Biofuel Research Journal

Biofuel Research Journal

Methanotroph biotransformation for nutrient recovery: a review of current strategies and future opportunities

Document Type : Review Paper

Authors
1 Laboratory of Environment-Enhancing Energy (E2E), College of Water Resources and Civil Engineering, China Agricultural University, Beijing, 100083, China.
2 Department of Biosystems Engineering, College of Agriculture, Isfahan University of Technology, Isfahan 84156-83111, Iran.
3 Department of Chemical Engineering, Biotechnology and Environmental Technology, University of Southern Denmark, Campusvej 55, DK-5230, Odense, Denmark.
4 Department of Environmental and Resource Engineering, Technical University of Denmark, Lyngby DK-2800, Denmark.
5 Key Laboratory of Non-point Source Pollution Control, Ministry of Agriculture and Rural Affairs, Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences, Beijing, 100081, China.
Abstract
The escalating global demand for protein and the imperative to meet sustainable development goals have driven the emergence of biotransformation platforms, with methanotrophs showing significant potential in this field. In this paper, the metabolism, nutritional requirements, cultivation strategies, and bioreactors of methanotrophs are reviewed. Integrating upstream and downstream technologies is also advocated to advance the development of methanotroph biotransformation platforms toward a circular economy model. The advancements in utilizing biogas as a viable carbon source and wastewater as a nitrogen source are discussed, emphasizing the need for detailed quality control and safety assessments to ensure the suitability of single-cell protein as animal feed. In general, by integrating advanced nutrient recovery technologies to define new process routes, methanotroph biotransformation platforms can bring better environmental benefits by reducing carbon emissions and saving resources. Shifting to renewable energy is crucial for achieving environmental sustainability. By using renewable energy to power microbial fermentation, biomass dehydration, and waste recycling, the platform can offset high energy consumption and attain significant market competitiveness with traditional protein sources.

Graphical Abstract

Methanotroph biotransformation for nutrient recovery: a review of current strategies and future opportunities

Highlights

  • Renewable energy is a crucial driver in promoting methanotroph biotransformation platforms.
  • Environmental benefits are the core competitiveness of the second-generation methanotroph single-cell protein (M-SCP).
  • M-SCP from waste should be tested in extensive feeding trials to verify safety.
  • Combining biotransformation and nutrient recovery from a circular economy perspective.

Keywords

  1. Abbasi, T., Tauseef, S.M., Abbasi, S.A., 2012. Anaerobic digestion for global warming control and energy generation-An overview. Renew. Sust. Energy Rev. 16(5), 3228-3242.
  2. Acosta, N., Sakarika, M., Kerckhof, F.M., Law, C.K.Y., De Vrieze, J., Rabaey, K., 2020. Microbial protein production from methane via electrochemical biogas upgrading. Chem. Eng. J. 391, 123625.
  3. Ahmadi, F., Lackner, M., 2024. Recent findings in methanotrophs: genetics, molecular ecology, and biopotential. Appl. Microbiol. Biotechnol. 108(1), 16-21.
  4. AlSayed, A., Fergala, A., Khattab, S., Eldyasti, A., 2018. Kinetics of type I methanotrophs mixed culture enriched from waste activated sludge. Biochem. Eng. J. 132, 60-67.
  5. Angelidaki, I., Treu, L., Tsapekos, P., Luo, G., Campanaro, S., Wenzel, H., Kougias, P.G., 2018. Biogas upgrading and utilization: current status and perspectives. Biotechnol. Adv. 36(2), 452-466.
  6. Angouria-Tsorochidou, E., Seghetta, M., Tremier, A., Thomsen, M., 2022. Life cycle assessment of digestate post-treatment and utilization. Sci. Total Environ. 815, 152764.
  7. Areniello, M., Matassa, S., Esposito, G., Lens, P.N.L., 2023. Biowaste upcycling into second-generation microbial protein through mixed-culture fermentation. Trends Biotechnol. 41(2), 197-213.
  8. Awe, O.W., Zhao, Y., Nzihou, A., Minh, D.P., Lyczko, N., 2017. A review of biogas utilisation, purification and upgrading technologies. Waste Biomass Valorization. 8(2), 267-283.
  9. Banks, M., Johnson, R., Giver, L., Bryant, G., Guo, M., 2022. Industrial production of microbial protein products. Curr. Opin. Biotechnol. 75, 102707.
  10. Bishoff, D., AlSayed, A., Fergala, A., Eldyasti, A., 2021. Redirecting methane for a novel biological nitrogen removal process using methanotrophic mixed culture in a sequential batch reactor. Chem. Eng. J. 404, 126487.
