A Prospective Study on the Fermentation Landscape of Gaseous Substrates to Biorenewables Using Methanosarcina acetivorans Metabolic Model

Nazem-Bokaee, Hadi; Maranas, Costas D.

doi:10.3389/fmicb.2018.01855

Title: A Prospective Study on the Fermentation Landscape of Gaseous Substrates to Biorenewables Using Methanosarcina acetivorans Metabolic Model

Journal Article · Fri Aug 24 00:00:00 EDT 2018 · Frontiers in Microbiology

DOI:https://doi.org/10.3389/fmicb.2018.01855· OSTI ID:1466420

Nazem-Bokaee, Hadi; Maranas, Costas D.

The abundance of methane in shale gas and of other gases such as carbon monoxide, hydrogen, and carbon dioxide as chemical process byproducts has motivated the use of gas fermentation for bioproduction. Recent advances in metabolic engineering and synthetic biology allow for engineering of microbes metabolizing a variety of chemicals including gaseous feeds into a number of biorenewables and transportation liquid fuels. New computational tools enable the systematic exploration of all feasible conversion alternatives. Here we computationally assessed all thermodynamically feasible ways of co-utilizing CH₄, CO, and CO₂ using ferric as terminal electron acceptor for the production of all key precursor metabolites. We identified the thermodynamically feasible co-utilization ratio ranges of CH₄, CO, and CO₂ toward production of the target metabolite(s) as a function of ferric uptake. A revised version of the iMAC868 genome-scale metabolic model of Methanosarcina acetivorans was chosen to assess co-utilization of CH₄, CO, and CO₂ and their conversion into selected target products using the optStoic pathway design tool. This revised version contains the latest information on electron flow mechanisms by the methanogen while supplied with methane as the sole carbon source. The interplay between different gas co-utilization ratios and the energetics of reverse methanogenesis were also analyzed using the same metabolic model.

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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:: AR0000431

OSTI ID:: 1466420

Alternate ID(s):: OSTI ID: 1510462

Journal Information:: Frontiers in Microbiology, Journal Name: Frontiers in Microbiology Vol. 9; ISSN 1664-302X

Publisher:: Frontiers Media SACopyright Statement

Country of Publication:: Switzerland

Language:: English

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Cited by: 5 works

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References (43)

