Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Displacing fishmeal with protein derived from stranded methane

Nature Sustainability volume 5, pages 47–56 (2022)Cite this article

Subjects

Abstract

Methane emitted and flared from industrial sources across the United States is a major contributor to global climate change. Methanotrophic bacteria can transform this methane into useful protein-rich biomass, already approved for inclusion into animal feed. In the rapidly growing aquaculture industry, methanotrophic additives have a favourable amino acid profile and can offset ocean-caught fishmeal, reducing demands on over-harvested fisheries. Here we analyse the economic potential of producing methanotrophic microbial protein from stranded methane produced at wastewater treatment plants, landfills, and oil and gas facilities. Our results show that current technology can enable production, in the United States alone, equivalent to 14% of the global fishmeal market at prices at or below the current cost of fishmeal (roughly US$1,600 per metric ton). A sensitivity analysis highlights technically and economically feasible cost reductions (such as reduced cooling or labour requirements), which could allow stranded methane from the United States alone to satisfy global fishmeal demand.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Process model for methanotrophic biomass production.
Fig. 2: Methane sources and capture potential.
Fig. 3: Levelized cost of methanotrophic microbial protein across baseline scenarios in which methane comes from wastewater treatment, landfills, oil and gas facilities, and the natural gas grid.
Fig. 4: Supply curve for methanotrophic production using stranded methane.
Fig. 5: Sensitivity analysis for baseline methanotroph production at landfills, individually varying the parameters to low and high values.

Similar content being viewed by others

Data availability

The data used in the analysis and figures are publicly available. The data on flaring from oil and gas facilities are available through the Earth Observation Group (https://eogdata.mines.edu/download_global_flare.html). All data on methane emissions from oil and gas facilities and landfills, flaring from landfills, and unit processes at wastewater treatment plants are available from the US EPA through the following programmes: Facilities Level Information on GreenHouse gases Tool (https://ghgdata.epa.gov/ghgp/main.do), Landfill Methane Outreach Program (https://www.epa.gov/lmop/lmop-landfill-and-project-database) and Clean Watersheds Needs Survey for 2004 (https://www.epa.gov/cwns/clean-watersheds-needs-survey-cwns-2004-report-and-data), 2008 (https://www.epa.gov/cwns/clean-watersheds-needs-survey-cwns-2008-report-and-data) and 2012 (https://www.epa.gov/cwns/clean-watersheds-needs-survey-cwns-2012-report-and-data).

Code availability

Code supporting the current study is available at https://github.com/sahar-elabbadi/methane-to-protein.

References

  1. Mbow, C. et al. in Special Report on Climate Change and Land (eds Shukla, P. R. et al.) 437–550 (IPCC, 2019).

  2. GLOBEFISH Highlights January 2020 Issue, with Jan.–Sep. 2019 Statistics (FAO, 2020).

  3. Edwards, P., Zhang, W., Belton, B. & Little, D. C. Misunderstandings, myths and mantras in aquaculture: its contribution to world food supplies has been systematically over reported. Mar. Policy 106, 103547 (2019).

    Article  Google Scholar 

  4. Willett, W. et al. Food in the Anthropocene: the EAT-Lancet commission on healthy diets from sustainable food systems. Lancet 393, 447–492 (2019).

    Article  Google Scholar 

  5. Shah, M. R. et al. Microalgae in aquafeeds for a sustainable aquaculture industry. J. Appl. Phycol. 30, 197–213 (2018).

    Article  Google Scholar 

  6. Naylor, R. L. et al. A 20-year retrospective review of global aquaculture. Nature 591, 551–563 (2021).

    Article  CAS  Google Scholar 

  7. Ortuño Crespo, G. & Dunn, D. C. A review of the impacts of fisheries on open-ocean ecosystems. ICES J. Mar. Sci. 74, 2283–2297 (2017).

    Article  Google Scholar 

  8. Malcorps, W. et al. The sustainability conundrum of fishmeal substitution by plant ingredients in shrimp feeds. Sustainability 11, 1212 (2019).

    Article  Google Scholar 

  9. Boucher, O., Friedlingstein, P., Collins, B. & Shine, K. P. The indirect global warming potential and global temperature change potential due to methane oxidation. Environ. Res. Lett. 4, 044007 (2009).

    Article  Google Scholar 

  10. Inventory of U.S. Greenhouse Gas Emissions and Sinks: 1990–2018 Technical Report No. 430-R-20-002 (US Environmental Protection Agency, 2020).

  11. Clomburg, J. M., Crumbley, A. M. & Gonzalez, R. Industrial biomanufacturing: the future of chemical production. Science 355, eaag0804 (2017).

