A nitrogenase-like enzyme system catalyzes methionine, ethylene, and methane biogenesis

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

doi:10.1126/science.abb6310

Title: A nitrogenase-like enzyme system catalyzes methionine, ethylene, and methane biogenesis

Journal Article · Fri Aug 28 00:00:00 EDT 2020 · Science (Online)

DOI: https://doi.org/10.1126/science.abb6310 · OSTI ID:1658249

^[1];

^[2];

^[3];

^[4];

^[5];

^[2];

^[3];

^[4]

The Ohio State Univ., Columbus, OH (United States); The Ohio State University
Colorado State Univ., Fort Collins, CO (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Chemical Sciences Division
The Ohio State Univ., Columbus, OH (United States)
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)

Bacterial production of hydrocarbon gases like ethylene and methane affects soil ecosystems and the climate. This study reveals that methane and ethylene from land and freshwater bacteria are directly produced by a previously unknown methionine biosynthesis pathway. This pathway employs a nitrogenase-like reductase that is distinct from known nitrogenases and nitrogenase-like reductases. The nitrogenase-like methylthio-alkane reductase specifically functions in carbon-sulfur bond breakage to reduce ubiquitous and significant volatile organic sulfur compounds such as dimethyl sulfide and (2-methylthio)ethanol. The liberated methanethiol serves as the immediate precursor to methionine. Whereas ethylene or methane is released into the environment. This pathway provides a biological route to the synthesis of ethylene in the absence of oxygen. Finally, 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 that is distinct from archaeal methanogenesis.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: The Ohio State Univ., Columbus, OH (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); NCI

Contributing Organization:: 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

Grant/Contract Number:: SC0019338

OSTI ID:: 1658249

Journal Information:: Science (Online), Journal Name: Science (Online) Journal Issue: 6507 Vol. 369; ISSN 1095-9203

Publisher:: AAASCopyright Statement

Country of Publication:: United States

Language:: English

References (61)