  11. Biswas, A., Takakuwa, F., Yamada, S., Matsuda, A., Saville, R.M., LeBlanc, A., Silverman, J.A., Sato, N., Tanaka, H., 2020. Methanotroph (Methylococcus capsulatus, Bath) bacteria meal as an alternative protein source for Japanese yellowtail, Seriola quinqueradiata. Aquaculture. 529, 735700.
  12. Bodelier, P.L., Laanbroek, H.J., 2004. Nitrogen as a regulatory factor of methane oxidation in soils and sediments. FEMS Microbiol. Ecol. 47(3), 265-277.
  13. Bolognesi, S., Cecconet, D., Callegari, A., Capodaglio, A.G., 2021. Bioelectrochemical treatment of municipal solid waste landfill mature leachate and dairy wastewater as co-substrates. Environ Sci Pollut Res Int 28(19), 24639-24649.
  14. Bordel, S., Rodríguez, Y., Hakobyan, A., Rodríguez, E., Lebrero, R., Muñoz, R., 2019. Genome scale metabolic modeling reveals the metabolic potential of three Type II methanotrophs of the genus Methylocystis. Metab. Eng. 54, 191-199.
  15. Castanheira, É.G., Freire, F., 2013. Greenhouse gas assessment of soybean production: implications of land use change and different cultivation systems. J. Cleaner Prod. 54, 49-60.
  16. Cathcart, A., Smyth, B.M., Lyons, G., Murray, S.T., Rooney, D., Johnston, C.R., 2023. Optimising mechanical separation of anaerobic digestate for total solids and nutrient removal. J. Environ. Manage. 345, 118449.
  17. Chen, Y., Chi, S., Zhang, S., Dong, X., Yang, Q., Liu, H., Zhang, W., Deng, J., Tan, B. and Xie, S., 2021. Replacement of fish meal with Methanotroph (Methylococcus capsulatus, Bath) bacteria meal in the diets of Pacific white shrimp (Litopenaeus vannamei). Aquaculture, 541, 736801.
  18. Clomburg, J.M., Crumbley, A.M., Gonzalez, R., 2017. Industrial biomanufacturing: the future of chemical production. Science. 355(6320).
  19. Dahlgren, E., Göçmen, C., Lackner, K., van Ryzin, G., 2013. Small Modular Infrastructure. Eng. Econ. 58(4), 231-264.
  20. Daud, S.M., Noor, Z.Z., Mutamim, N.S.A., Baharuddin, N.H., Faizal, A.N.M., Aris, A., Ibrahim, R.S., 2023. Microbial electrochemical systems and membrane bioreactor technology for wastewater treatment. Chem. Eng. Technol. 46(8), 1648-1663.
  21. de Carvalho, J.C., Magalhaes, A.I., Pereira, G.V.D., Medeiros, A.B.P., Sydney, E.B., Rodrigues, C., Aulestia, D.T.M., Vandenberghe, L.P.D., Soccol, V.T., Soccol, C.R., 2020. Microalgal biomass pretreatment for integrated processing into biofuels, food, and feed. Bioresour. Technol. 300, 122719.
  22. Dizon, L.S.H., Bertrand, R.S., Holmes, W.E., Hernandez, R.A., Fortela, D.L.B., Chistoserdov, A., Zappi, M.E., Revellame, E.D., 2023. Analysis of methanotroph populations from various sources for production of high-value products. Eng. Proc. 31(1), 30.
  23. Drosg, B., Werner, F., Al Seadi, T., Madsen, M., Linke, B., 2015. Nutrient Recovery by Biogas Digestate Processing.
  24. Du, J.X., Waite, T.D., Feng, J., Lei, Y., Tang, W.W., 2023. Coupled electrochemical methods for nitrogen and phosphorus recovery from wastewater: a review. Environ. Chem. Lett. 21(2), 885-909.
  25. El Abbadi, S.H., Sherwin, E.D., Brandt, A.R., Luby, S.P., Criddle, C.S., 2021. Displacing fishmeal with protein derived from stranded methane. Nat. Sustainability. 5(1), 47-56.
  26. Elyasi, S.N., He, L., Tsapekos, P., Rafiee, S., Khoshnevisan, B., Carbajales-Dale, M., Mohtasebi, S.S., Liu, H.B., Angelidaki, I., 2021. Could biological biogas upgrading be a sustainable substitution for water scrubbing technology? a case study in Denmark. Energy Convers. Manage. 245, 114550.