    Article  Google Scholar 

  12. Øverland, M., Tauson, A.-H., Shearer, K. & Skrede, A. Evaluation of methane-utilising bacteria products as feed ingredients for monogastric animals. Arch. Anim. Nutr. 64, 171–189 (2010).

    Article  Google Scholar 

  13. El Abbadi, S. H. & Criddle, C. S. Engineering the dark food chain. Environ. Sci. Technol. 53, 2273–2287 (2019).

    Article  CAS  Google Scholar 

  14. Our products. Calysta http://www.feedkind.com/products/ (2021).

  15. Protein. Unibio https://www.unibio.dk/end-product/protein/ (2021).

  16. Levett, I. et al. Techno-economic assessment of poly-3-hydroxybutyrate (PHB) production from methane—the case for thermophilic bioprocessing. J. Environ. Chem. Eng. 4, 3724–3733 (2016).

    Article  CAS  Google Scholar 

  17. Pikaar, I. et al. Decoupling livestock from land use through industrial feed production pathways. Environ. Sci. Technol. 52, 7351–7359 (2018).

    Article  CAS  Google Scholar 

  18. Matassa, S. et al. Upcycling of biowaste carbon and nutrients in line with consumer confidence: the ‘full gas’ route to single cell protein. Green Chem. 22, 4912–4929 (2020).

    Article  CAS  Google Scholar 

  19. Verbeeck, K., De Vrieze, J., Pikaar, I., Verstraete, W. & Rabaey, K. Assessing the potential for up-cycling recovered resources from anaerobic digestion through microbial protein production. Microb. Biotechnol. https://doi.org/10.1111/1751-7915.13600 (2020).

  20. Landfill Gas Energy Project Data and Landfill Technical Data (Environmental Protection Agency, 2020).

  21. Facilities Level Information on GreenHouse Gases Tool (Environmental Protection Agency, 2019).

  22. Global Gas Flaring Observed from Space (Earth Observation Group, 2019).

  23. Clean Watersheds Needs Survey (CWNS) 2004 Report and Data (Environmental Protection Agency, 2004).

  24. Clean Watersheds Needs Survey (CWNS) 2008 Report and Data (Environmental Protection Agency, 2008).

  25. Clean Watersheds Needs Survey (CWNS) 2012 Report and Data (Environmental Protection Agency, 2012).

  26. Yanwen, S., Linville, J. L., Meltem, U.-D., Mintz, M. M. & Snyder, S. W. An overview of biogas production and utilization at full-scale wastewater treatment plants (WWTPs) in the United States: challenges and opportunities towards energy-neutral WWTPs. Renew. Sustain. Energy Rev. 50, 346–362 (2015).

    Article  Google Scholar 

  27. Cho, J. H. & Kim, I. H. Fish meal—nutritive value. J. Anim. Physiol. Anim. Nutr. 95, 685–692 (2011).

    Article  CAS  Google Scholar 

  28. Humbird, D., Davis, R. & McMillan, J. D. Aeration costs in stirred-tank and bubble column bioreactors. Biochem. Eng. J. 127, 161–166 (2017).

    Article  CAS  Google Scholar 

  29. Electric Power Monthly (US Energy Information Administration, 2021).

  30. Petersen, L. A. H., John, V., Jørgensen, S. B. & Gernaey, K. V. Mixing and mass transfer in a pilot scale U-loop bioreactor. Biotechnol. Bioeng. 114, 344–354 (2017).

    Article  CAS  Google Scholar 

  31. Criddle, C. S., Billington, S. L. & Frank, C. W. Renewable Bioplastics and Biocomposites from Biogas Methane and Waste-Derived Feedstock: Development of Enabling Technology, Life Cycle Assessment, and Analysis of Costs Technical Report No. DRRR-2014-1502 (California Department of Resources Recycling and Recovery, 2014).

  32. Cusworth, D. H. et al. Using remote sensing to detect, validate, and quantify methane emissions from California solid waste operations. Environ. Res. Lett. 15, 054012 (2020).

    Article  CAS  Google Scholar 

  33. Siegert, M. et al. Comparison of nonprecious metal cathode materials for methane production by electromethanogenesis. ACS Sustain. Chem. Eng. 2, 910–917 (2014).

    Article  CAS  Google Scholar 

  34. Kim, A. H. et al. More than a fertilizer: wastewater-derived struvite as a high value, sustainable fire retardant. Green Chem. 23, 4510–4523 (2021).

    Article  CAS  Google Scholar 

  35. Commodity Prices—Annual Prices Technical Report (World Bank, 2021).

  36. Jannathulla, R. et al. Fishmeal availability in the scenarios of climate change: inevitability of fishmeal replacement in aquafeeds and approaches for the utilization of plant protein sources. Aquac. Res. 50, 3493–3506 (2019).