Rhodopseudomonas viridis, nov. spec., ein neu isoliertes, obligat phototrophes Bakterium Drews, G.; Giesbrecht, P. Archiv f�r Mikrobiologie, Vol. 53, Issue 3 https://doi.org/10.1007/BF00446672	journal	January 1966
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 Larsen, Rachel; Wilson, Marlena; Guss, Adam Archives of Microbiology, Vol. 178, Issue 3 https://doi.org/10.1007/s00203-002-0442-2	journal	September 2002
Light-dependent utilization of organic compounds and photoproduction of molecular hydrogen by photosynthetic bacteria; relationships with nitrogen metabolism Ormerod, John G.; Ormerod, Kari S.; Gest, Howard Archives of Biochemistry and Biophysics, Vol. 94, Issue 3 https://doi.org/10.1016/0003-9861(61)90073-X	journal	September 1961
Engineered biosynthesis of bacteriochlorophyll b in Rhodobacter sphaeroides Canniffe, Daniel P.; Hunter, C. Neil Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1837, Issue 10 https://doi.org/10.1016/j.bbabio.2014.07.011	journal	October 2014
NWChem: A comprehensive and scalable open-source solution for large scale molecular simulations Valiev, M.; Bylaska, E. J.; Govind, N. Computer Physics Communications, Vol. 181, Issue 9, p. 1477-1489 https://doi.org/10.1016/j.cpc.2010.04.018	journal	September 2010
Biosynthesis of Nitrogenase Cofactors Burén, Stefan; Jiménez-Vicente, Emilio; Echavarri-Erasun, Carlos Chemical Reviews, Vol. 120, Issue 12 https://doi.org/10.1021/acs.chemrev.9b00489	journal	January 2020
Mechanistic Diversity in the RuBisCO Superfamily: The “Enolase” in the Methionine Salvage Pathway in Geobacillus kaustophilus ^† ^, ^‡ Imker, Heidi J.; Fedorov, Alexander A.; Fedorov, Elena V. Biochemistry, Vol. 46, Issue 13 https://doi.org/10.1021/bi7000483	journal	April 2007
Mechanism of Nitrogen Fixation by Nitrogenase: The Next Stage Hoffman, Brian M.; Lukoyanov, Dmitriy; Yang, Zhi-Yong Chemical Reviews, Vol. 114, Issue 8 https://doi.org/10.1021/cr400641x	journal	January 2014
MyriMatch: Highly Accurate Tandem Mass Spectral Peptide Identification by Multivariate Hypergeometric Analysis Tabb, David L.; Fernando, Christopher G.; Chambers, Matthew C. Journal of Proteome Research, Vol. 6, Issue 2 https://doi.org/10.1021/pr0604054	journal	February 2007
IDPicker 2.0: Improved Protein Assembly with High Discrimination Peptide Identification Filtering Ma, Ze-Qiang; Dasari, Surendra; Chambers, Matthew C. Journal of Proteome Research, Vol. 8, Issue 8 https://doi.org/10.1021/pr900360j	journal	August 2009
Occurrence of Ethylene, and its Significance, in Anaerobic Soil Smith, K. A.; Russell, R. Scott Nature, Vol. 222, Issue 5195 https://doi.org/10.1038/222769b0	journal	May 1969
Identification of Substrates and Isolation of Microorganisms responsible for Ethylene Production in the Soil Lynch, J. M. Nature, Vol. 240, Issue 5375 https://doi.org/10.1038/240045a0	journal	November 1972
Ethylene in soil Lynch, J. M. Nature, Vol. 256, Issue 5518 https://doi.org/10.1038/256576a0	journal	August 1975
X-ray crystal structure of the light-independent protochlorophyllide reductase Muraki, Norifumi; Nomata, Jiro; Ebata, Kozue Nature, Vol. 465, Issue 7294 https://doi.org/10.1038/nature08950	journal	May 2010
Isotopic evidence for biological nitrogen fixation by molybdenum-nitrogenase from 3.2 Gyr Stüeken, Eva E.; Buick, Roger; Guy, Bradley M. Nature, Vol. 520, Issue 7549 https://doi.org/10.1038/nature14180	journal	February 2015
Elucidation of the biosynthesis of the methane catalyst coenzyme F430 Moore, Simon J.; Sowa, Sven T.; Schuchardt, Christopher Nature, Vol. 543, Issue 7643 https://doi.org/10.1038/nature21427	journal	February 2017
A RubisCO-like protein links SAM metabolism with isoprenoid biosynthesis Erb, Tobias J.; Evans, Bradley S.; Cho, Kyuil Nature Chemical Biology, Vol. 8, Issue 11 https://doi.org/10.1038/nchembio.1087	journal	October 2012
The structure of vanadium nitrogenase reveals an unusual bridging ligand Sippel, Daniel; Einsle, Oliver Nature Chemical Biology, Vol. 13, Issue 9 https://doi.org/10.1038/nchembio.2428	journal	July 2017
Marine methane paradox explained by bacterial degradation of dissolved organic matter Repeta, Daniel J.; Ferrón, Sara; Sosa, Oscar A. Nature Geoscience, Vol. 9, Issue 12 https://doi.org/10.1038/ngeo2837	journal	November 2016
Fast gapped-read alignment with Bowtie 2 Langmead, Ben; Salzberg, Steven L. Nature Methods, Vol. 9, Issue 4 https://doi.org/10.1038/nmeth.1923	journal	March 2012
The Perseus computational platform for comprehensive analysis of (prote)omics data Tyanova, Stefka; Temu, Tikira; Sinitcyn, Pavel Nature Methods, Vol. 13, Issue 9 https://doi.org/10.1038/nmeth.3901	journal	June 2016