  27. Farago, M., Damgaard, A., Madsen, J.A., Andersen, J.K., Thornberg, D., Andersen, M.H., Rygaard, M., 2021. From wastewater treatment to water resource recovery: environmental and economic impacts of full-scale implementation. Water Res. 204, 117554.
  28. Fasaei, F., Bitter, J.H., Slegers, P.M., van Boxtel, A.J.B., 2018. Techno-economic evaluation of microalgae harvesting and dewatering systems. Algal Res. 31, 347-362.
  29. Fergala, A., AlSayed, A., Eldyasti, A., 2018. Behavior of type II methanotrophic bacteria enriched from activated sludge process while utilizing ammonium as a nitrogen source. Int. Biodeterior. Biodegrad. 130, 8-16.
  30. Garofalo, D.F.T., Novaes, R.M.L., Pazianotto, R.A.A., Maciel, V.G., Brandão, M., Shimbo, J.Z., Folegatti-Matsuura, M.I.S., 2022. Land-use change CO2 emissions associated with agricultural products at municipal level in Brazil. J. Cleaner Prod. 364, 132549.
  31. Gesicka, A., Oleskowicz-Popiel, P., Lezyk, M., 2021. Recent trends in methane to bioproduct conversion by methanotrophs. Biotechnol. Adv. 53, 107861.
  32. Gkotsis, P., Kougias, P., Mitrakas, M., Zouboulis, A., 2023. Biogas upgrading technologies-Recent advances in membrane-based processes. Int. J. Hydrogen Energy. 48(10), 3965-3993.
  33. Graham, A.E., Ledesma-Amaro, R., 2023. The microbial food revolution. Nat. Commun. 14(1), 2231.
  34. Gregory, G.J., Bennett, R.K., Papoutsakis, E.T., 2022. Recent advances toward the bioconversion of methane and methanol in synthetic methylotrophs. Metab. Eng. 71, 99-116.
  35. Gundupalli, M.P., Ansari, S., Vital da Costa, J.P., Qiu, F., Anderson, J., Luckert, M., Bressler, D.C., 2024. Bacterial single cell protein (BSCP): a sustainable protein source from methylobacterium species. Trends Food Sci. Tech. 147, 104426.
  36. Han, B., Su, T., Wu, H., Gou, Z., Xing, X.H., Jiang, H., Chen, Y., Li, X., Murrell, J.C., 2009. Paraffin oil as a "methane vector" for rapid and high cell density cultivation of Methylosinus trichosporium Appl. Microbiol. Biotechnol. 83(4), 669-677.
  37. He, R., Chen, M., Ma, R.C., Su, Y., Zhang, X., 2017. Ammonium conversion and its feedback effect on methane oxidation of Methylosinus sporium. J. Biosci. Bioeng. 123(4), 466-473.
  38. Hjorth, M., Christensen, K.V., Christensen, M.L., Sommer, S.G., 2010. Solid-liquid separation of animal slurry in theory and practice. a review. Agron. Sustainable Dev. 30(1), 153-180.
  39. Hou, D., Jassby, D., Nerenberg, R., Ren, Z.J., 2019. Hydrophobic Gas Transfer Membranes for Wastewater Treatment and Resource Recovery. Environ. Sci. Technol. 53(20), 11618-11635.
  40. IPCC AR6, 2021. Climate Change 2021-The Physical Science Basis. pp. 22-23.
  41. Jiang, W., Villamor, D.H., Peng, H.D., Chen, J., Liu, L., Haritos, V., Ledesma-Amaro, R., 2021. Metabolic engineering strategies to enable microbial utilization of C1 feedstocks. Nat. Chem. Biol. 17(8), 845-855.
  42. Kambara, H., Shinno, T., Matsuura, N., Matsushita, S., Aoi, Y., Kindaichi, T., Ozaki, N., Ohashi, A., 2022. Environmental factors affecting the community of methane-oxidizing bacteria. Microbes Environ. 37(1), ME27074.
  43. Kang, N.K., Chau, T.H.T., Lee, E.Y., 2024. Engineered methane biocatalysis: strategies to assimilate methane for chemical production. Curr. Opin. Biotechnol. 85, 103031.
  44. Kenney, G.E., Sadek, M., Rosenzweig, A.C., 2016. Copper-responsive gene expression in the methanotroph Methylosinus trichosporium Metallomics. 8(9), 931-940.
  45. Khan, S., Jain, G., Srivastava, A., Verma, P.C., Pande, V., Dubey, R.S., Khan, M., Haque, S., Ahmad, S., 2023. Enzymatic biomethanol production: future perspective. Sustainable Mater.Technol. 38, e00729.
