Assessing methanotrophy and carbon fixation for biofuel production by Methanosarcina acetivorans

Nazem-Bokaee, Hadi; Gopalakrishnan, Saratram; Ferry, James G.; Wood, Thomas K.; Maranas, Costas D.

doi:10.1186/s12934-015-0404-4

Title: Assessing methanotrophy and carbon fixation for biofuel production by Methanosarcina acetivorans

Journal Article · Sun Jan 17 00:00:00 EST 2016 · Microbial Cell Factories

DOI:https://doi.org/10.1186/s12934-015-0404-4· OSTI ID:1618800

Nazem-Bokaee, Hadi; Gopalakrishnan, Saratram; Ferry, James G.; Wood, Thomas K.; Maranas, Costas D.

Methanosarcina acetivorans is a model archaeon with renewed interest due to its unique reversible methane production pathways. However, the mechanism and relevant pathways implicated in (co)utilizing novel carbon substrates in this organism are still not fully understood. This paper provides a comprehensive inventory of thermodynamically feasible routes for anaerobic methane oxidation, co-reactant utilization, and maximum carbon yields of major biofuel candidates by M. acetivorans. Here, an updated genome-scale metabolic model of M. acetivorans is introduced (iMAC868 containing 868 genes, 845 reactions, and 718 metabolites) by integrating information from two previously reconstructed metabolic models (i.e., iVS941 and iMB745), modifying 17 reactions, adding 24 new reactions, and revising 64 gene-proteinreaction associations based on newly available information. The new model establishes improved predictions of growth yields on native substrates and is capable of correctly predicting the knockout outcomes for 27 out of 28 gene deletion mutants. By tracing a bifurcated electron flow mechanism, the iMAC868 model predicts thermodynamically feasible (co)utilization pathway of methane and bicarbonate using various terminal electron acceptors through the reversal of the aceticlastic pathway. In conclusion, this effort paves the way in informing the search for thermodynamically feasible ways of (co)utilizing novel carbon substrates in the domain Archaea.

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Research Organization:: Pennsylvania State Univ., University Park, PA (United States)

Sponsoring Organization:: USDOE Advanced Research Projects Agency - Energy (ARPA-E)

Grant/Contract Number:: ARPA-E DE-AR0000431; AR0000431

OSTI ID:: 1618800

Alternate ID(s):: OSTI ID: 1238778

Journal Information:: Microbial Cell Factories, Journal Name: Microbial Cell Factories Vol. 15 Journal Issue: 1; ISSN 1475-2859

Publisher:: Springer Science + Business MediaCopyright Statement

Country of Publication:: United Kingdom

Language:: English

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Cited by: 28 works

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References (66)

