A novel electrolytic gas lift reactor for efficient microbial electrosynthesis of hydrogen-oxidizing bacterial single-cell protein from CO₂

Abstract

Coupling water electrolysis with hydrogen-oxidizing bacteria (HOB) fermentation is a promising approach for single-cell protein (SCP) production. However, this inorganic-biological hybrid system is hindered by low efficiency, primarily due to the inhibition of electrochemical reactions on microbial activities and low hydrogen utilization. Here, we report an electrolytic gas lift reactor designed to improve the efficiency of this hybrid system for HOB-SCP production. By integrating the cathode of the electrolyzer with a gas lift reactor, the setup mitigated the inhibition of anodic reactive oxygen species on HOB and enhanced hydrogen utilization efficiency. By gradually increasing the current (1-2-4-6 A), the reactor achieved a maximum biomass yield of 0.20 g cell dry weight/L/d, a protein content of 58.3%, and a hydrogen utilization efficiency of 100%. The microbial community was dominated by HOB such as Ancylobacter (74.4%) and Xanthobacter (8.2%). These results indicated that the innovative reactor design effectively improved the performance of HOB-SCP production by inorganic-biological hybrid systems. The electrolytic gas lift reactor demonstrates substantial potential for scaling up and practical applications.

Keywords

Microbial electrosynthesis / Electrolytic gas lift reactor / Hydrogen-oxidizing bacteria / Single-cell protein

References

[1] SzczepanskiL, SassS, OldingC, et al. . Germans' attitudes toward the microbial protein Solein® and willingness to consume it– The effect of information-based framing. Food Quality and Preference, 2024.

[2] ChandraR, CollisS. Digital agriculture for small-scale producers. Commun ACM, 2021.

[3] FalconWP, NaylorRL, ShankarND. Rethinking global food demand for 2050. Popul Dev Rev, 2022.

[4] SantecchiaA, Castro-AmoedoR, NguyenT-V, et al. . The critical role of electricity storage for a clean and renewable European economy. Energy Environ Sci, 2023.

[5] WoernC, GrossmannL. Microbial gas fermentation technology for sustainable food protein production. Biotechnol Adv, 2023.

[6] SharmaB, YadavDK, MalakarS, et al. . Insect proteins– production technologies, bio-functional, and food applications: a perspective. Food Bioscience, 2024.

[7] RuuskanenV, GivirovskiyG, ElfvingJ, et al. . Neo-carbon Food concept: a pilot-scale hybrid biological–inorganic system with direct air capture of carbon dioxide. J Clean Prod, 2021.

[8] YuJ, DowA, PingaliS. The energy efficiency of carbon dioxide fixation by a hydrogen-oxidizing bacterium. Int J Hydrog Energy, 2013.

[9] PanderB, MortimerZ, WoodsC, et al. . Hydrogen oxidising bacteria for production of single-cell protein and other food and feed ingredients. Eng Biol, 2020.

[10] MatassaS, BoonN, VerstraeteW. Resource recovery from used water: the manufacturing abilities of hydrogen-oxidizing bacteria. Water Res, 2015.

[11] LiuC, SakimotoKK, ColonBC, et al. . Ambient nitrogen reduction cycle using a hybrid inorganic-biological system. Proc Natl Acad Sci U S A, 2017.

[12] YuJ. Fixation of carbon dioxide by a hydrogen-oxidizing bacterium for value-added products. World J Microbiol Biotechnol, 2018.

[13] NyyssöläA, OjalaLS, WuokkoM, et al. . Production of Endotoxin-Free Microbial Biomass for Food Applications by Gas Fermentation of Gram-positive H₂-Oxidizing Bacteria. ACS Food Sci Technol, 2021.

[14] CuiK, GuoK, Carvajal-ArroyoJM, et al. . An electrolytic bubble column with an external hollow fiber membrane gas–liquid contactor for effective microbial electrosynthesis of acetate from CO₂. Chem Eng J, 2023.

[15] YangX, JiangY, WangS, et al. . Self-sustained ammonium recovery from wastewater and upcycling for hydrogen-oxidizing bacteria-based power-to-protein conversion. Bioresour Technol, 2022.

[16] PanZ, HuX, CaiW, et al. . An electrolytic bubble column with gas recirculation for high-rate Microbial Electrosynthesis of acetate from CO₂. Ind Eng Chem Res, 2023.

[17] ChenMX, LiYJ, WuL, et al. . Optimal conditions and nitrogen removal performance of aerobic denitrifier Comamonas sp. pw-6 and its bioaugmented application in synthetic domestic wastewater treatment. Water Sci Technol, 2024.

