journal	February 2000
Copper stress underlies the fundamental change in intracellular location of methane mono-oxygenase in methane-oxidizing organisms: Studies in batch and continuous cultures Stanley, S. H.; Prior, S. D.; Leak, D. J. Biotechnology Letters, Vol. 5, Issue 7 https://doi.org/10.1007/BF00132233	journal	July 1983
Oxygen profiles and methane turnover in a flooded rice microcosm Frenzel, Peter; Rothfuss, Franz; Conrad, Ralf Biology and Fertility of Soils, Vol. 14, Issue 2 https://doi.org/10.1007/BF00336255	journal	October 1992
Methane oxidation in the soil surface layer of a flooded rice field and the effect of ammonium Conrad, R.; Rothfuss, F. Biology and Fertility of Soils, Vol. 12, Issue 1 https://doi.org/10.1007/BF00369384	journal	September 1991
The model structure of the copper-dependent ammonia monooxygenase Musiani, Francesco; Broll, Valquiria; Evangelisti, Elisa JBIC Journal of Biological Inorganic Chemistry, Vol. 25, Issue 7 https://doi.org/10.1007/s00775-020-01820-0	journal	September 2020
Stress-related ecophysiology of members of the genus Rhodanobacter isolated from a mixed waste contaminated subsurface Prakash, Om; Green, Stefan J.; Singh, Pooja Frontiers of Environmental Science & Engineering, Vol. 15, Issue 2 https://doi.org/10.1007/s11783-020-1315-0	journal	September 2020
Determination of Cd, Cu, Pb and Zn in environmental samples: microwave-assisted total digestion versus aqua regia and nitric acid extraction Sastre, J.; Sahuquillo, A.; Vidal, M. Analytica Chimica Acta, Vol. 462, Issue 1 https://doi.org/10.1016/S0003-2670(02)00307-0	journal	June 2002
Cytochrome aa3 from Nitrosomonas europaea. Dispirito, A. A.; Lipscomb, J. D.; Hooper, A. B. Journal of Biological Chemistry, Vol. 261, Issue 36 https://doi.org/10.1016/S0021-9258(19)75997-3	journal	December 1986
Regulation of expression of methane monooxygenases by copper ions Murrell, J. Colin; McDonald, Ian R.; Gilbert, Bettina Trends in Microbiology, Vol. 8, Issue 5, p. 221-225 https://doi.org/10.1016/S0966-842X(00)01739-X	journal	May 2000
Nitrous oxide reductase Pauleta, Sofia R.; Dell’Acqua, Simone; Moura, Isabel Coordination Chemistry Reviews, Vol. 257, Issue 2 https://doi.org/10.1016/j.ccr.2012.05.026	journal	January 2013
The nitrogen cycle Stein, Lisa Y.; Klotz, Martin G. Current Biology, Vol. 26, Issue 3 https://doi.org/10.1016/j.cub.2015.12.021	journal	February 2016
Extractable DOC and DON from a dry-land long-term rotation and cropping system in Texas, USA Carrillo-Gonzalez, R.; Gonzalez-Chavez, M. C. A.; Aitkenhead-Peterson, J. A. Geoderma, Vol. 197-198 https://doi.org/10.1016/j.geoderma.2012.12.019	journal	April 2013
Microbial nitrate respiration – Genes, enzymes and environmental distribution Kraft, Beate; Strous, Marc; Tegetmeyer, Halina E. Journal of Biotechnology, Vol. 155, Issue 1 https://doi.org/10.1016/j.jbiotec.2010.12.025	journal	August 2011
Potential of a novel facultative anaerobic denitrifying Cupriavidus sp. W12 to remove fluoride and calcium through calcium bioprecipitation Liu, Jiaran; Su, Junfeng; Ali, Amjad Journal of Hazardous Materials, Vol. 423 https://doi.org/10.1016/j.jhazmat.2021.126976	journal	February 2022
Spectral and thermodynamic properties of Ag(I), Au(III), Cd(II), Co(II), Fe(III), Hg(II), Mn(II), Ni(II), Pb(II), U(IV), and Zn(II) binding by methanobactin from Methylosinus trichosporium OB3b Choi, Dong W.; Do, Young S.; Zea, Corbin J. Journal of Inorganic Biochemistry, Vol. 100, Issue 12, p. 2150-2161 https://doi.org/10.1016/j.jinorgbio.2006.08.017	journal	December 2006
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
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