Genetic manipulation of Methanosarcina spp. Kohler, Petra R. A.; Metcalf, William W. Frontiers in Microbiology, Vol. 3 https://doi.org/10.3389/fmicb.2012.00259	journal	January 2012
The Biochemistry of Methane Oxidation Hakemian, Amanda S.; Rosenzweig, Amy C. Annual Review of Biochemistry, Vol. 76, Issue 1 https://doi.org/10.1146/annurev.biochem.76.061505.175355	journal	June 2007
The Genome of M. acetivorans Reveals Extensive Metabolic and Physiological Diversity Galagan, J. E. Genome Research, Vol. 12, Issue 4 https://doi.org/10.1101/gr.223902	journal	April 2002
Methane oxidation by anaerobic archaea for conversion to liquid fuels Mueller, Thomas J.; Grisewood, Matthew J.; Nazem-Bokaee, Hadi Journal of Industrial Microbiology & Biotechnology, Vol. 42, Issue 3 https://doi.org/10.1007/s10295-014-1548-7	journal	November 2014
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
Proteome of Methanosarcina a cetivorans Part I: An Expanded View of the Biology of the Cell Li, Qingbo; Li, Lingyun; Rejtar, Tomas Journal of Proteome Research, Vol. 4, Issue 1 https://doi.org/10.1021/pr049832c	journal	February 2005
Genetic Analysis of the Methanol- and Methylamine-Specific Methyltransferase 2 Genes of Methanosarcina acetivorans C2A Bose, A.; Pritchett, M. A.; Metcalf, W. W. Journal of Bacteriology, Vol. 190, Issue 11 https://doi.org/10.1128/JB.00117-08	journal	March 2008
Ferredoxin requirement for electron transport from the carbon monoxide dehydrogenase complex to a membrane-bound hydrogenase in acetate-grown Methanosarcina thermophila. Terlesky, K. C.; Ferry, J. G. Journal of Biological Chemistry, Vol. 263, Issue 9 https://doi.org/10.1016/S0021-9258(18)68892-1	journal	March 1988
Biological Methane Oxidation: Regulation, Biochemistry, and Active Site Structure of Particulate Methane Monooxygenase Lieberman, Raquel L.; Rosenzweig, Amy C. Critical Reviews in Biochemistry and Molecular Biology, Vol. 39, Issue 3 https://doi.org/10.1080/10409230490475507	journal	January 2004
Methane-consuming archaebacteria in marine sediments Hinrichs, Kai-Uwe; Hayes, John M.; Sylva, Sean P. Nature, Vol. 398, Issue 6730 https://doi.org/10.1038/19751	journal	April 1999
Products of trace methane oxidation during nonmethyltrophic growth by Methanosarcina Moran, James J.; House, Christopher H.; Thomas, B. Journal of Geophysical Research, Vol. 112, Issue G2 https://doi.org/10.1029/2006JG000268	journal	January 2007
Natural gas from shale formation – The evolution, evidences and challenges of shale gas revolution in United States Wang, Qiang; Chen, Xi; Jha, Awadhesh N. Renewable and Sustainable Energy Reviews, Vol. 30 https://doi.org/10.1016/j.rser.2013.08.065	journal	February 2014
Short-Lived Climate Pollution Pierrehumbert, R. T. Annual Review of Earth and Planetary Sciences, Vol. 42, Issue 1 https://doi.org/10.1146/annurev-earth-060313-054843	journal	May 2014
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
An exact arithmetic toolbox for a consistent and reproducible structural analysis of metabolic network models Chindelevitch, Leonid; Trigg, Jason; Regev, Aviv Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms5893	journal	October 2014
Soil microorganisms as controllers of atmospheric trace gases (H2, CO, CH4, OCS, N2O, and NO). Conrad, R. Microbiological reviews, Vol. 60, Issue 4 https://doi.org/10.1128/MMBR.60.4.609-640.1996	journal	January 1996
Metabolic engineering of Escherichia coli for 1-butanol production Atsumi, Shota; Cann, Anthony F.; Connor, Michael R. Metabolic Engineering, Vol. 10, Issue 6, p. 305-311 https://doi.org/10.1016/j.ymben.2007.08.003	journal	November 2008
Class I and class II lysyl-tRNA synthetase mutants and the genetic encoding of pyrrolysine in Methanosarcina spp.: lysyl-tRNA synthetases in Methanosarcina Mahapatra, Anirban; Srinivasan, Gayathri; Richter, Kerstin B. Molecular Microbiology, Vol. 64, Issue 5 https://doi.org/10.1111/j.1365-2958.2007.05740.x	journal	May 2007
