A nitrogenase-like enzyme system catalyzes methionine, ethylene, and methane biogenesis
Abstract
Bacterial production of gaseous hydrocarbons such as ethylene and methane affects soil environments and atmospheric climate. We demonstrate that biogenic methane and ethylene from terrestrial and freshwater bacteria are directly produced by a previously unknown methionine biosynthesis pathway. This pathway, present in numerous species, uses a nitrogenase-like reductase that is distinct from known nitrogenases and nitrogenase-like reductases and specifically functions in C–S bond breakage to reduce ubiquitous and appreciable volatile organic sulfur compounds such as dimethyl sulfide and (2-methylthio)ethanol. Liberated methanethiol serves as the immediate precursor to methionine, while ethylene or methane is released into the environment. Anaerobic ethylene production by this pathway apparently explains the long-standing observation of ethylene accumulation in oxygen-depleted soils. Methane production reveals an additional bacterial pathway distinct from archaeal methanogenesis.
- Authors:
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[1];
[2];
[3];
[1];
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[1];
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[4];
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- The Ohio State Univ., Columbus, OH (United States)
- Colorado State Univ., Fort Collins, CO (United States)
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Chemical Sciences Division
- Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
- Publication Date:
- Research Org.:
- The Ohio State Univ., Columbus, OH (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); NCI
- Contributing Org.:
- University of Colorado Cancer Center’s Genomics and Microarray Core Shared Resource; University of Colorado Boulder Research Computing Group; Environmental Molecular Sciences Laboratory; Battelle and UT-Battelle, LLC
- OSTI Identifier:
- 1658249
- Alternate Identifier(s):
- OSTI ID: 1813253
- Grant/Contract Number:
- SC0019338; AC05-76RLO1830; P30CA046934; AC05-00OR22725
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Science (Online)
- Additional Journal Information:
- Journal Name: Science (Online); Journal Volume: 369; Journal Issue: 6507; Related Information: All raw mass spectraand searched data files for the proteome measurements have beendeposited into the ProteomeXchange repository: MassIVE accessionnumber MSV000084455 (FTP link to files: ftp://massive.ucsd.edu/MSV000084455/) and ProteomeXchange accession numberPXD015818. Raw transcriptomics reads are available in the NCBISequence Read Archive under accession numbers SRR10887327through SRR10887338 and BioProject accession number PRJNA601207.; Journal ID: ISSN 1095-9203
- Publisher:
- AAAS
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; 54 ENVIRONMENTAL SCIENCES; 10 SYNTHETIC FUELS; Nitrogenase; ethylene; methane; dimethyl sulfide; soil; sulfur; bacteria
Citation Formats
North, Justin A, Narrowe, Adrienne B, Xiong, Weili, Byerly, Kathryn M, Zhao, Guanqi, Young, Sarah J, Murali, Srividya, Wildenthal, John A, Cannon, William R, Wrighton, Kelly C, Hettich, Robert L, and Tabita, Fred Robert. A nitrogenase-like enzyme system catalyzes methionine, ethylene, and methane biogenesis. United States: N. p., 2020.
Web. doi:10.1126/science.abb6310.
North, Justin A, Narrowe, Adrienne B, Xiong, Weili, Byerly, Kathryn M, Zhao, Guanqi, Young, Sarah J, Murali, Srividya, Wildenthal, John A, Cannon, William R, Wrighton, Kelly C, Hettich, Robert L, & Tabita, Fred Robert. A nitrogenase-like enzyme system catalyzes methionine, ethylene, and methane biogenesis. United States. https://doi.org/10.1126/science.abb6310
North, Justin A, Narrowe, Adrienne B, Xiong, Weili, Byerly, Kathryn M, Zhao, Guanqi, Young, Sarah J, Murali, Srividya, Wildenthal, John A, Cannon, William R, Wrighton, Kelly C, Hettich, Robert L, and Tabita, Fred Robert. Fri .
"A nitrogenase-like enzyme system catalyzes methionine, ethylene, and methane biogenesis". United States. https://doi.org/10.1126/science.abb6310. https://www.osti.gov/servlets/purl/1658249.