Copper limiting threshold in the terrestrial ammonia oxidizing archaeon Nitrososphaera viennensis Reyes, Carolina; Hodgskiss, Logan H.; Baars, Oliver Research in Microbiology, Vol. 171, Issue 3-4 https://doi.org/10.1016/j.resmic.2020.01.003	journal	April 2020
Fungal denitrification revisited – Recent advancements and future opportunities Aldossari, Nouf; Ishii, Satoshi Soil Biology and Biochemistry, Vol. 157 https://doi.org/10.1016/j.soilbio.2021.108250	journal	June 2021
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
The Catalytic Center in Nitrous Oxide Reductase, Cu _Z , Is a Copper−Sulfide Cluster Rasmussen, Tim; Berks, Ben C.; Sanders-Loehr, Joann Biochemistry, Vol. 39, Issue 42 https://doi.org/10.1021/bi001811i	journal	September 2000
Purification, Characterization, and Preliminary Crystallographic Study of Copper-Containing Nitrous Oxide Reductase from Pseudomonas nautica 617 Prudêncio, Miguel; Pereira, Alice S.; Tavares, Pedro Biochemistry, Vol. 39, Issue 14 https://doi.org/10.1021/bi9926328	journal	March 2000
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
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
Stimulation by ammonium-based fertilizers of methane oxidation in soil around rice roots Bodelier, Paul L. E.; Roslev, Peter; Henckel, Thilo Nature, Vol. 403, Issue 6768 https://doi.org/10.1038/35000193	journal	January 2000
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
Applying stable isotope probing of phospholipid fatty acids and rRNA in a Chinese rice field to study activity and composition of the methanotrophic bacterial communities in situ Qiu, Qiongfen; Noll, Matthias; Abraham, Wolf-Rainer The ISME Journal, Vol. 2, Issue 6 https://doi.org/10.1038/ismej.2008.34	journal	April 2008
Structural basis of inter-protein electron transfer for nitrite reduction in denitrification Nojiri, Masaki; Koteishi, Hiroyasu; Nakagami, Takuya Nature, Vol. 462, Issue 7269 https://doi.org/10.1038/nature08507	journal	November 2009
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
Copper import in Escherichia coli by the yersiniabactin metallophore system Koh, Eun-Ik; Robinson, Anne E.; Bandara, Nilantha Nature Chemical Biology, Vol. 13, Issue 9 https://doi.org/10.1038/nchembio.2441	journal	July 2017
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
Global prevalence of methane oxidation by symbiotic bacteria in peat-moss ecosystems Kip, Nardy; van Winden, Julia F.; Pan, Yao Nature Geoscience, Vol. 3, Issue 9 https://doi.org/10.1038/ngeo939	journal	August 2010
DADA2: High-resolution sample inference from Illumina amplicon data Callahan, Benjamin J.; McMurdie, Paul J.; Rosen, Michael J. Nature Methods, Vol. 13, Issue 7 https://doi.org/10.1038/nmeth.3869	journal	May 2016
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
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
Aerobic methane oxidation under copper scarcity in a stratified lake Guggenheim, Carole; Brand, Andreas; Bürgmann, Helmut Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-40642-2	journal	March 2019
Copper-dependent reciprocal transcriptional regulation of methane monooxygenase genes in Methylococcus capsulatus and Methylosinus trichosporium Nielsen, Allan K.; Gerdes, Kenn; Murrell, J. Colin Molecular Microbiology, Vol. 25, Issue 02 https://doi.org/10.1046/j.1365-2958.1997.4801846.x	journal	July 1997
Effects of O2 and CH4 on presence and activity of the indigenous methanotrophic community in rice field soil Henckel, Thilo; Roslev, Peter; Conrad, Ralf Environmental Microbiology, Vol. 2, Issue 6 https://doi.org/10.1046/j.1462-2920.2000.00149.x	journal	December 2000
Structure and function of a hexameric copper-containing nitrite reductase Nojiri, Masaki; Xie, Yong; Inoue, Tsuyoshi Proceedings of the National Academy of Sciences, Vol. 104, Issue 11 https://doi.org/10.1073/pnas.0609195104	journal	March 2007