ModelFinder: fast model selection for accurate phylogenetic estimates Kalyaanamoorthy, Subha; Minh, Bui Quang; Wong, Thomas K. F. Nature Methods, Vol. 14, Issue 6 https://doi.org/10.1038/nmeth.4285	journal	May 2017
The physiology and habitat of the last universal common ancestor Weiss, Madeline C.; Sousa, Filipa L.; Mrnjavac, Natalia Nature Microbiology, Vol. 1, Issue 9 https://doi.org/10.1038/nmicrobiol.2016.116	journal	July 2016
Salvage of the 5-deoxyribose byproduct of radical SAM enzymes Beaudoin, Guillaume A. W.; Li, Qiang; Folz, Jacob Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-05589-4	journal	August 2018
A pathway for biological methane production using bacterial iron-only nitrogenase Zheng, Yanning; Harris, Derek F.; Yu, Zheng Nature Microbiology, Vol. 3, Issue 3 https://doi.org/10.1038/s41564-017-0091-5	journal	January 2018
COSMO: a new approach to dielectric screening in solvents with explicit expressions for the screening energy and its gradient Klamt, A.; Schüürmann, G. J. Chem. Soc., Perkin Trans. 2, Issue 5 https://doi.org/10.1039/p29930000799	journal	January 1993
Density‐functional thermochemistry. III. The role of exact exchange Becke, Axel D. The Journal of Chemical Physics, Vol. 98, Issue 7, p. 5648-5652 https://doi.org/10.1063/1.464913	journal	April 1993
Catalytic activities of NifEN: Implications for nitrogenase evolution and mechanism Hu, Y.; Yoshizawa, J. M.; Fay, A. W. Proceedings of the National Academy of Sciences, Vol. 106, Issue 40 https://doi.org/10.1073/pnas.0907872106	journal	September 2009
Microbial pathway for anaerobic 5′-methylthioadenosine metabolism coupled to ethylene formation North, Justin A.; Miller, Anthony R.; Wildenthal, John A. Proceedings of the National Academy of Sciences, Vol. 114, Issue 48 https://doi.org/10.1073/pnas.1711625114	journal	November 2017
Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans Figurski, D. H.; Helinski, D. R. Proceedings of the National Academy of Sciences, Vol. 76, Issue 4 https://doi.org/10.1073/pnas.76.4.1648	journal	April 1979
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 Dey, Swati; North, Justin A.; Sriram, Jaya Journal of Biological Chemistry, Vol. 290, Issue 52 https://doi.org/10.1074/jbc.M115.691295	journal	October 2015
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 Nomata, Jiro; Mizoguchi, Tadashi; Tamiaki, Hitoshi Journal of Biological Chemistry, Vol. 281, Issue 21 https://doi.org/10.1074/jbc.M601750200	journal	March 2006
ATP-driven Reduction by Dark-operative Protochlorophyllide Oxidoreductase from Chlorobium tepidum Mechanistically Resembles Nitrogenase Catalysis Bröcker, Markus J.; Virus, Simone; Ganskow, Stefanie Journal of Biological Chemistry, Vol. 283, Issue 16 https://doi.org/10.1074/jbc.M708010200	journal	February 2008
Jalview Version 2--a multiple sequence alignment editor and analysis workbench Waterhouse, A. M.; Procter, J. B.; Martin, D. M. A. Bioinformatics, Vol. 25, Issue 9 https://doi.org/10.1093/bioinformatics/btp033	journal	January 2009
trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses Capella-Gutierrez, S.; Silla-Martinez, J. M.; Gabaldon, T. Bioinformatics, Vol. 25, Issue 15 https://doi.org/10.1093/bioinformatics/btp348	journal	June 2009
DanteR: an extensible R-based tool for quantitative analysis of -omics data Taverner, Tom; Karpievitch, Yuliya V.; Polpitiya, Ashoka D. Bioinformatics, Vol. 28, Issue 18 https://doi.org/10.1093/bioinformatics/bts449	journal	July 2012
GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database Chaumeil, Pierre-Alain; Mussig, Aaron J.; Hugenholtz, Philip Bioinformatics https://doi.org/10.1093/bioinformatics/btz848	journal	November 2019
The Natural History of Nitrogen Fixation Raymond, Jason; Siefert, Janet L.; Staples, Christopher R. Molecular Biology and Evolution, Vol. 21, Issue 3 https://doi.org/10.1093/molbev/msh047	journal	March 2004
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability Katoh, K.; Standley, D. M. Molecular Biology and Evolution, Vol. 30, Issue 4 https://doi.org/10.1093/molbev/mst010	journal	January 2013
IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies Nguyen, Lam-Tung; Schmidt, Heiko A.; von Haeseler, Arndt Molecular Biology and Evolution, Vol. 32, Issue 1 https://doi.org/10.1093/molbev/msu300	journal	November 2014
UFBoot2: Improving the Ultrafast Bootstrap Approximation Hoang, Diep Thi; Chernomor, Olga; von Haeseler, Arndt Molecular Biology and Evolution, Vol. 35, Issue 2 https://doi.org/10.1093/molbev/msx281	journal	October 2017
The EMBL-EBI search and sequence analysis tools APIs in 2019 Madeira, Fábio; Park, Young mi; Lee, Joon Nucleic Acids Research, Vol. 47, Issue W1 https://doi.org/10.1093/nar/gkz268	journal	April 2019
Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density Lee, Chengteh; Yang, Weitao; Parr, Robert G. Physical Review B, Vol. 37, Issue 2 https://doi.org/10.1103/PhysRevB.37.785	journal	January 1988
The Acetylene-Ethylene Assay for N ₂ Fixation: Laboratory and Field Evaluation Hardy, R. W. F.; Holsten, R. D.; Jackson, E. K. Plant Physiology, Vol. 43, Issue 8 https://doi.org/10.1104/pp.43.8.1185	journal	August 1968
Nitrogenase MoFe protein from Clostridium pasteurianum at 1.08 Å resolution: comparison with the Azotobacter vinelandii MoFe protein Zhang, Li-Mei; Morrison, Christine N.; Kaiser, Jens T. Acta Crystallographica Section D Biological Crystallography, Vol. 71, Issue 2 https://doi.org/10.1107/S1399004714025243	journal	January 2015
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 Zheng, Hao; Dietrich, Carsten; Radek, Renate Environmental Microbiology, Vol. 18, Issue 1 https://doi.org/10.1111/1462-2920.12960	journal	July 2015
Methylthioadenosine/S-adenosylhomocysteine nucleosidase, a critical enzyme for bacterial metabolism: Involvement of MTA/SAH nucleosidase in bacterial metabolism Parveen, Nikhat; Cornell, Kenneth A. Molecular Microbiology, Vol. 79, Issue 1 https://doi.org/10.1111/j.1365-2958.2010.07455.x	journal	November 2010
A bifunctional salvage pathway for two distinct S‐adenosylmethionine byproducts that is widespread in bacteria, including pathogenic Escherichia coli North, Justin A.; Wildenthal, John A.; Erb, Tobias J. Molecular Microbiology https://doi.org/10.1111/mmi.14459	journal	January 2020
Aquatic and terrestrial cyanobacteria produce methane Bižić, M.; Klintzsch, T.; Ionescu, D. Science Advances, Vol. 6, Issue 3 https://doi.org/10.1126/sciadv.aax5343	journal	January 2020
The biosynthetic pathway of coenzyme F430 in methanogenic and methanotrophic archaea Zheng, Kaiyuan; Ngo, Phong D.; Owens, Victoria L. Science, Vol. 354, Issue 6310 https://doi.org/10.1126/science.aag2947	journal	October 2016
A bound reaction intermediate sheds light on the mechanism of nitrogenase Sippel, Daniel; Rohde, Michael; Netzer, Julia Science, Vol. 359, Issue 6383 https://doi.org/10.1126/science.aar2765	journal	March 2018
Complete Genome Sequence of the Photosynthetic Purple Nonsulfur Bacterium Rhodobacter capsulatus SB 1003 Strnad, Hynek; Lapidus, Alla; Paces, Jan Journal of Bacteriology, Vol. 192, Issue 13 https://doi.org/10.1128/JB.00366-10	journal	April 2010
Regulation of Uptake Hydrogenase and Effects of Hydrogen Utilization on Gene Expression in Rhodopseudomonas palustris Rey, F. E.; Oda, Y.; Harwood, C. S. Journal of Bacteriology, Vol. 188, Issue 17 https://doi.org/10.1128/JB.00381-06	journal	August 2006
Electron Transfer to Nitrogenase in Different Genomic and Metabolic Backgrounds Poudel, Saroj; Colman, Daniel R.; Fixen, Kathryn R. Journal of Bacteriology, Vol. 200, Issue 10 https://doi.org/10.1128/JB.00757-17	journal	February 2018
Roles of RubisCO and the RubisCO-Like Protein in 5-Methylthioadenosine Metabolism in the Nonsulfur Purple Bacterium Rhodospirillum rubrum Singh, J.; Tabita, F. R. Journal of Bacteriology, Vol. 192, Issue 5 https://doi.org/10.1128/JB.01442-09	journal	December 2009
Characterization of the DraT/DraG System for Posttranslational Regulation of Nitrogenase in the Endophytic Betaproteobacterium Azoarcus sp. Strain BH72 Oetjen, Janina; Reinhold-Hurek, Barbara Journal of Bacteriology, Vol. 191, Issue 11 https://doi.org/10.1128/JB.01720-08	journal	June 2009
Mutagenesis and Functional Characterization of theglnB, glnA, and nifA Genes from the Photosynthetic Bacterium Rhodospirillum rubrum Zhang, Yaoping; Pohlmann, Edward L.; Ludden, Paul W. Journal of Bacteriology, Vol. 182, Issue 4 https://doi.org/10.1128/JB.182.4.983-992.2000	journal	February 2000
Distribution of nitrogen fixation and nitrogenase-like sequences amongst microbial genomes Dos Santos, Patricia C.; Fang, Zhong; Mason, Steven W. BMC Genomics, Vol. 13, Issue 1 https://doi.org/10.1186/1471-2164-13-162	journal	January 2012
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 Love, Michael I.; Huber, Wolfgang; Anders, Simon Genome Biology, Vol. 15, Issue 12 https://doi.org/10.1186/s13059-014-0550-8	journal	December 2014
New insights into the evolutionary history of biological nitrogen fixation Boyd, Eric S.; Peters, John W. Frontiers in Microbiology, Vol. 4 https://doi.org/10.3389/fmicb.2013.00201	journal	January 2013
Soil and Crop Management Practices to Minimize the Impact of Waterlogging on Crop Productivity Manik, S. M. Nuruzzaman; Pengilley, Georgina; Dean, Geoffrey Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.00140	journal	February 2019