@article{osti_1658249,
title = {A nitrogenase-like enzyme system catalyzes methionine, ethylene, and methane biogenesis},
author = {North, Justin A and Narrowe, Adrienne B and Xiong, Weili and Byerly, Kathryn M and Zhao, Guanqi and Young, Sarah J and Murali, Srividya and Wildenthal, John A and Cannon, William R and Wrighton, Kelly C and Hettich, Robert L and Tabita, Fred Robert},
abstractNote = {Bacterial production of gaseous hydrocarbons such as ethylene and methane affects soil environments and atmospheric climate. We demonstrate that biogenic methane and ethylene from terrestrial and freshwater bacteria are directly produced by a previously unknown methionine biosynthesis pathway. This pathway, present in numerous species, uses a nitrogenase-like reductase that is distinct from known nitrogenases and nitrogenase-like reductases and specifically functions in C–S bond breakage to reduce ubiquitous and appreciable volatile organic sulfur compounds such as dimethyl sulfide and (2-methylthio)ethanol. Liberated methanethiol serves as the immediate precursor to methionine, while ethylene or methane is released into the environment. Anaerobic ethylene production by this pathway apparently explains the long-standing observation of ethylene accumulation in oxygen-depleted soils. Methane production reveals an additional bacterial pathway distinct from archaeal methanogenesis.},
doi = {10.1126/science.abb6310},
journal = {Science (Online)},
number = 6507,
volume = 369,
place = {United States},
year = {2020},
month = {8}
}
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Works referenced in this record:
Isotopic evidence for biological nitrogen fixation by molybdenum-nitrogenase from 3.2 Gyr
journal, February 2015
- Stüeken, Eva E.; Buick, Roger; Guy, Bradley M.
- Nature, Vol. 520, Issue 7549
The physiology and habitat of the last universal common ancestor
journal, July 2016
- Weiss, Madeline C.; Sousa, Filipa L.; Mrnjavac, Natalia
- Nature Microbiology, Vol. 1, Issue 9
New insights into the evolutionary history of biological nitrogen fixation
journal, January 2013
- Boyd, Eric S.; Peters, John W.
- Frontiers in Microbiology, Vol. 4
The biosynthetic pathway of coenzyme F430 in methanogenic and methanotrophic archaea
journal, October 2016
- Zheng, Kaiyuan; Ngo, Phong D.; Owens, Victoria L.
- Science, Vol. 354, Issue 6310
Elucidation of the biosynthesis of the methane catalyst coenzyme F430
journal, February 2017
- Moore, Simon J.; Sowa, Sven T.; Schuchardt, Christopher
- Nature, Vol. 543, Issue 7643
X-ray crystal structure of the light-independent protochlorophyllide reductase
journal, May 2010
- Muraki, Norifumi; Nomata, Jiro; Ebata, Kozue
- Nature, Vol. 465, Issue 7294
A Second Nitrogenase-like Enzyme for Bacteriochlorophyll Biosynthesis: RECONSTITUTION OF CHLOROPHYLLIDE a REDUCTASE WITH PURIFIED X-PROTEIN (BchX) AND YZ-PROTEIN (BchY-BchZ) FROM RHODOBACTER CAPSULATUS
journal, March 2006
- Nomata, Jiro; Mizoguchi, Tadashi; Tamiaki, Hitoshi
- Journal of Biological Chemistry, Vol. 281, Issue 21
Distribution of nitrogen fixation and nitrogenase-like sequences amongst microbial genomes
journal, January 2012
- Dos Santos, Patricia C.; Fang, Zhong; Mason, Steven W.
- BMC Genomics, Vol. 13, Issue 1
The Natural History of Nitrogen Fixation
journal, March 2004
- Raymond, Jason; Siefert, Janet L.; Staples, Christopher R.
- Molecular Biology and Evolution, Vol. 21, Issue 3
Microbial pathway for anaerobic 5′-methylthioadenosine metabolism coupled to ethylene formation
journal, November 2017
- North, Justin A.; Miller, Anthony R.; Wildenthal, John A.