Computational methods in metabolic engineering for strain design Long, Matthew R.; Ong, Wai Kit; Reed, Jennifer L. Current Opinion in Biotechnology, Vol. 34 https://doi.org/10.1016/j.copbio.2014.12.019	journal	August 2015
Effect of Syngas Composition and CO ₂ -Diluted Oxygen on Performance of a Premixed Swirl-Stabilized Combustor Williams, Timothy C.; Shaddix*, Christopher R.; Schefer, Robert W. Combustion Science and Technology, Vol. 180, Issue 1 https://doi.org/10.1080/00102200701487061	journal	November 2007
The Fischer–Tropsch process: 1950–2000 Dry, Mark E. Catalysis Today, Vol. 71, Issue 3-4 https://doi.org/10.1016/S0920-5861(01)00453-9	journal	January 2002
Clostridia: the importance of their exceptional substrate and metabolite diversity for biofuel and biorefinery applications Tracy, Bryan P.; Jones, Shawn W.; Fast, Alan G. Current Opinion in Biotechnology, Vol. 23, Issue 3 https://doi.org/10.1016/j.copbio.2011.10.008	journal	June 2012
Gas fermentation - a biotechnological solution for today's challenges Dürre, Peter Microbial Biotechnology, Vol. 10, Issue 1 https://doi.org/10.1111/1751-7915.12431	journal	October 2016
ToMI-FBA: A genome-scale metabolic flux based algorithm to select optimum hosts and media formulations for expressing pathways of interest Nazem-Bokaee, Hadi; S. Senger, Ryan AIMS Bioengineering, Vol. 2, Issue 4 https://doi.org/10.3934/bioeng.2015.4.335	journal	January 2015
Fermentative production of butanol—the industrial perspective Green, Edward M. Current Opinion in Biotechnology, Vol. 22, Issue 3 https://doi.org/10.1016/j.copbio.2011.02.004	journal	June 2011
Integrated bioprocess for conversion of gaseous substrates to liquids Hu, Peng; Chakraborty, Sagar; Kumar, Amit Proceedings of the National Academy of Sciences, Vol. 113, Issue 14 https://doi.org/10.1073/pnas.1516867113	journal	March 2016
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
H-B-E (hexanol-butanol-ethanol) fermentation for the production of higher alcohols from syngas/waste gas Fernández-Naveira, Ánxela; Veiga, María C.; Kennes, Christian Journal of Chemical Technology & Biotechnology, Vol. 92, Issue 4 https://doi.org/10.1002/jctb.5194	journal	February 2017
Production of butanol and ethanol from synthesis gas via fermentation Worden, R. M.; Grethlein, A. J.; Jain, M. K. Fuel, Vol. 70, Issue 5 https://doi.org/10.1016/0016-2361(91)90175-A	journal	May 1991
A Method for Finding Metabolic Pathways Using Atomic Group Tracking Huang, Yiran; Zhong, Cheng; Lin, Hai Xiang PLOS ONE, Vol. 12, Issue 1 https://doi.org/10.1371/journal.pone.0168725	journal	January 2017
Bioconversion of natural gas to liquid fuel: Opportunities and challenges Fei, Qiang; Guarnieri, Michael T.; Tao, Ling Biotechnology Advances, Vol. 32, Issue 3 https://doi.org/10.1016/j.biotechadv.2014.03.011	journal	May 2014
Artificial electron acceptors decouple archaeal methane oxidation from sulfate reduction Scheller, S.; Yu, H.; Chadwick, G. L. Science, Vol. 351, Issue 6274 https://doi.org/10.1126/science.aad7154	journal	February 2016
Design of computational retrobiosynthesis tools for the design of de novo synthetic pathways Hadadi, Noushin; Hatzimanikatis, Vassily Current Opinion in Chemical Biology, Vol. 28 https://doi.org/10.1016/j.cbpa.2015.06.025	journal	October 2015
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
Methane as a Resource: Can the Methanotrophs Add Value? Strong, P. J.; Xie, S.; Clarke, W. P. Environmental Science & Technology, Vol. 49, Issue 7 https://doi.org/10.1021/es504242n	journal	March 2015
Traits of selected Clostridium strains for syngas fermentation to ethanol : Syngas Fermentation Strain Comparison Martin, Michael E.; Richter, Hanno; Saha, Surya Biotechnology and Bioengineering, Vol. 113, Issue 3 https://doi.org/10.1002/bit.25827	journal	September 2015
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
A Review of Recent Literature to Search for an Efficient Catalytic Process for the Conversion of Syngas to Ethanol Subramani, Velu; Gangwal, Santosh K. Energy & Fuels, Vol. 22, Issue 2 https://doi.org/10.1021/ef700411x	journal	March 2008
2,3-Butanediol Production by Acetogenic Bacteria, an Alternative Route to Chemical Synthesis, Using Industrial Waste Gas Köpke, Michael; Mihalcea, Christophe; Liew, FungMin Applied and Environmental Microbiology, Vol. 77, Issue 15 https://doi.org/10.1128/AEM.00355-11	journal	June 2011
