A staged representation electrochemical stimulated strategy to regulate intracellular reducing power for improving succinate production by Escherichia coli AFP111.

E. coli NADH/NAD+ microbial electrolysis cell oxidation reduction potential succinate

Journal

Biotechnology journal
ISSN: 1860-7314
Titre abrégé: Biotechnol J
Pays: Germany
ID NLM: 101265833

Informations de publication

Date de publication:
May 2021
Historique:
revised: 06 01 2021
received: 25 09 2020
accepted: 12 01 2021
pubmed: 14 2 2021
medline: 12 5 2021
entrez: 13 2 2021
Statut: ppublish

Résumé

Escherichia coli AFP111 was previously engineered for succinate production by eliminating byproducts of synthesis pathways. Still, the succinate yield is limited due to the insufficient NADH supplement, when fed with glucose. Microbial electrolysis cell (MEC) allows microorganisms to perform unbalanced fermentation by establishing polarized cathode interaction. In this study, a cathode electrode was used as an additional electron donor to improve succinate synthesis by E. coli AFP111. In MEC with -0.65 V (vs. Ag/AgCl) poised on cathode electrode, 95.72% electrons were transferred into cells via neutral red (NR), and the ratio of NADH/NAD Staged representation of electrochemical stimulated strategy is effective for succinate producing in engineered E. coli by regulating intracellular reducing power, which provides a new concept for producing reduced metabolite in unbalanced fermentation.

Sections du résumé

BACKGROUND BACKGROUND
Escherichia coli AFP111 was previously engineered for succinate production by eliminating byproducts of synthesis pathways. Still, the succinate yield is limited due to the insufficient NADH supplement, when fed with glucose. Microbial electrolysis cell (MEC) allows microorganisms to perform unbalanced fermentation by establishing polarized cathode interaction.
METHODS AND RESULTS RESULTS
In this study, a cathode electrode was used as an additional electron donor to improve succinate synthesis by E. coli AFP111. In MEC with -0.65 V (vs. Ag/AgCl) poised on cathode electrode, 95.72% electrons were transferred into cells via neutral red (NR), and the ratio of NADH/NAD
CONCLUSION AND IMPLICATIONS CONCLUSIONS
Staged representation of electrochemical stimulated strategy is effective for succinate producing in engineered E. coli by regulating intracellular reducing power, which provides a new concept for producing reduced metabolite in unbalanced fermentation.

Identifiants

pubmed: 33580738
doi: 10.1002/biot.202000415
doi:

Substances chimiques

Escherichia coli Proteins 0
Succinic Acid AB6MNQ6J6L
Glucose IY9XDZ35W2

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e2000415

Subventions

Organisme : Jiangsu Synergetic Innovation Center for Advanced Bio-Manufacture of China
Organisme : National Natural Science Foundation of China
ID : 21706124
Organisme : National Natural Science Foundation of China
ID : 21727818
Organisme : National Key R&D Program of China
ID : 2018YFA0901500
Organisme : Key Science and Technology Project of Jiangsu Province
ID : BE2016389

Informations de copyright

© 2021 Wiley-VCH GmbH.