    Article  CAS  Google Scholar 

  37. Nathan, P., Klinger, D. H., Sims, N. A., Janice-Renee, Y. & Kittinger, J. N. Nutritional attributes, substitutability, scalability, and environmental intensity of an illustrative subset of current and future protein sources for aquaculture feeds: joint consideration of potential synergies and trade-offs. Environ. Sci. Technol. 52, 5532–5544 (2018).

    Article  Google Scholar 

  38. Cumberlege, T., Blenkinsopp, T. & Clark, J. Assessment of Environmental Footprint of FeedKind Protein Technical Report (Carbon Trust, 2016).

  39. Veiga, P., Mendes, M., Martin, D. & Lee-Harwood, B. Reduction Fisheries: SFP Fisheries Sustainability Overview 2019 Technical Report (Sustainable Fisheries Partnership, 2019).

  40. Zhang, W. et al. Fishing for feed in China: facts, impacts and implications. Fish Fish. 21, 47–62 (2020).

    Article  Google Scholar 

  41. Kok, B. et al. Fish as feed: using economic allocation to quantify the Fish In : Fish Out ratio of major fed aquaculture species. Aquaculture 528, 735474 (2020).

    Article  CAS  Google Scholar 

  42. Klinger, D. & Naylor, R. Searching for solutions in aquaculture: charting a sustainable course. Annu. Rev. Environ. Resour. 37, 247–276 (2012).

    Article  Google Scholar 

  43. van der Ha, D., Bundervoet, B., Verstraete, W. & Boon, N. A sustainable, carbon neutral methane oxidation by a partnership of methane oxidizing communities and microalgae. Water Res. 45, 2845–2854 (2011).

    Article  Google Scholar 

  44. Rasouli, Z., Valverde-Pérez, B., D’Este, M., De Francisci, D. & Angelidaki, I. Nutrient recovery from industrial wastewater as single cell protein by a co-culture of green microalgae and methanotrophs. Biochem. Eng. J. 134, 129–135 (2018).

    Article  CAS  Google Scholar 

  45. Gingerich, D. B. & Mauter, M. S. Air emission reduction benefits of biogas electricity generation at municipal wastewater treatment plants. Environ. Sci. Technol. 52, 1633–1643 (2018).

    Article  CAS  Google Scholar 

  46. Parker, N., Williams, R., Dominguez-Faus, R. & Scheitrum, D. Renewable natural gas in California: an assessment of the technical and economic potential. Energy Policy 111, 235–245 (2017).

    Article  Google Scholar 

  47. Rittmann, B. E. & McCarty, P. L. Environmental Biotechnology: Principles and Applications 2nd edn (McGraw-Hill Education, 2020).

  48. Vo, T. T. Q., Wall, D. M., Ring, D., Rajendran, K. & Murphy, J. D. Techno-economic analysis of biogas upgrading via amine scrubber, carbon capture and ex-situ methanation. Appl. Energy 212, 1191–1202 (2018).

    Article  CAS  Google Scholar 

  49. Wendlandt, K.-D., Jechorek, M., Helm, J. & Stottmeister, U. Producing poly-3-hydroxybutyrate with a high molecular mass from methane. J. Biotechnol. 86, 127–133 (2001).

    Article  CAS  Google Scholar 

  50. Garrett, D. E. Chemical Engineering Economics (Van Nostrand Reinhold, 1989).

  51. CPI for All Urban Consumers (CPI-U) Technical Report (US Bureau of Labor Statistics, 2020).

  52. Weighted Average Cost of Capital (WACC): Explanation and Examples Technical Report (New Constructs, 2016).

  53. Retail Sales of Electricity to Ultimate Customers (Annual) Technical Report (US Energy Information Administration, 2020).

  54. Yang, S. et al. Global molecular analyses of methane metabolism in methanotrophic Alphaproteobacterium, Methylosinus trichosporium OB3b. Part II. Metabolomics and 13C-labeling study. Front. Microbiol. 4, 70 (2013).

    Google Scholar 

  55. Czyrnek-Delêtre, M. M., Ahern, E. P. & Murphy, J. D. Is small-scale upgrading of landfill gas to biomethane for use as a cellulosic transport biofuel economically viable? Biofuels Bioprod. Biorefin. 10, 139–149 (2016).

    Article  Google Scholar 

  56. Tansel, B. & Surita, S. C. Managing siloxanes in biogas-to-energy facilities: economic comparison of pre- vs post-combustion practices. Waste Manage. 96, 121–127 (2019).