Similar Records

A nitrogenase-like enzyme system catalyzes methionine, ethylene, and methane biogenesis

Journal Article · Fri Aug 28 00:00:00 EDT 2020 · Science · OSTI ID:1668785

North, Justin A.; Narrowe, Adrienne B.; Xiong, Weili; +9 more

Novel Microbial Routes to Synthesize Industrially Significant Precursor Compounds

Technical Report · Tue Apr 30 00:00:00 EDT 2024 · OSTI ID:2281171

North, Justin Andrew; Cannon, William R.; Wrighton, Kelly C.

Architecture, Catalysis and Regulation of Methylthio-Alkane Reductase for Bacterial Sulfur Acquisition from Volatile Organic Sulfur Compounds

Journal Article · Wed Oct 01 00:00:00 EDT 2025 · Nature Catalysis · OSTI ID:2588496

Murali, Srividya; Hu, Guo-Bin; Kreitler, Dale; +10 more

Related Subjects

10 SYNTHETIC FUELS
54 ENVIRONMENTAL SCIENCES
59 BASIC BIOLOGICAL SCIENCES
Nitrogenase
bacteria
dimethyl sulfide
ethylene
methane
soil
sulfur

Title: A nitrogenase-like enzyme system catalyzes methionine, ethylene, and methane biogenesis

Citation Formats

References (61)

Similar Records

Related Subjects