  46. Khider, M.L.K., Brautaset, T., Irla, M., 2021. Methane monooxygenases: central enzymes in methanotrophy with promising biotechnological applications. World. J. Microb. Biot. 37(4).
  47. Khoshnevisan, B., Dodds, M., Tsapekos, P., Torresi, E., Smets, B.F., Angelidaki, I., Zhang, Y., Valverde-Perez, B., 2020a. Coupling electrochemical ammonia extraction and cultivation of methane oxidizing bacteria for production of microbial protein. J. Environ. Manage. 265, 110560.
  48. Khoshnevisan, B., Tabatabaei, M., Tsapekos, P., Rafiee, S., Aghbashlo, M., Lindeneg, S., Angelidaki, I., 2020b. Environmental life cycle assessment of different biorefinery platforms valorizing municipal solid waste to bioenergy, microbial protein, lactic and succinic acid. Renew. Sust. Energy Rev. 117, 109493.
  49. Khoshnevisan, B., Duan, N., Tsapekos, P., Awasthi, M.K., Liu, Z.D., Mohammadi, A., Angelidaki, I., Tsang, D.C.W., Zhang, Z.Q., Pan, J.T., Ma, L., Aghbashlo, M., Tabatabaei, M., Liu, H.B., 2021. A critical review on livestock manure biorefinery technologies: sustainability, challenges, and future perspectives. Renew. Sust. Energy Rev. 135, 110033.
  50. Khoshnevisan, B., He, L., Xu, M., Valverde-Pérez, B., Sillman, J., Mitraka, G.-C., Kougias, P.G., Zhang, Y., Yan, S., Ji, L., Carbajales-Dale, M., Elyasi, S.N., Marami, H., Tsapekos, P., Liu, H., Angelidaki, I., 2022. From renewable energy to sustainable protein sources: advancement, challenges, and future roadmaps. Renew. Sust. Energy Rev. 157, 112041.
  51. Khoshnevisan, B., Tsapekos, P., Zhang, Y., Valverde-Perez, B., Angelidaki, I., 2019. Urban biowaste valorization by coupling anaerobic digestion and single cell protein production. Bioresour. Technol. 290, 121743.
  52. Kim, I.T., Ahn, K.H., Lee, Y.E., Jeong, Y., Park, J.R., Shin, D.C., Jung, J.H., 2021. An experimental study on the biological fixation and effective use of carbon using biogas and bacterial community dominated by methanotrophs, methanol-oxidizing bacteria, and ammonia-oxidizing bacteria. Catalysts. 11(11), 1342.
  53. Kobayashi, Y., El-Wali, M., Guethmundsson, H., Guethmundsdottir, E.E., Friethjonsson, O.H., Karlsson, E.N., Roitto, M., Tuomisto, H.L., 2023. Life-cycle assessment of yeast-based single-cell protein production with oat processing side-stream. Sci. Total Environ. 873, 162318.
  54. Komarek, A.M., Dunston, S., Enahoro, D., Godfray, H.C.J., Herrero, M., Mason-D'Croz, D., Rich, K.M., Scarborough, P., Springmann, M., Sulser, T.B., Wiebe, K., Willenbockel, D., 2021. Income, consumer preferences, and the future of livestock-derived food demand. Global Environ. Change. 70, 102343.
  55. Kumar, P., Mehta, N., Abubakar, A.A., Verma, A.K., Kaka, U., Sharma, N., Sazili, A.Q., Pateiro, M., Kumar, M., Lorenzo, J.M., 2023. Potential alternatives of animal proteins for sustainability in the food sector. Food Rev. Int. 39(8), 5703-5728.
  56. Kwon, M., Ho, A., Yoon, S., 2019. Novel approaches and reasons to isolate methanotrophic bacteria with biotechnological potentials: recent achievements and perspectives. Appl. Microbiol. Biotechnol. 103(1), 1-8.
  57. Le, H.T.Q., Lee, E.Y., 2023. Methanotrophs: Metabolic versatility from utilization of methane to multi-carbon sources and perspectives on current and future applications. Bioresour. Technol. 384, 129296.
  58. Li, R., Fan, X.L., Jiang, Y.F., Wang, R.A., Guo, R.B., Zhang, Y.F., Fu, S.F., 2023. From anaerobic digestion to single cell protein synthesis: a promising route beyond biogas utilization. Water Res. 243, 120417.
  59. Luo, G., Angelidaki, I., 2012. Integrated biogas upgrading and hydrogen utilization in an anaerobic reactor containing enriched hydrogenotrophic methanogenic culture. Biotechnol. Bioeng. 109(11), 2729-2736.