TransportDB: a comprehensive database resource for cytoplasmic membrane transport systems and outer membrane channels Ren, Q.; Chen, K.; Paulsen, I. T. Nucleic Acids Research, Vol. 35, Issue Database https://doi.org/10.1093/nar/gkl925	journal	January 2007
New perspectives on anaerobic methane oxidation Valentine, David L.; Reeburgh, William S. Environmental Microbiology, Vol. 2, Issue 5 https://doi.org/10.1046/j.1462-2920.2000.00135.x	journal	October 2000
Proteome of Methanosarcina a cetivorans Part II: Comparison of Protein Levels in Acetate- and Methanol-Grown Cells Li, Qingbo; Li, Lingyun; Rejtar, Tomas Journal of Proteome Research, Vol. 4, Issue 1 https://doi.org/10.1021/pr049831k	journal	February 2005
Quantitative prediction of cellular metabolism with constraint-based models: the COBRA Toolbox v2.0 Schellenberger, Jan; Que, Richard; Fleming, Ronan M. T. Nature Protocols, Vol. 6, Issue 9 https://doi.org/10.1038/nprot.2011.308	journal	August 2011
Structure of a methyl-coenzyme M reductase from Black Sea mats that oxidize methane anaerobically Shima, Seigo; Krueger, Martin; Weinert, Tobias Nature, Vol. 481, Issue 7379 https://doi.org/10.1038/nature10663	journal	November 2011
The effects of alternate optimal solutions in constraint-based genome-scale metabolic models Mahadevan, R.; Schilling, C. H. Metabolic Engineering, Vol. 5, Issue 4 https://doi.org/10.1016/j.ymben.2003.09.002	journal	October 2003
Calculation of Standard Transformed Gibbs Energies and Standard Transformed Enthalpies of Biochemical Reactants Alberty, Robert A. Archives of Biochemistry and Biophysics, Vol. 353, Issue 1 https://doi.org/10.1006/abbi.1998.0638	journal	May 1998
Genome-Scale Metabolic Reconstruction and Hypothesis Testing in the Methanogenic Archaeon Methanosarcina acetivorans C2A Benedict, M. N.; Gonnerman, M. C.; Metcalf, W. W. Journal of Bacteriology, Vol. 194, Issue 4 https://doi.org/10.1128/JB.06040-11	journal	December 2011
Production and Consumption of H2 during Growth of Methanosarcina spp. on Acetate Lovley, Derek R.; Ferry, James G. Applied and Environmental Microbiology, Vol. 49, Issue 1 https://doi.org/10.1128/AEM.49.1.247-249.1985	journal	January 1985
Promiscuous archaeal ATP synthase concurrently coupled to Na+ and H+ translocation Schlegel, K.; Leone, V.; Faraldo-Gomez, J. D. Proceedings of the National Academy of Sciences, Vol. 109, Issue 3 https://doi.org/10.1073/pnas.1115796109	journal	January 2012
An unconventional pathway for reduction of CO2 to methane in CO-grown Methanosarcina acetivorans revealed by proteomics Lessner, D. J.; Li, L.; Li, Q. Proceedings of the National Academy of Sciences, Vol. 103, Issue 47 https://doi.org/10.1073/pnas.0608833103	journal	November 2006
KEGG: Kyoto Encyclopedia of Genes and Genomes Ogata, H.; Goto, S.; Sato, K. Nucleic Acids Research, Vol. 27, Issue 1 https://doi.org/10.1093/nar/27.1.29	journal	January 1999
In vivo role of three fused corrinoid/methyl transfer proteins in Methanosarcina acetivorans Oelgeschläger, Ellen; Rother, Michael Molecular Microbiology, Vol. 72, Issue 5 https://doi.org/10.1111/j.1365-2958.2009.06723.x	journal	June 2009
Methane as Fuel for Anaerobic Microorganisms Thauer, Rudolf K.; Shima, Seigo Annals of the New York Academy of Sciences, Vol. 1125, Issue 1 https://doi.org/10.1196/annals.1419.000	journal	March 2008
Anaerobic Oxidation of Methane: Progress with an Unknown Process Knittel, Katrin; Boetius, Antje Annual Review of Microbiology, Vol. 63, Issue 1 https://doi.org/10.1146/annurev.micro.61.080706.093130	journal	October 2009
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
BRENDA in 2013: integrated reactions, kinetic data, enzyme function data, improved disease classification: new options and contents in BRENDA Schomburg, Ida; Chang, Antje; Placzek, Sandra Nucleic Acids Research, Vol. 41, Issue D1 https://doi.org/10.1093/nar/gks1049	journal	November 2012