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 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
Bacterial Evolutionary Precursors of Eukaryotic Copper–Zinc Superoxide Dismutases Wright, Gareth S. A. Molecular Biology and Evolution, Vol. 38, Issue 9 https://doi.org/10.1093/molbev/msab157	journal	May 2021
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools Quast, Christian; Pruesse, Elmar; Yilmaz, Pelin Nucleic Acids Research, Vol. 41, Issue D1 https://doi.org/10.1093/nar/gks1219	journal	November 2012
Rhodanobacter denitrificans sp. nov., isolated from nitrate-rich zones of a contaminated aquifer Prakash, Om; Green, Stefan J.; Jasrotia, Puja International Journal of Systematic and Evolutionary Microbiology, Vol. 62, Issue Pt_10 https://doi.org/10.1099/ijs.0.035840-0	journal	October 2012
Small-scale oxygen distribution determines the vinyl chloride biodegradation pathway in surficial sediments of riverbed hyporheic zones Atashgahi, Siavash; Maphosa, Farai; Doğan, Eylem FEMS Microbiology Ecology, Vol. 84, Issue 1 https://doi.org/10.1111/1574-6941.12044	journal	December 2012
Dissolved organic nitrogen and carbon in pastoral soils: the New Zealand experience Ghani, A.; Dexter, M.; Carran, R. A. European Journal of Soil Science, Vol. 58, Issue 3 https://doi.org/10.1111/j.1365-2389.2006.00873.x	journal	June 2007
Diversity of the active methanotrophic community in acidic peatlands as assessed by mRNA and SIP-PLFA analyses Chen, Yin; Dumont, Marc G.; McNamara, Niall P. Environmental Microbiology, Vol. 10, Issue 2 https://doi.org/10.1111/j.1462-2920.2007.01466.x	journal	February 2008
Selective stimulation of type I methanotrophs in a rice paddy soil by urea fertilization revealed by RNA-based stable isotope probing Noll, Matthias; Frenzel, Peter; Conrad, Ralf FEMS Microbiology Ecology, Vol. 65, Issue 1 https://doi.org/10.1111/j.1574-6941.2008.00497.x	journal	July 2008
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
The Biogeochemical Cycles of Trace Metals in the Oceans Morel, F. M. M. Science, Vol. 300, Issue 5621 https://doi.org/10.1126/science.1083545	journal	May 2003
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
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
Cell biology and molecular basis of denitrification. Zumft, W. G. Microbiology and molecular biology reviews : MMBR, Vol. 61, Issue 4 https://doi.org/10.1128/.61.4.533-616.1997	journal	January 1997
Detection and Diversity of Fungal Nitric Oxide Reductase Genes ( p450nor ) in Agricultural Soils Higgins, Steven A.; Welsh, Allana; Orellana, Luis H. Applied and Environmental Microbiology, Vol. 82, Issue 10 https://doi.org/10.1128/AEM.00243-16	journal	March 2016
Development of a Dual-Index Sequencing Strategy and Curation Pipeline for Analyzing Amplicon Sequence Data on the MiSeq Illumina Sequencing Platform Kozich, James J.; Westcott, Sarah L.; Baxter, Nielson T. Applied and Environmental Microbiology, Vol. 79, Issue 17 https://doi.org/10.1128/AEM.01043-13	journal	June 2013
MbnC Is Not Required for the Formation of the N-Terminal Oxazolone in the Methanobactin from Methylosinus trichosporium OB3b Dershwitz, Philip; Gu, Wenyu; Roche, Julien Applied and Environmental Microbiology, Vol. 88, Issue 2 https://doi.org/10.1128/AEM.01841-21	journal	January 2022
Metals and Methanotrophy Semrau, Jeremy D.; DiSpirito, Alan A.; Gu, Wenyu Applied and Environmental Microbiology, Vol. 84, Issue 6 https://doi.org/10.1128/AEM.02289-17	journal	January 2018
Enhancement of Nitrous Oxide Emissions in Soil Microbial Consortia via Copper Competition between Proteobacterial Methanotrophs and Denitrifiers Chang, Jin; Kim, Daehyun D.; Semrau, Jeremy D. Applied and Environmental Microbiology, Vol. 87, Issue 5 https://doi.org/10.1128/AEM.02301-20	journal	February 2021