- Proceedings of the National Academy of Sciences, Vol. 114, Issue 48
Methylthioadenosine/S-adenosylhomocysteine nucleosidase, a critical enzyme for bacterial metabolism: Involvement of MTA/SAH nucleosidase in bacterial metabolism
journal, November 2010
- Parveen, Nikhat; Cornell, Kenneth A.
- Molecular Microbiology, Vol. 79, Issue 1
Biosynthesis of Nitrogenase Cofactors
journal, January 2020
- Burén, Stefan; Jiménez-Vicente, Emilio; Echavarri-Erasun, Carlos
- Chemical Reviews, Vol. 120, Issue 12
Mutagenesis and Functional Characterization of theglnB, glnA, and nifA Genes from the Photosynthetic Bacterium Rhodospirillum rubrum
journal, February 2000
- Zhang, Yaoping; Pohlmann, Edward L.; Ludden, Paul W.
- Journal of Bacteriology, Vol. 182, Issue 4
A RubisCO-like protein links SAM metabolism with isoprenoid biosynthesis
journal, October 2012
- Erb, Tobias J.; Evans, Bradley S.; Cho, Kyuil
- Nature Chemical Biology, Vol. 8, Issue 11
The structure of vanadium nitrogenase reveals an unusual bridging ligand
journal, July 2017
- Sippel, Daniel; Einsle, Oliver
- Nature Chemical Biology, Vol. 13, Issue 9
Nitrogenase MoFe protein from Clostridium pasteurianum at 1.08 Å resolution: comparison with the Azotobacter vinelandii MoFe protein
journal, January 2015
- Zhang, Li-Mei; Morrison, Christine N.; Kaiser, Jens T.
- Acta Crystallographica Section D Biological Crystallography, Vol. 71, Issue 2
A bound reaction intermediate sheds light on the mechanism of nitrogenase
journal, March 2018
- Sippel, Daniel; Rohde, Michael; Netzer, Julia
- Science, Vol. 359, Issue 6383
Aquatic and terrestrial cyanobacteria produce methane
journal, January 2020
- Bižić, M.; Klintzsch, T.; Ionescu, D.
- Science Advances, Vol. 6, Issue 3
Marine methane paradox explained by bacterial degradation of dissolved organic matter
journal, November 2016
- Repeta, Daniel J.; Ferrón, Sara; Sosa, Oscar A.
- Nature Geoscience, Vol. 9, Issue 12
A pathway for biological methane production using bacterial iron-only nitrogenase
journal, January 2018
- Zheng, Yanning; Harris, Derek F.; Yu, Zheng
- Nature Microbiology, Vol. 3, Issue 3
Occurrence of Ethylene, and its Significance, in Anaerobic Soil
journal, May 1969
- Smith, K. A.; Russell, R. Scott
- Nature, Vol. 222, Issue 5195
Soil and Crop Management Practices to Minimize the Impact of Waterlogging on Crop Productivity
journal, February 2019
- Manik, S. M. Nuruzzaman; Pengilley, Georgina; Dean, Geoffrey
- Frontiers in Plant Science, Vol. 10
Identification of Substrates and Isolation of Microorganisms responsible for Ethylene Production in the Soil
journal, November 1972
- Lynch, J. M.
- Nature, Vol. 240, Issue 5375
A bifunctional salvage pathway for two distinct S‐adenosylmethionine byproducts that is widespread in bacteria, including pathogenic Escherichia coli
journal, January 2020
- North, Justin A.; Wildenthal, John A.; Erb, Tobias J.
- Molecular Microbiology
Salvage of the 5-deoxyribose byproduct of radical SAM enzymes
journal, August 2018
- Beaudoin, Guillaume A. W.; Li, Qiang; Folz, Jacob
- Nature Communications, Vol. 9, Issue 1
E ndomicrobium proavitum , the first isolate of E ndomicrobia class. nov. (phylum E lusimicrobia ) - an ultramicrobacterium with an unusual cell cycle that fixes nitrogen with a Group IV nitrogenase
journal, July 2015
- Zheng, Hao; Dietrich, Carsten; Radek, Renate
- Environmental Microbiology, Vol. 18, Issue 1
Mechanistic Diversity in the RuBisCO Superfamily: The “Enolase” in the Methionine Salvage Pathway in Geobacillus kaustophilus † , ‡
journal, April 2007
- Imker, Heidi J.; Fedorov, Alexander A.; Fedorov, Elena V.