  60. Manesis, A.C., Jodts, R.J., Hoffman, B.M., Rosenzweig, A.C., 2021. Copper binding by a unique family of metalloproteins is dependent on kynurenine formation. Proc. Natl. Acad. Sci. USA. 118(23), e2100680118.
  61. Marami, H., He, L., Rafiee, S., Khoshnevisan, B., Tsapekos, P., Mobli, H., Elyasi, S.N., Liu, H., Angelidaki, I., 2022a. Bridging to circular bioeconomy through a novel biorefinery platform on a wastewater treatment plant. Renew. Sust. Energy Rev. 154, 111895.
  62. Marami, H., Tsapekos, P., Khoshnevisan, B., Madsen, J.A., Andersen, J.K., Rafiee, S., Angelidaki, I., 2022b. Going beyond conventional wastewater treatment plants within circular bioeconomy concept - a sustainability assessment study. Water Sci. Technol. 85(6), 1878-1903.
  63. Marcellin, E., Angenent, L.T., Nielsen, L.K., Molitor, B., 2022. Recycling carbon for sustainable protein production using gas fermentation. Curr. Opin. Biotechnol. 76, 102723.
  64. Myung, J., Kim, M., Pan, M., Criddle, C.S., Tang, S.K.Y., 2016. Low energy emulsion-based fermentation enabling accelerated methane mass transfer and growth of poly(3-hydroxybutyrate)-accumulating methanotrophs. Bioresour. Technol. 207, 302-307.
  65. Ngoc Pham, D., Duc Nguyen, A., Hoang Anh Mai, D., Yeol Lee, E., 2023. Development of a novel methanotrophic platform to produce ectoine from methane and lignocellulose-derived sugars. Chem. Eng. J. 463, 142361.
  66. Nyerges, G., Stein, L.Y., 2009. Ammonia cometabolism and product inhibition vary considerably among species of methanotrophic bacteria. FEMS Microbiol. Lett. 297(1), 131-136.
  67. O'Shea, R., Lin, R., Wall, D.M., Browne, J.D., Murphy, J.D., 2022. A comparison of digestate management options at a large anaerobic digestion plant. J. Environ. Manage. 317, 115312.
  68. Overland, M., Skrede, A., Matre, T., 2001. Bacterial protein grown on natural gas as feed for pigs. Acta Agric. Scand. A. 51(2), 97-106.
  69. Pei, S.C., Liu, P., Parker, D.A., Mackie, R.I., Rao, C., 2022. Systems analysis of the effect of hydrogen sulfide on the growth of Methylococcus capsulatus Appl. Microbiol. Biotechnol. 106(23), 7879-7890.
  70. Peng, P., Kang-Yun, C.S., Chang, J., Gu, W.Y., DiSpirito, A.A., Semrau, J.D., 2022. Two tonb-dependent transporters in Methylosinus trichosporium OB3b are responsible for uptake of different forms of methanobactin and are involved in the canonical "copper switch". Appl. Environ. Microbiol. 88(1).
  71. Petersen, L.A., Villadsen, J., Jorgensen, S.B., Gernaey, K.V., 2017. Mixing and mass transfer in a pilot scale U-loop bioreactor. Biotechnol. Bioeng. 114(2), 344-354.
  72. Petersen, L.A.H., Bequette, B.W., Jorgensen, S.B., Villadsen, J., Christensen, I., Gernaey, K.V., 2020. Modeling and system identification of an unconventional bioreactor used for single cell protein production. Chem. Eng. J. 390, 124438.
  73. Picone, N., Blom, P., Wallenius, A.J., Hogendoorn, C., Mesman, R., Cremers, G., Gagliano, A.L., D'Alessandro, W., Quatrini, P., Jetten, M.S.M., Pol, A., Op den Camp, H.J.M., 2021. Methylacidimicrobium thermophilum AP8, a novel methane- and hydrogen-oxidizing bacterium isolated from volcanic soil on Pantelleria Island, Italy. Front. Microbiol. 12, 637762.
  74. Qin, S., Wang, K., Gao, F.Z., Ge, B.S., Cui, H.L., Li, W.J., 2023. Biotechnologies for bulk production of microalgal biomass: from mass cultivation to dried biomass acquisition. Biotechnol. Biofuels Bioprod. 16(1), 131.
  75. Rajesh, M., Kamalam, B.S., Sharma, P., Verma, V.C., Pandey, A., Dubey, M.K., Ciji, A., Akhtar, M.S., Pandey, N., Sarma, D., Kaushik, S.J., 2022. Evaluation of a novel methanotroph bacteria meal grown on natural gas as fish meal substitute in rainbow trout, Oncorhynchus mykiss. Aquacult. Res. 53(6), 2159-2174.