Methane formation and methane oxidation by methanogenic bacteria. Zehnder, A. J.; Brock, T. D. Journal of Bacteriology, Vol. 137, Issue 1 https://doi.org/10.1128/JB.137.1.420-432.1979	journal	January 1979
Methanosarcina acetivorans sp. nov., an Acetotrophic Methane-Producing Bacterium Isolated from Marine Sediments Sowers, Kevin R.; Baron, Stephen F.; Ferry, James G. Applied and Environmental Microbiology, Vol. 47, Issue 5 https://doi.org/10.1128/AEM.47.5.971-978.1984	journal	January 1984
Genetic analysis of mch mutants in two Methanosarcina species demonstrates multiple roles for the methanopterin-dependent C-1 oxidation/reduction pathway and differences in H ₂ metabolism between closely related species : Methyl reduction in Guss, Adam M.; Mukhopadhyay, Biswarup; Zhang, Jun Kai Molecular Microbiology, Vol. 55, Issue 6 https://doi.org/10.1111/j.1365-2958.2005.04514.x	journal	January 2005
Methanogenesis by Methanosarcina acetivorans involves two structurally and functionally distinct classes of heterodisulfide reductase Buan, Nicole R.; Metcalf, William W. Molecular Microbiology, Vol. 75, Issue 4 https://doi.org/10.1111/j.1365-2958.2009.06990.x	journal	February 2010
Unconventional gas – A review of regional and global resource estimates McGlade, Christophe; Speirs, Jamie; Sorrell, Steve Energy, Vol. 55 https://doi.org/10.1016/j.energy.2013.01.048	journal	June 2013
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
The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases Caspi, R.; Altman, T.; Dreher, K. Nucleic Acids Research, Vol. 40, Issue D1 https://doi.org/10.1093/nar/gkr1014	journal	November 2011
Metabolic engineering of microorganisms for biofuels production: from bugs to synthetic biology to fuels Lee, Sung Kuk; Chou, Howard; Ham, Timothy S. Current Opinion in Biotechnology, Vol. 19, Issue 6, p. 556-563 https://doi.org/10.1016/j.copbio.2008.10.014	journal	December 2008
Rethinking biological activation of methane and conversion to liquid fuels Haynes, Chad A.; Gonzalez, Ramon Nature Chemical Biology, Vol. 10, Issue 5 https://doi.org/10.1038/nchembio.1509	journal	April 2014
Quantitative Proteomic and Microarray Analysis of the Archaeon M ethanosarcina acetivorans Grown with Acetate versus Methanol Li, Lingyun; Li, Qingbo; Rohlin, Lars Journal of Proteome Research, Vol. 6, Issue 2 https://doi.org/10.1021/pr060383l	journal	February 2007
Energy conservation via electron bifurcating ferredoxin reduction and proton/Na+ translocating ferredoxin oxidation Buckel, Wolfgang; Thauer, Rudolf K. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1827, Issue 2 https://doi.org/10.1016/j.bbabio.2012.07.002	journal	February 2013
The key nickel enzyme of methanogenesis catalyses the anaerobic oxidation of methane Scheller, Silvan; Goenrich, Meike; Boecher, Reinhard Nature, Vol. 465, Issue 7298 https://doi.org/10.1038/nature09015	journal	June 2010
Metagenome and mRNA expression analyses of anaerobic methanotrophic archaea of the ANME-1 group Meyerdierks, Anke; Kube, Michael; Kostadinov, Ivaylo Environmental Microbiology, Vol. 12, Issue 2 https://doi.org/10.1111/j.1462-2920.2009.02083.x	journal	February 2010
Anaerobic growth of Methanosarcina acetivorans C2A on carbon monoxide: An unusual way of life for a methanogenic archaeon Rother, M.; Metcalf, W. W. Proceedings of the National Academy of Sciences, Vol. 101, Issue 48 https://doi.org/10.1073/pnas.0407486101	journal	November 2004
Bioenergetics and anaerobic respiratory chains of aceticlastic methanogens Welte, Cornelia; Deppenmeier, Uwe Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1837, Issue 7 https://doi.org/10.1016/j.bbabio.2013.12.002	journal	July 2014