- Biochemistry, Vol. 46, Issue 13
Roles of RubisCO and the RubisCO-Like Protein in 5-Methylthioadenosine Metabolism in the Nonsulfur Purple Bacterium Rhodospirillum rubrum
journal, December 2009
- Singh, J.; Tabita, F. R.
- Journal of Bacteriology, Vol. 192, Issue 5
Complete Genome Sequence of the Photosynthetic Purple Nonsulfur Bacterium Rhodobacter capsulatus SB 1003
journal, April 2010
- Strnad, Hynek; Lapidus, Alla; Paces, Jan
- Journal of Bacteriology, Vol. 192, Issue 13
Regulation of Uptake Hydrogenase and Effects of Hydrogen Utilization on Gene Expression in Rhodopseudomonas palustris
journal, August 2006
- Rey, F. E.; Oda, Y.; Harwood, C. S.
- Journal of Bacteriology, Vol. 188, Issue 17
Rhodopseudomonas viridis, nov. spec., ein neu isoliertes, obligat phototrophes Bakterium
journal, January 1966
- Drews, G.; Giesbrecht, P.
- Archiv f�r Mikrobiologie, Vol. 53, Issue 3
Light-dependent utilization of organic compounds and photoproduction of molecular hydrogen by photosynthetic bacteria; relationships with nitrogen metabolism
journal, September 1961
- Ormerod, John G.; Ormerod, Kari S.; Gest, Howard
- Archives of Biochemistry and Biophysics, Vol. 94, Issue 3
In Vivo Studies in Rhodospirillum rubrum Indicate That Ribulose-1,5-bisphosphate Carboxylase/Oxygenase (Rubisco) Catalyzes Two Obligatorily Required and Physiologically Significant Reactions for Distinct Carbon and Sulfur Metabolic Pathways
journal, October 2015
- Dey, Swati; North, Justin A.; Sriram, Jaya
- Journal of Biological Chemistry, Vol. 290, Issue 52
Engineered biosynthesis of bacteriochlorophyll b in Rhodobacter sphaeroides
journal, October 2014
- Canniffe, Daniel P.; Hunter, C. Neil
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1837, Issue 10
MyriMatch: Highly Accurate Tandem Mass Spectral Peptide Identification by Multivariate Hypergeometric Analysis
journal, February 2007
- Tabb, David L.; Fernando, Christopher G.; Chambers, Matthew C.
- Journal of Proteome Research, Vol. 6, Issue 2
IDPicker 2.0: Improved Protein Assembly with High Discrimination Peptide Identification Filtering
journal, August 2009
- Ma, Ze-Qiang; Dasari, Surendra; Chambers, Matthew C.
- Journal of Proteome Research, Vol. 8, Issue 8
DanteR: an extensible R-based tool for quantitative analysis of -omics data
journal, July 2012
- Taverner, Tom; Karpievitch, Yuliya V.; Polpitiya, Ashoka D.
- Bioinformatics, Vol. 28, Issue 18
The Perseus computational platform for comprehensive analysis of (prote)omics data
journal, June 2016
- Tyanova, Stefka; Temu, Tikira; Sinitcyn, Pavel
- Nature Methods, Vol. 13, Issue 9
Fast gapped-read alignment with Bowtie 2
journal, March 2012
- Langmead, Ben; Salzberg, Steven L.
- Nature Methods, Vol. 9, Issue 4
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
journal, December 2014
- Love, Michael I.; Huber, Wolfgang; Anders, Simon
- Genome Biology, Vol. 15, Issue 12
Genetic analysis of pigment biosynthesis in Xanthobacter autotrophicus Py2 using a new, highly efficient transposon mutagenesis system that is functional in a wide variety of bacteria
journal, September 2002
- Larsen, Rachel; Wilson, Marlena; Guss, Adam
- Archives of Microbiology, Vol. 178, Issue 3
Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans
journal, April 1979
- Figurski, D. H.; Helinski, D. R.