  76. Rasouli, Z., Valverde-Pérez, B., D’Este, M., De Francisci, D., Angelidaki, I., 2018. Nutrient recovery from industrial wastewater as single cell protein by a co-culture of green microalgae and methanotrophs. Biochem. Eng. J. 134, 129-135.
  77. Ritala, A., Hakkinen, S.T., Toivari, M., Wiebe, M.G., 2017. Single Cell Protein-State-of-the-Art, Industrial Landscape and Patents 2001-2016. Front. Microbiol. 8, 300589.
  78. Roberts, N., Hilliard, M., He, Q.P., Wang, J., 2020. A microalgae-methanotroph coculture is a promising platform for fuels and chemical production from wastewater. Front. Energy Res. 8, 563352.
  79. Rocha-Rios, J., Muñoz, R., Revah, S., 2010. Effect of silicone oil fraction and stirring rate on methane degradation in a stirred tank reactor. J. Chem. Technol. Biotechnol. 85(3), 314-319.
  80. Rocha-Rios, J., Quijano, G., Thalasso, F., Revah, S., Muñoz, R., 2011. Methane biodegradation in a two-phase partition internal loop airlift reactor with gas recirculation. J. Chem. Technol. Biotechnol. 86(3), 353-360.
  81. Rodríguez Arredondo, M., Kuntke, P., Jeremiasse, A.W., Sleutels, T.H.J.A., Buisman, C.J.N., ter Heijne, A., 2015. Bioelectrochemical systems for nitrogen removal and recovery from wastewater. Environ. Sci. Water Res.Technol. 1(1), 22-33.
  82. Ruiz-Ruiz, P., Gomez-Borraz, T.L., Revah, S., Morales, M., 2020. Methanotroph-microalgae co-culture for greenhouse gas mitigation: effect of initial biomass ratio and methane concentration. Chemosphere. 259, 127418.
  83. Safaric, L., Björn, A., Svensson, B.H., Bastviken, D., Yekta, S.S., 2023. Rheology, micronutrients, and process disturbance in continuous stirred-tank biogas reactors. Ind. Eng. Chem. Res. 62(43), 17372-17384.
  84. Sahoo, K.K., Sinha, A., Das, D., 2023. Process engineering strategy for improved methanol production in Methylosinus trichosporium through enhanced mass transfer and solubility of methane and carbon dioxide. Bioresour. Technol. 371, 128603.
  85. Sakarika, M., Ganigué, R., Rabaey, K., 2022. Methylotrophs: from C1 compounds to food. Curr. Opin. Biotechnol. 75, 102685.
  86. Salehi, R., Chaiprapat, S., 2021. Conversion of biogas from anaerobic digestion to single cell protein and bio-methanol: mechanism, microorganisms and key factors-a review. Environ. Eng. Res. 27(4), 210109-210100.
  87. Schmitz, R.A., Peeters, S.H., Versantvoort, W., Picone, N., Pol, A., Jetten, M.S.M., Op den Camp, H.J.M., 2021. Verrucomicrobial methanotrophs: ecophysiology of metabolically versatile acidophiles. FEMS Microbiol. Rev. 45(5), fuab007.
  88. Schoyen, H.F., Hetland, H., Rouvinen-Watt, K., Skrede, A., 2007. Growth performance and ileal and total tract amino acid digestibility in broiler chickens fed diets containing bacterial protein produced on natural gas. Poult. Sci. 86(1), 87-93.
  89. Shahzad, H.M.A., Almomani, F., Shahzad, A., Mahmoud, K.A., Rasool, K., 2024. Challenges and opportunities in biogas conversion to microbial protein: a pathway for sustainable resource recovery from organic waste. Process Saf. Environ.Prot. 185, 644-659.
  90. Sharif, M., Zafar, M.H., Aqib, A.I., Saeed, M., Farag, M.R., Alagawany, M., 2021. Single cell protein: sources, mechanism of production, nutritional value and its uses in aquaculture nutrition. Aquaculture. 531, 735885.
  91. Singh, R., Ryu, J., Kim, S.W., 2019. Microbial consortia including methanotrophs: some benefits of living together. J. Microbiol. 57(11), 939-952.
  92. Spiller, M., Muys, M., Papini, G., Sakarika, M., Buyle, M., Vlaeminck, S.E., 2020. Environmental impact of microbial protein from potato wastewater as feed ingredient: comparative consequential life cycle assessment of three production systems and soybean meal. Water Res. 171, 115406.