    Article  CAS  Google Scholar 

  57. Aguilera, P. G. & Gutiérrez Ortiz, F. J. Techno-economic assessment of biogas plant upgrading by adsorption of hydrogen sulfide on treated sewage-sludge. Energy Convers. Manage. 126, 411–420 (2016).

    Article  CAS  Google Scholar 

  58. Pipatmanomai, S., Kaewluan, S. & Vitidsant, T. Economic assessment of biogas-to-electricity generation system with H2S removal by activated carbon in small pig farm. Appl. Energy 86, 669–674 (2009).

    Article  CAS  Google Scholar 

  59. United States Natural Gas Industrial Price (Dollars per Thousand Cubic Feet) (US Energy Information Administration, 2020).

  60. Pieja, A. J., Rostkowski, K. H. & Criddle, C. S. Distribution and selection of poly-3-hydroxybutyrate production capacity in methanotrophic proteobacteria. Microb. Ecol. 62, 564–573 (2011).

    Article  CAS  Google Scholar 

  61. Noreddine, G., Missimer, T. M. & Amy, G. L. Technical review and evaluation of the economics of water desalination: current and future challenges for better water supply sustainability. Desalination 309, 197–207 (2013).

    Article  Google Scholar 

  62. U.S. Refinery Utilization and Capacity (US Energy Information Administration, 2019).

  63. Jorge Luis, M., Dubrawski, K. L., El Abbadi, S. H., Choo, K.-H. & Criddle, C. S. Membrane and fluid contactors for safe and efficient methane delivery in methanotrophic bioreactors. J. Environ. Eng. 146, 03120006 (2020).

    Article  Google Scholar 

  64. Jinghua, X. & VanBriesen, J. M. Expanded thermodynamic true yield prediction model: adjustments and limitations. Biodegradation 19, 99–127 (2008).

    Article  Google Scholar 

Download references

Acknowledgements

This study was funded by the Stanford Center for Innovation in Global Health (S.H.E., C.S.C. and S.P.L.) and the Stanford Natural Gas Initiative (S.H.E., E.D.S., C.S.C. and A.R.B.), an industry consortium that supports independent research at Stanford University. We thank R. Hickey for input on industrial bioreactor scaling.

Author information

Authors and Affiliations

  1. Department of Civil and Environmental Engineering, Stanford University, Stanford, CA, USA

    Sahar H. El Abbadi & Craig S. Criddle

  2. Department of Energy Resources Engineering, Stanford University, Stanford, CA, USA

    Evan D. Sherwin & Adam R. Brandt

  3. Infectious Diseases and Geographic Medicine, Stanford University, Stanford, CA, USA

    Stephen P. Luby

  4. Stanford Woods Institute for the Environment, Stanford University, Stanford, CA, USA

    Stephen P. Luby & Craig S. Criddle

Authors
  1. Sahar H. El Abbadi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Evan D. Sherwin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Adam R. Brandt
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Stephen P. Luby
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Craig S. Criddle
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

S.H.E. and E.D.S. conceptualized the project. S.H.E. and E.D.S. devised the methodology with feedback from A.R.B., C.S.C. and S.P.L. S.H.E. and E.D.S. validated the methodology, conducted the investigation and wrote the original draft of the paper. S.H.E., E.D.S., A.R.B., S.P.L. and C.S.C. reviewed and edited the paper. E.D.S., A.R.B. and C.S.C. supervised the project. S.H.E. and E.D.S. conducted the project administration. S.H.E., E.D.S., A.R.B., S.P.L. and C.S.C. acquired the funding.

Corresponding author

Correspondence to Craig S. Criddle.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer review information Nature Sustainability thanks Richard Cottrell, Richard Newton and Jo De Vrieze for their contribution to the peer review of this work.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Tables 1–14, Figs. 1–7, Notes 1–3 and Methods.

Reporting Summary

Supplementary Data 1

Raw data for Figs. 2 and 4, including the methane source size for each point source in the analysis, the corresponding amount of methanotrophic SCP that can be produced from the source and the model output for the cost of SCP (US$ per ton) for production at the location.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

El Abbadi, S.H., Sherwin, E.D., Brandt, A.R. et al. Displacing fishmeal with protein derived from stranded methane. Nat Sustain 5, 47–56 (2022). https://doi.org/10.1038/s41893-021-00796-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41893-021-00796-2

This article is cited by

Search

Advanced search

Quick links

Nature Briefing: Translational Research

Sign up for the Nature Briefing: Translational Research newsletter — top stories in biotechnology, drug discovery and pharma.

Get what matters in translational research, free to your inbox weekly. Sign up for Nature Briefing: Translational Research