[18] XueX, LiuZ, CaiW, et al. . Porous polyurethane particles enhanced the acetate production of a hydrogen-mediated microbial electrosynthesis reactor. Bioresource Technol Rep, 2022.

[19] WangW, LuW, PapadakisVG, et al. . Microbial protein production under mixotrophic mode: ammonium assimilation pathway and C/N ratio optimization. J Environ Chem Eng, 2024.

[20] ShangG, CuiK, CaiW, et al. . A 20 L electrochemical continuous stirred-tank reactor for high rate microbial electrosynthesis of methane from CO₂. Chem Eng J, 2023.

[21] CaiW, CuiK, LiuZ, et al. . An electrolytic-hydrogen-fed moving bed biofilm reactor for efficient microbial electrosynthesis of methane from CO₂. Chem Eng J, 2022.

[22] LuY, YuJ. Gas mass transfer with microbial CO₂ fixation and poly(3-hydroxybutyrate) synthesis in a packed bed bioreactor. Biochem Eng J, 2017.

[23] LinL, HuangH, ZhangX, et al. . Hydrogen-oxidizing bacteria and their applications in resource recovery and pollutant removal. Sci Total Environ, 2022.

[24] MoritaRY. Is H₂ the Universal Energy Source for Long-Term Survival?>. Microb Ecol, 1999.

[25] HuX, KerckhofFM, GhesquiereJ, et al. . Microbial protein out of Thin Air: fixation of Nitrogen Gas by an Autotrophic Hydrogen-Oxidizing Bacterial Enrichment. Environ Sci Technol, 2020.

[26] HuX, WeiW, ZhangJ, et al. . Nitrite self-degradation process in radish paocai under the synergistic regulation of prokaryotic microorganisms. Food Bioscience, 2024.

[27] FangX, YanY, XuY, et al. . Advanced electrolysis sulfur-based biofiltration for simultaneous total nitrogen removal and estrogen toxicity reduction from low carbon-to-nitrogen ratio wastewater. Bioresour Technol, 2024.

[28] PousN, BalaguerMD, MatassaS, et al. . Electro-cultivation of hydrogen-oxidizing bacteria to accumulate ammonium and carbon dioxide into protein-rich biomass. Bioresource Technol Rep, 2022.

[29] OverlandM, TausonAH, ShearerK, et al. . Evaluation of methane-utilising bacteria products as feed ingredients for monogastric animals. Arch Anim Nutr, 2010.

[30] Malinovsky AV. Reason for Indispensability of Threonine in Humans and Other Mammals in Comparative Aspect. Biochemistry (Mosc) (2017). https://doi.org/10.1134/S0006297917090097

[31] HouY, YinY, WuG. Dietary essentiality of nutritionally non-essential amino acids for animals and humans. Exp Biol Med (Maywood), 2015.

[32] RazakMA, BegumPS, ViswanathB, et al. . Multifarious Beneficial Effect of nonessential amino acid, Glycine: a review. Oxid Med Cell Longev, 2017.

[33] ChangK, GaoD, YanJ, et al. . Critical roles of protein arginine methylation in the Central Nervous System. Mol Neurobiol, 2023.

[34] Joint FAOWHO U. N. U. E. C. o. P., Amino Acid Requirements in Human, Food N et al. Protein and amino acid requirements in human nutrition: report of a joint FAO/WHO/UNU expert consultation. World Health Organization(2007). http://iris.who.int/handle/10665/43411

[35] MatassaS, VerstraeteW, PikaarI, et al. . Autotrophic nitrogen assimilation and carbon capture for microbial protein production by a novel enrichment of hydrogen-oxidizing bacteria. Water Res, 2016.

[36] BarbosaRG, PinheirovVH, VerstraeteVST, BoonW. Enrichment of hydrogen-oxidizing Bacteria from high-temperature and high-salinity environments. Appl Environ Microbiol, 2021.

[37] YangX, XuM, ZouR, et al. . Microbial protein production from CO₂, H₂, and recycled nitrogen: focusing on ammonia toxicity and nitrogen sources. J Clean Prod, 2021.

[38] YangX, JiangY, ZouR, et al. . Green electricity-driven simultaneous ammonia recovery and in-situ upcycling for microbial protein production. Chem Eng J, 2022.

[39] ChenK, MaC, ChengX, et al. . Construction of Cupriavidus necator displayed with superoxide dismutases for enhanced growth in bioelectrochemical systems. Bioresour Bioprocess, 2023.

Funding

National Natural Science Foundation of China(No. 52204043)

China Postdoctoral Science Foundation(No. 2024M762609)

RIGHTS & PERMISSIONS

Jiangnan University