Références

Thakker, C., Martinez, I., San, K. Y., & Bennett, G. N. (2012). Succinate production in Escherichia coli. Biotechnology Journal, 7, 213-224. https://doi.org/10.1002/biot.201100061.
Schindler, B. D., Joshi, R. V., & Vieille, C. (2014). Respiratory glycerol metabolism of Actinobacillus succinogenes 130Z for succinate production. Journal of Industrial Microbiology & Biotechnology, 41, 1339-1352. https://doi.org/10.1007/s10295-014-1480-x.
Litsanov, B., Brocker, M., & Bott, M. (2012). Toward homosuccinate fermentation: Metabolic engineering of Corynebacterium glutamicum for anaerobic production of succinate from glucose and formate. Applied and Environmental Microbiology, 78, 3325-3337. https://doi.org/10.1128/AEM.07790-11
Yan, D., Wang, C., Zhou, J., Liu, Y., & Yang, M. (2014). Construction of reductive pathway in Saccharomyces cerevisiae for effective succinic acid fermentation at low pH value. Bioresource Technology, 156, 232-239. https://doi.org/10.1016/j.biortech.2014.01.053.
Balzer, G. J., Thakker, C., Bennett, G. N., & San, K. Y. (2013). Metabolic engineering of Escherichia coli to minimize byproduct formate and improving succinate productivity through increasing NADH availability by heterologous expression of NAD+-dependent formate dehydrogenase. Metabolic Engineering, 20, 1-8. https://doi.org/10.1016/j.ymben.2013.07.005.
Van Heerden, C. D., & Nicol, W. (2013). Continuous and batch cultures of Escherichia coli KJ134 for succinic acid fermentation: Metabolic flux distributions and production characteristics. Microbial Cell Factories, 12, 80. https://doi.org/10.1186/1475-2859-12-80.
Xia, T., Altman, E., & Eiteman, M. A. (2015). Succinate production from xylose-glucose mixtures using a consortium of engineered Escherichia coli. Engineering in Life Sciences, 15, 65-72. https://doi.org/10.1002/elsc.201400113
Singh, A., Lynch, M. D., & Gill, R. T. (2009). Genes restoring redox balance in fermentation-deficient Escherichia coli NZN111. Metabolic Engineering, 11, 347-354. https://doi.org/10.1016/j.ymben.2009.07.002
Singh, A., Cher Soh, K., Hatzimanikatis, V., & Gill, R. T. (2011). Manipulating redox and ATP balancing for improved production of succinate in E. coli. Metabolic Engineering, 13, 76-81. https://doi.org/10.1016/j.ymben.2010.10.006
Zhang, X., Shanmugam, K. T., & Ingram, L. O. (2010). Fermentation of glycerol to succinate by metabolically engineered strains of Escherichia coli. Applied and Environmental Microbiology, 76, 2397-2401. https://doi.org/10.1128/AEM.02902-09.
Zhu, X., Tan, Z., Xu, H., Chen, J., & Zhang, X. (2014). Metabolic evolution of two reducing equivalent-conserving pathways for high-yield succinate production in Escherichia coli. Metabolic Engineering, 24, 87-96. https://doi.org/10.1016/j.ymben.2014.05.003.
She, P., Song, B., Xing, X. H., Loosdrecht, M. V., & Liu, Z. (2006). Electrolytic stimulation of bacteria Enterobacter dissolvens by a direct current. Biochemical Engineering Journal, 28, 23-29. https://doi.org/10.1016/j.bej.2005.08.033
Butler, J. E., Young, N. D., & Lovley, D. R. (2010). Evolution of electron transfer out of the cell: Comparative genomics of six Geobacter genomes. Bmc Genomics [Electronic Resource], 11, 40. https://doi.org/10.1186/1471-2164-11-40
Malaeb, L., Katuri, K. P., Logan, B. E., Maab, H., Nunes, S. P., & Saikaly, P. E. (2013). A hybrid microbial fuel cell membrane bioreactor with a conductive ultrafiltration membrane biocathode for wastewater treatment. Environmental Science & Technology, 47, 11821-11828. https://doi.org/10.1021/es4030113.
Villano, M., Monaco, G., Aulenta, F., & Majone, M. (2011). Electrochemically assisted methane production in a biofilm reactor. Journal of Power Sources, 196, 9467-9472. https://doi.org/10.1016/j.jpowsour.2011.07.016
Zhao, Y., Cao, W., Wang, Z., Zhang, B., Chen, K., & Ouyang, P. (2016). Enhanced succinic acid production from corncob hydrolysate by microbial electrolysis cells. Bioresource Technology, 202, 152-157. https://doi.org/10.1016/j.biortech.2015.12.002.
Wang, Z., Li, H., Feng, J., Zhang, A., Ying, H., He, X., Jiang, M., Chen, K., & Ouyang, P. (2018). Enhanced succinic acid production from polyacrylamide-pretreated cane molasses in microbial electrolysis cells. Journal of Chemical Technology and Biotechnology, 93, 855-860. https://doi.org/10.1002/jctb.5440.
Kracke, F., Vassilev, I., & Kromer, J. O. (2015). Microbial electron transport and energy conservation - the foundation for optimizing bioelectrochemical systems. Frontiers in Microbiology, 6, 575. https://doi.org/10.3389/fmicb.2015.00575.