- Proceedings of the National Academy of Sciences, Vol. 76, Issue 4
The Acetylene-Ethylene Assay for N 2 Fixation: Laboratory and Field Evaluation
journal, August 1968
- Hardy, R. W. F.; Holsten, R. D.; Jackson, E. K.
- Plant Physiology, Vol. 43, Issue 8
Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density
journal, January 1988
- Lee, Chengteh; Yang, Weitao; Parr, Robert G.
- Physical Review B, Vol. 37, Issue 2
Density‐functional thermochemistry. III. The role of exact exchange
journal, April 1993
- Becke, Axel D.
- The Journal of Chemical Physics, Vol. 98, Issue 7, p. 5648-5652
COSMO: a new approach to dielectric screening in solvents with explicit expressions for the screening energy and its gradient
journal, January 1993
- Klamt, A.; Schüürmann, G.
- J. Chem. Soc., Perkin Trans. 2, Issue 5
NWChem: A comprehensive and scalable open-source solution for large scale molecular simulations
journal, September 2010
- Valiev, M.; Bylaska, E. J.; Govind, N.
- Computer Physics Communications, Vol. 181, Issue 9, p. 1477-1489
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability
journal, January 2013
- Katoh, K.; Standley, D. M.
- Molecular Biology and Evolution, Vol. 30, Issue 4
trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses
journal, June 2009
- Capella-Gutierrez, S.; Silla-Martinez, J. M.; Gabaldon, T.
- Bioinformatics, Vol. 25, Issue 15
IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies
journal, November 2014
- Nguyen, Lam-Tung; Schmidt, Heiko A.; von Haeseler, Arndt
- Molecular Biology and Evolution, Vol. 32, Issue 1
ModelFinder: fast model selection for accurate phylogenetic estimates
journal, May 2017
- Kalyaanamoorthy, Subha; Minh, Bui Quang; Wong, Thomas K. F.
- Nature Methods, Vol. 14, Issue 6
UFBoot2: Improving the Ultrafast Bootstrap Approximation
journal, October 2017
- Hoang, Diep Thi; Chernomor, Olga; von Haeseler, Arndt
- Molecular Biology and Evolution, Vol. 35, Issue 2
The EMBL-EBI search and sequence analysis tools APIs in 2019
journal, April 2019
- Madeira, Fábio; Park, Young mi; Lee, Joon
- Nucleic Acids Research, Vol. 47, Issue W1
Jalview Version 2--a multiple sequence alignment editor and analysis workbench
journal, January 2009
- Waterhouse, A. M.; Procter, J. B.; Martin, D. M. A.
- Bioinformatics, Vol. 25, Issue 9
GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database
journal, November 2019
- Chaumeil, Pierre-Alain; Mussig, Aaron J.; Hugenholtz, Philip
- Bioinformatics
Electron Transfer to Nitrogenase in Different Genomic and Metabolic Backgrounds
journal, February 2018
- Poudel, Saroj; Colman, Daniel R.; Fixen, Kathryn R.
- Journal of Bacteriology, Vol. 200, Issue 10
Mechanism of Nitrogen Fixation by Nitrogenase: The Next Stage
journal, January 2014
- Hoffman, Brian M.; Lukoyanov, Dmitriy; Yang, Zhi-Yong
- Chemical Reviews, Vol. 114, Issue 8
Characterization of the DraT/DraG System for Posttranslational Regulation of Nitrogenase in the Endophytic Betaproteobacterium Azoarcus sp. Strain BH72
journal, June 2009
- Oetjen, Janina; Reinhold-Hurek, Barbara
- Journal of Bacteriology, Vol. 191, Issue 11
ATP-driven Reduction by Dark-operative Protochlorophyllide Oxidoreductase from Chlorobium tepidum Mechanistically Resembles Nitrogenase Catalysis
journal, February 2008
- Bröcker, Markus J.; Virus, Simone; Ganskow, Stefanie
- Journal of Biological Chemistry, Vol. 283, Issue 16
Catalytic activities of NifEN: Implications for nitrogenase evolution and mechanism
journal, September 2009
- Hu, Y.; Yoshizawa, J. M.; Fay, A. W.
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 40