  93. Sun, Z.F., Zhao, L., Wu, K.K., Wang, Z.H., Wu, J.T., Chen, C., Yang, S.S., Wang, A.J., Ren, N.Q., 2022. Overview of recent progress in exogenous hydrogen supply biogas upgrading and future perspective. Sci. Total Environ. 848, 157824.
  94. Tambone, F., Orzi, V., D'Imporzano, G., Adani, F., 2017. Solid and liquid fractionation of digestate: Mass balance, chemical characterization, and agronomic and environmental value. Bioresour. Technol. 243, 1251-1256.
  95. The Good Food Institute, 2023. Alternative Proteins: 2022 State of Global Policy Report.
  96. Tsapekos, P., Khoshnevisan, B., Alvarado-Morales, M., Zhu, X., Pan, J., Tian, H., Angelidaki, I., 2021. Upcycling the anaerobic digestion streams in a bioeconomy approach: a review. Renew. Sust. Energy Rev. 151, 111635.
  97. Tsapekos, P., Khoshnevisan, B., Zhu, X., Zha, X., Angelidaki, I., 2019. Methane oxidising bacteria to upcycle effluent streams from anaerobic digestion of municipal biowaste. J. Environ. Manage. 251, 109590.
  98. Tsapekos, P., Zhu, X., Pallis, E., Angelidaki, I., 2020. Proteinaceous methanotrophs for feed additive using biowaste as carbon and nutrients source. Bioresour. Technol. 313, 123646.
  99. Valverde-Pérez, B., Pape, M.L., Kjeldgaard, A.F., Zachariae, A.A., Schneider, C., Hélix-Nielsen, C., Zarebska, A., Smets, B.F., 2020a. Dewatering methanotrophic enrichments intended for single cell protein production using biomimetic aquaporin forward osmosis membranes. Sep. Purif. Technol. 235, 116133.
  100. Valverde-Pérez, B., Xing, W., Zachariae, A.A., Skadborg, M.M., Kjeldgaard, A.F., Palomo, A., Smets, B.F., 2020b. Cultivation of methanotrophic bacteria in a novel bubble-free membrane bioreactor for microbial protein production. Bioresour. Technol. 310, 123388.
  101. van der Ha, D., Bundervoet, B., Verstraete, W., Boon, N., 2011. A sustainable, carbon neutral methane oxidation by a partnership of methane oxidizing communities and microalgae. Water Res. 45(9), 2845-2854.
  102. Verbeeck, K., De Vrieze, J., Pikaar, I., Verstraete, W., Rabaey, K., 2021. Assessing the potential for up-cycling recovered resources from anaerobic digestion through microbial protein production. Microb. Biotechnol. 14(3), 897-910.
  103. Vethathirri, R.S., Santillan, E., Wuertz, S., 2021. Microbial community-based protein production from wastewater for animal feed applications. Bioresour. Technol. 341, 125723.
  104. Wan, Y.X., Li, R.X., Wang, X., Liao, C.M., 2023. Recovery of reactive nitrogen from wastewater using bioelectrochemical systems. Sep. Purif. Technol. 327, 125002.
  105. Wang, S., Liu, Q.X., Li, J., Wang, Z.W., 2021. Methane in wastewater treatment plants: status, characteristics, and bioconversion feasibility by methane oxidizing bacteria for high value-added chemicals production and wastewater treatment. Water Res. 198, 117122.
  106. Willett, W., Rockstrom, J., Loken, B., Springmann, M., Lang, T., Vermeulen, S., Garnett, T., Tilman, D., DeClerck, F., Wood, A., Jonell, M., Clark, M., Gordon, L.J., Fanzo, J., Hawkes, C., Zurayk, R., Rivera, J.A., De Vries, W., Sibanda, L.M., Afshin, A., Chaudhary, A., Herrero, M., Agustina, R., Branca, F., Lartey, A., Fan, S.G., Crona, B., Fox, E., Bignet, V., Troell, M., Lindahl, T., Singh, S., Cornell, S.E., Reddy, K.S., Narain, S., Nishtar, S., Murray, C.J.L., 2019. Food in the anthropocene: the EAT-Lancet Commission on healthy diets from sustainable food systems. Lancet. 393(10170), 447-492.
  107. Wood, A.P., Aurikko, J.P., Kelly, D.P., 2004. A challenge for 21st century molecular biology and biochemistry: what are the causes of obligate autotrophy and methanotrophy?. FEMS Microbiol. Rev. 28(3), 335-352.