Lovley, D. R. (2012). Electromicrobiology. Annual Review of Microbiology, 66, 391-409. https://doi.org/10.1146/annurev-micro-092611-150104
Lebedev, N., Mahmud, S., Griva, I., Blom, A., & Tender, L. M. (2015). On the electron transfer through Geobacter sulfurreducens PilA protein. Journal of Polymer Science Part B Polymer Physics, 53, 1706-1717. https://doi.org/10.1002/polb.23809.
Yong, Y., Yu, Y., Yang, Y., Liu, J., Wang, Y., & Song, H. (2013). Enhancement of extracellular electron transfer and bioelectricity output by synthetic porin. Biotechnology and Bioengineering, 110, 408-416. https://doi.org/10.1002/bit.24732.
Zhou, M., Chen, J., Freguia, S., Rabaey, K., & Keller, J. (2013). Carbon and electron fluxes during the electricity driven 1,3-propanediol biosynthesis from glycerol. Environmental Science & Technology, 47, 11199-11205. https://doi.org/10.1021/es402132r.
Ma, J., Li, F., Liu, R., Liang, L., & Ouyang, P. (2014). Succinic acid production from sucrose and molasses by metabolically engineered E. coli using a cell surface display system. Biochemical Engineering Journal, 91, 240-249. https://doi.org/10.1016/j.bej.2014.08.014.
Lohner, S. T., Jörg S. D., Logan, B. E., Leigh, J., & Spormann, A. M. (2014). Hydrogenase-independent uptake and metabolism of electrons by the archaeon methanococcus maripaludis. The ISME Journal, 8. https://doi.org/10.1038/ismej.2014.82.
Bond, D. R. (2003). Electricity production by Geobacter sulfurreducens attached to electrodes. Applied and Environmental Microbiology, 69, 1548-1555. https://doi.org/10.1128/AEM.69.3.1548-1555.2003
Park, D. H., Laivenieks, M., Guettler, M. V., Jain, M. K., & Zeikus, J. G. (1999). Microbial utilization of electrically reduced neutral red as the sole electron donor for growth and metabolite production. Applied and Environmental Microbiology, 65, 2912-2917.
Jiang, M., Chen, J., He, A., Wu, H., Kong, X., Liu, L., Yin, C.-y., Chen, W.-f., Pan, C. (2014). Enhanced acetone/butanol/ethanol production by Clostridium beijerinckii IB4 using pH control strategy. Process Biochemistry, 49, 1238-1244. https://doi.org/10.1016/j.procbio.2014.04.017.
Harrington, T. D., Mohamed, A., Tran, V. N., Biria, S., Gargouri, M., Park. J. J., Gang D. R., Beyenal, H. (2015). eNeutral red-mediated microbial electrosynthesis by Escherichia coli, Klebsiella pneumoniae, and Zymomonas mobilis. Bioresource Technology, 195, 57-65. https://doi.org/10.1016/j.biortech.2015.06.005
De Graef, M. R., Alexeeva, S., Snoep, J. L., & De Mattos, M. J. T. (1999). The steady-state internal redox state (NADH/NAD+) reflects the external redox state and is correlated with catabolic adaptation in Escherichia coli. Journal of Bacteriology, 181, 2351-2357. https://doi.org/10.1128/JB.181.8.2351-2357.1999
Pandit, A. V., & Mahadevan, R. (2011). In silico characterization of microbial electrosynthesis for metabolic engineering of biochemicals. Microbial Cell Factories, 10, 76. https://doi.org/10.1016/j.biortech.2015.06.005
Emde, R., & Schink, B. (1990). Enhanced propionate formation by Propionibacterium freudenreichii subsp. freudenreichii in a three-electrode amperometric culture system. Applied and Environmental Microbiology, 56, 2771-2776.
Xie, X., Criddle, C., & Cui, Y. (2015). Design and fabrication of bioelectrodes for microbial bioelectrochemical systems. Energy & Environmental Science, 8, 3418-3441. https://doi.org/10.1039/c5ee01862e.
Harrington, T. D., Tran, V. N., Mohamed, A., Renslow, R., Biria, S., Orfe, L., Call, D. R., & Beyenal, H. (2015). The mechanism of neutral red-mediated microbial electrosynthesis in Escherichia coli: Menaquinone reduction. Bioresource Technology, 192, 689-695. https://doi.org/10.1016/j.biortech.2015.06.037
Dumas, C., Basseguy, R., & Bergel, A. (2008). Microbial electrocatalysis with Geobacter sulfurreducens biofilm on stainless steel cathodes. Electrochimica Acta, 53, 2494-2500. https://doi.org/10.1016/j.electacta.2007.10.018.
Mu, Y., Yu, H. Q., & Wang, G. (2007). Evaluation of three methods for enriching H2-producing cultures from anaerobic sludge. Enzyme and Microbial Technology, 40, 947-953. https://doi.org/10.1016/j.enzmictec.2006.07.033
Okino, S., Inui, M., & Yukawa, H., Production of organic acids by Corynebacterium glutamicum under oxygen deprivation. Applied Microbiology and Biotechnology, 2005, 68, 475-480.
Gong, Z. Y., Yu, H., Zhang, J. Q., Li, F., & Song, H. (2020). Microbial electro-fermentation for synthesis of chemicals and biofuels driven by bi-directional extracellular electron transfer. Synthetic and Systems Biotechnology, 4, 304-313. https://doi.org/10.1016/j.synbio.2020.08.004.