Activity-Based Protein Profiling of Ammonia Monooxygenase in Nitrosomonas europaea Bennett, Kristen; Sadler, Natalie C.; Wright, Aaron T. Applied and Environmental Microbiology, Vol. 82, Issue 8 https://doi.org/10.1128/AEM.03556-15	journal	April 2016
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
Methane and Trichloroethylene Degradation byMethylosinus trichosporium OB3b Expressing Particulate Methane Monooxygenase Lontoh, Sonny; Semrau, Jeremy D. Applied and Environmental Microbiology, Vol. 64, Issue 3 https://doi.org/10.1128/AEM.64.3.1106-1114.1998	journal	March 1998
Investigation of an Acetate-Fed Denitrifying Microbial Community by Stable Isotope Probing, Full-Cycle rRNA Analysis, and Fluorescent In Situ Hybridization-Microautoradiography Ginige, M. P.; Keller, J.; Blackall, L. L. Applied and Environmental Microbiology, Vol. 71, Issue 12 https://doi.org/10.1128/AEM.71.12.8683-8691.2005	journal	December 2005
The Membrane-Associated Methane Monooxygenase (pMMO) and pMMO-NADH:Quinone Oxidoreductase Complex from Methylococcus capsulatus Bath Choi, Dong-W.; Kunz, Ryan C.; Boyd, Eric S. Journal of Bacteriology, Vol. 185, Issue 19 https://doi.org/10.1128/JB.185.19.5755-5764.2003	journal	September 2003
Linkage between Catecholate Siderophores and the Multicopper Oxidase CueO in Escherichia coli Grass, G.; Thakali, K.; Klebba, P. E. Journal of Bacteriology, Vol. 186, Issue 17 https://doi.org/10.1128/JB.186.17.5826-5833.2004	journal	August 2004
Methanobactin and the Link between Copper and Bacterial Methane Oxidation DiSpirito, Alan A.; Semrau, Jeremy D.; Murrell, J. Colin Microbiology and Molecular Biology Reviews, Vol. 80, Issue 2 https://doi.org/10.1128/MMBR.00058-15	journal	March 2016
Variable Inhibition of Nitrous Oxide Reduction in Denitrifying Bacteria by Different Forms of Methanobactin Chang, Jin; Peng, Peng; DiSpirito, Alan A. Applied and Environmental Microbiology, Vol. 88, Issue 7 https://doi.org/10.1128/aem.02346-21	journal	April 2022
In vitro activation of ammonia monooxygenase from Nitrosomonas europaea by copper. Ensign, S. A.; Hyman, M. R.; Arp, D. J. Journal of Bacteriology, Vol. 175, Issue 7 https://doi.org/10.1128/jb.175.7.1971-1980.1993	journal	April 1993
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
Methanotrophic bacteria. Hanson, R. S.; Hanson, T. E. Microbiological reviews, Vol. 60, Issue 2 https://doi.org/10.1128/mr.60.2.439-471.1996	journal	January 1996
CYTOCHROME C OXIDASE: Structure and Spectroscopy Michel, H.; Behr, J.; Harrenga, A. Annual Review of Biophysics and Biomolecular Structure, Vol. 27, Issue 1 https://doi.org/10.1146/annurev.biophys.27.1.329	journal	June 1998
Metagenomic biomarker discovery and explanation Segata, Nicola; Izard, Jacques; Waldron, Levi Genome Biology, Vol. 12, Issue 6 https://doi.org/10.1186/gb-2011-12-6-r60	journal	January 2011
phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data McMurdie, Paul J.; Holmes, Susan PLoS ONE, Vol. 8, Issue 4 https://doi.org/10.1371/journal.pone.0061217	journal	April 2013
The Global Methane Budget 2000–2017 Saunois, Marielle; Stavert, Ann R.; Poulter, Ben Earth System Science Data, Vol. 12, Issue 3 https://doi.org/10.5194/essd-12-1561-2020	journal	January 2020

Similar Records

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

Journal Article · Sun Mar 13 20:00:00 EDT 2022 · Applied and Environmental Microbiology · OSTI ID:1865104

Related Subjects

54 ENVIRONMENTAL SCIENCES
59 BASIC BIOLOGICAL SCIENCES
60 APPLIED LIFE SCIENCES
biogenic global cycles
metals
microbial communities
microbially-influenced global change
soil microbes

Inhibition of nitrous oxide reduction in forest soil microcosms by different forms of methanobactin

Citation Formats

References (76)

Similar Records

Related Subjects