Trace methane oxidation studied in several Euryarchaeota under diverse conditions Moran, James J.; House, Christopher H.; Freeman, Katherine H. Archaea, Vol. 1, Issue 5 https://doi.org/10.1155/2005/650670	journal	January 2005
Methanogenic archaea: ecologically relevant differences in energy conservation Thauer, Rudolf K.; Kaster, Anne-Kristin; Seedorf, Henning Nature Reviews Microbiology, Vol. 6, Issue 8 https://doi.org/10.1038/nrmicro1931	journal	June 2008
Electron Transport in the Pathway of Acetate Conversion to Methane in the Marine Archaeon Methanosarcina acetivorans Li, Q.; Li, L.; Rejtar, T. Journal of Bacteriology, Vol. 188, Issue 2 https://doi.org/10.1128/JB.188.2.702-710.2006	journal	December 2005
The Rush to Drill for Natural Gas: A Public Health Cautionary Tale Finkel, Madelon L.; Law, Adam American Journal of Public Health, Vol. 101, Issue 5 https://doi.org/10.2105/AJPH.2010.300089	journal	May 2011
Metabolic reconstruction of the archaeon methanogen Methanosarcina Acetivorans Satish Kumar, Vinay; Ferry, James G.; Maranas, Costas D. BMC Systems Biology, Vol. 5, Issue 1 https://doi.org/10.1186/1752-0509-5-28	journal	January 2011
Electron transport during aceticlastic methanogenesis by Methanosarcina acetivorans involves a sodium-translocating Rnf complex Schlegel, Katharina; Welte, Cornelia; Deppenmeier, Uwe FEBS Journal, Vol. 279, Issue 24 https://doi.org/10.1111/febs.12031	journal	November 2012
Coupling of ferredoxin and heterodisulfide reduction via electron bifurcation in hydrogenotrophic methanogenic archaea Kaster, A. -K.; Moll, J.; Parey, K. Proceedings of the National Academy of Sciences, Vol. 108, Issue 7 https://doi.org/10.1073/pnas.1016761108	journal	January 2011
Characterization of the RnfB and RnfG Subunits of the Rnf Complex from the Archaeon Methanosarcina acetivorans Suharti, Suharti; Wang, Mingyu; de Vries, Simon PLoS ONE, Vol. 9, Issue 5 https://doi.org/10.1371/journal.pone.0097966	journal	May 2014
Reversing methanogenesis to capture methane for liquid biofuel precursors Soo, Valerie W. C.; McAnulty, Michael J.; Tripathi, Arti Microbial Cell Factories, Vol. 15, Issue 1 https://doi.org/10.1186/s12934-015-0397-z	journal	January 2016
Methyl Sulfide Production by a Novel Carbon Monoxide Metabolism in Methanosarcina acetivorans Moran, J. J.; House, C. H.; Vrentas, J. M. Applied and Environmental Microbiology, Vol. 74, Issue 2 https://doi.org/10.1128/AEM.01750-07	journal	November 2007
Opportunity, challenges and policy choices for China on the development of shale gas Hu, Desheng; Xu, Shengqing Energy Policy, Vol. 60 https://doi.org/10.1016/j.enpol.2013.04.068	journal	September 2013
What is flux balance analysis? Orth, Jeffrey D.; Thiele, Ines; Palsson, Bernhard Ø Nature Biotechnology, Vol. 28, Issue 3 https://doi.org/10.1038/nbt.1614	journal	March 2010
Assimilation of methane and inorganic carbon by microbial communities mediating the anaerobic oxidation of methane Wegener, Gunter; Niemann, Helge; Elvert, Marcus Environmental Microbiology, Vol. 10, Issue 9 https://doi.org/10.1111/j.1462-2920.2008.01653.x	journal	September 2008
Methanotrophic archaea possessing diverging methane-oxidizing and electron-transporting pathways Wang, Feng-Ping; Zhang, Yu; Chen, Ying The ISME Journal, Vol. 8, Issue 5 https://doi.org/10.1038/ismej.2013.212	journal	December 2013
Anaerobic oxidation of methane with sulfate: on the reversibility of the reactions that are catalyzed by enzymes also involved in methanogenesis from CO2 Thauer, Rudolf K. Current Opinion in Microbiology, Vol. 14, Issue 3 https://doi.org/10.1016/j.mib.2011.03.003	journal	June 2011
Methane, microbes and models: fundamental understanding of the soil methane cycle for future predictions: Methane, microbes and models Nazaries, Loïc; Murrell, J. Colin; Millard, Pete Environmental Microbiology, Vol. 15, Issue 9 https://doi.org/10.1111/1462-2920.12149	journal	May 2013