Auteurs

Tianwen Zheng (T)

State Key Laboratory of Materials-Oriented Chemical Engineering, College of Biotechnology and Pharmaceutical Engineering, Nanjing Tech University, Nanjing, P. R. China.

Bin Xu (B)

State Key Laboratory of Materials-Oriented Chemical Engineering, College of Biotechnology and Pharmaceutical Engineering, Nanjing Tech University, Nanjing, P. R. China.

Yaliang Ji (Y)

State Key Laboratory of Materials-Oriented Chemical Engineering, College of Biotechnology and Pharmaceutical Engineering, Nanjing Tech University, Nanjing, P. R. China.

Wenming Zhang (W)

State Key Laboratory of Materials-Oriented Chemical Engineering, College of Biotechnology and Pharmaceutical Engineering, Nanjing Tech University, Nanjing, P. R. China.
Jiangsu National Synergetic Innovation Center for Advanced Materials (SICAM), Nanjing Tech University, Nanjing, P. R. China.

Fengxue Xin (F)

State Key Laboratory of Materials-Oriented Chemical Engineering, College of Biotechnology and Pharmaceutical Engineering, Nanjing Tech University, Nanjing, P. R. China.
Jiangsu National Synergetic Innovation Center for Advanced Materials (SICAM), Nanjing Tech University, Nanjing, P. R. China.

Weiliang Dong (W)

State Key Laboratory of Materials-Oriented Chemical Engineering, College of Biotechnology and Pharmaceutical Engineering, Nanjing Tech University, Nanjing, P. R. China.
Jiangsu National Synergetic Innovation Center for Advanced Materials (SICAM), Nanjing Tech University, Nanjing, P. R. China.

Ping Wei (P)

State Key Laboratory of Materials-Oriented Chemical Engineering, College of Biotechnology and Pharmaceutical Engineering, Nanjing Tech University, Nanjing, P. R. China.
Jiangsu National Synergetic Innovation Center for Advanced Materials (SICAM), Nanjing Tech University, Nanjing, P. R. China.

Jiangfeng Ma (J)

State Key Laboratory of Materials-Oriented Chemical Engineering, College of Biotechnology and Pharmaceutical Engineering, Nanjing Tech University, Nanjing, P. R. China.
Jiangsu National Synergetic Innovation Center for Advanced Materials (SICAM), Nanjing Tech University, Nanjing, P. R. China.

Min Jiang (M)

State Key Laboratory of Materials-Oriented Chemical Engineering, College of Biotechnology and Pharmaceutical Engineering, Nanjing Tech University, Nanjing, P. R. China.
Jiangsu National Synergetic Innovation Center for Advanced Materials (SICAM), Nanjing Tech University, Nanjing, P. R. China.

Articles similaires

Female Biofilms Animals Lactobacillus Mice
Host Specificity Bacteriophages Genomics Algorithms Escherichia coli
Biofilms Horses Animals Escherichia coli Mesenchymal Stem Cells

Aminoacid functionalised magnetite nanoparticles Fe

Spoială Angela, Motelica Ludmila, Ilie Cornelia-Ioana et al.
1.00
Magnetite Nanoparticles Tryptophan Biocompatible Materials Microbial Sensitivity Tests Humans

Classifications MeSH