  108. Wu, H., Vaneeckhaute, C., 2022. Nutrient recovery from wastewater: a review on the integrated Physicochemical technologies of ammonia stripping, adsorption and struvite precipitation. Chem. Eng. J. 433, 133664.
  109. Xiang, S., Liu, Y., Zhang, G., Ruan, R., Wang, Y., Wu, X., Zheng, H., Zhang, Q., Cao, L., 2020. New progress of ammonia recovery during ammonia nitrogen removal from various wastewaters. World J. Microbiol. Biotechnol. 36(10), 144.
  110. Xie, M., Shon, H.K., Gray, S.R., Elimelech, M., 2016. Membrane-based processes for wastewater nutrient recovery: technology, challenges, and future direction. Water Res. 89, 210-221.
  111. Xu, J., Wang, J., Ma, C.L., Wei, Z.X., Zhai, Y.D., Tian, N., Zhu, Z.G., Xue, M., Li, D.M., 2023. Embracing a low-carbon future by the production and marketing of C1 gas protein. Biotechnol. Adv. 63, 108096.
  112. Xu, M., Zhou, H., Yang, X., Angelidaki, I., Zhang, Y., 2020. Sulfide restrains the growth of Methylocapsa acidiphila converting renewable biogas to single cell protein. Water Res. 184, 116138.
  113. Xu, M., Zhao, D., Zhu, X., Su, Y., Angelidaki, I., Zhang, Y., 2021a. Biogas upgrading and valorization to single-cell protein in a bioinorganic electrosynthesis system. Chem. Eng. J. 426, 131837.
  114. Xu, M., Zhou, H., Zou, R., Yang, X., Su, Y., Angelidaki, I., Zhang, Y., 2021b. Beyond the farm: making edible protein from CO2 via hybrid bioinorganic electrosynthesis. One Earth. 4(6), 868-878.
  115. Yang, D.H., Chen, Q.H., Liu, R., Song, L., Zhang, Y., Dai, X.H., 2022a. Ammonia recovery from anaerobic digestate: state of the art, challenges and prospects. Bioresour. Technol. 363, 127957.
  116. Yang, X., Jiang, Y., Zou, R., Xu, M., Su, Y., Angelidaki, I., Zhang, Y., 2022b. Green electricity-driven simultaneous ammonia recovery and in-situ upcycling for microbial protein production. Chem. Eng. J. 430, 132890.
  117. Yang, Z.Y., Tsapekos, P., Zhang, Y.F., Zhang, Y., Angelidaki, I., Wang, W., 2021. Bio-electrochemically extracted nitrogen from residual resources for microbial protein production. Bioresour. Technol. 337, 125353.
  118. Yu, M.H., Li, X.S., Wang, J., Longshaw, M., Song, K., Wang, L., Zhang, C.X., Lu, K.I., 2023. Substituting fish meal with a bacteria protein (Methylococcus capsulatus, Bath) grown on natural gas: effects on growth non-specific immunity and gut health of spotted seabass (Lateolabrax maculatus). Anim. Feed Sci. Technol. 296, 115556.
  119. Zha, X., Tsapekos, P., Zhu, X., Khoshnevisan, B., Lu, X., Angelidaki, I., 2021. Bioconversion of wastewater to single cell protein by methanotrophic bacteria. Bioresour. Technol. 320(Pt A), 124351.
  120. Zhang, J., Yu, M., Wang, J., Longshaw, M., Song, K., Wang, L., Li, X., Zhang, C., Lu, K., 2023. Methanotroph (Methylococcus capsulatus, Bath) bacteria meal alleviates soybean meal-induced enteritis in spotted seabass (Lateolabrax maculatus) by modulating immune responses and the intestinal flora. Aquaculture. 575.
  121. Zheng, J., Zhang, W., Dan, Z., Cao, X., Cui, K., Zhu, S., Zhuang, Y., Mai, K., Ai, Q., 2023. Effects of fish meal replaced by methanotroph bacteria meal (Methylococcus capsulatus) on growth, body composition, antioxidant capacity, amino acids transporters and protein metabolism of turbot juveniles (Scophthalmus maximus). Aquaculture. 562, 738782.
  122. Zhou, J.L., Ming, S.Q., Liu, Q.R., Zhang, Y.H., Duan, N., 2024. Revealing the synergy mechanisms of organic components anaerobic co-digestion from the prevailing tendency of endogenous inhibitors. Chem. Eng. J. 479, 147707.
  123. Zhou, J.L., Qu, A.A., Ming, S.Q., Zhang, Y.H., Duan, N., 2022. Binary-component anaerobic co-digestion: synergies and microbial profiles. Renewable Energy. 201, 1-10.