Electron Bifurcation and Confurcation in Methanogenesis and Reverse Methanogenesis Yan, Zhen; Ferry, James G. Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.01322	journal	June 2018
Bioconversion of methane to lactate by an obligate methanotrophic bacterium Henard, Calvin A.; Smith, Holly; Dowe, Nancy Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep21585	journal	February 2016
Biotechnologies for greenhouse gases (CH4, N2O, and CO2) abatement: state of the art and challenges López, Juan C.; Quijano, Guillermo; Souza, Theo S. O. Applied Microbiology and Biotechnology, Vol. 97, Issue 6 https://doi.org/10.1007/s00253-013-4734-z	journal	February 2013
A Ferredoxin- and F ₄₂₀ H ₂ -Dependent, Electron-Bifurcating, Heterodisulfide Reductase with Homologs in the Domains Bacteria and Archaea Yan, Zhen; Wang, Mingyu; Ferry, James G. mBio, Vol. 8, Issue 1 https://doi.org/10.1128/mBio.02285-16	journal	February 2017
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
Heterologous Expression of the Clostridium carboxidivorans CO Dehydrogenase Alone or Together with the Acetyl Coenzyme A Synthase Enables both Reduction of CO ₂ and Oxidation of CO by Clostridium acetobutylicum Carlson, Ellinor D.; Papoutsakis, Eleftherios T. Applied and Environmental Microbiology, Vol. 83, Issue 16 https://doi.org/10.1128/AEM.00829-17	journal	June 2017
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
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
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
Technologies for large-scale gas conversion Aasberg-Petersen, K.; Bak Hansen, J. -H; Christensen, T. S. Applied Catalysis A: General, Vol. 221, Issue 1-2 https://doi.org/10.1016/S0926-860X(01)00811-0	journal	November 2001
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
Designing overall stoichiometric conversions and intervening metabolic reactions Chowdhury, Anupam; Maranas, Costas D. Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep16009	journal	November 2015
Fermentative production of ethanol from carbon monoxide Köpke, Michael; Mihalcea, Christophe; Bromley, Jason C. Current Opinion in Biotechnology, Vol. 22, Issue 3 https://doi.org/10.1016/j.copbio.2011.01.005	journal	June 2011
Syngas Biorefinery and Syngas Utilization De Tissera, Sashini; Köpke, Michael; Simpson, Sean D. Advances in Biochemical Engineering/Biotechnology https://doi.org/10.1007/10_2017_5	book	January 2017
Methane-Consuming Archaea Revealed by Directly Coupled Isotopic and Phylogenetic Analysis Orphan, V. J. Science, Vol. 293, Issue 5529 https://doi.org/10.1126/science.1061338	journal	July 2001
Assessing methanotrophy and carbon fixation for biofuel production by Methanosarcina acetivorans Nazem-Bokaee, Hadi; Gopalakrishnan, Saratram; Ferry, James G. Microbial Cell Factories, Vol. 15, Issue 1 https://doi.org/10.1186/s12934-015-0404-4	journal	January 2016
Fermentative butanol production by clostridia Lee, Sang Yup; Park, Jin Hwan; Jang, Seh Hee Biotechnology and Bioengineering, Vol. 101, Issue 2, p. 209-228 https://doi.org/10.1002/bit.22003	journal	October 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
COBRApy: COnstraints-Based Reconstruction and Analysis for Python Ebrahim, Ali; Lerman, Joshua A.; Palsson, Bernhard O. BMC Systems Biology, Vol. 7, Issue 1 https://doi.org/10.1186/1752-0509-7-74	journal	January 2013
A biochemical framework for anaerobic oxidation of methane driven by Fe(III)-dependent respiration Yan, Zhen; Joshi, Prachi; Gorski, Christopher A. Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-04097-9	journal	April 2018
Central Carbon Metabolism as a Minimal Biochemical Walk between Precursors for Biomass and Energy Noor, Elad; Eden, Eran; Milo, Ron Molecular Cell, Vol. 39, Issue 5 https://doi.org/10.1016/j.molcel.2010.08.031	journal	September 2010

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Kinetic modeling of Stickland reactions-coupled methanogenesis for a methanogenic culture Sangavai, C.; Bharathi, M.; Ganesh, Shilpkar P. AMB Express, Vol. 9, Issue 1 https://doi.org/10.1186/s13568-019-0803-8	journal	June 2019

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