Converting carbon dioxide to butyrate with an engineered strain of Clostridium ljungdahlii
Open accessAbstract
Microbial conversion of carbon dioxide to organic commodities via syngas metabolism or microbial electrosynthesis is an attractive option for production of renewable biocommodities. The recent development of an initial genetic toolbox for the acetogen Clostridium ljungdahlii has suggested that C. ljungdahlii may be an effective chassis for such conversions. This possibility was evaluated by engineering a strain to produce butyrate, a valuable commodity that is not a natural product of C. ljungdahlii metabolism. Heterologous genes required for butyrate production from acetyl-coenzyme A (CoA) were identified and introduced initially on plasmids and in subsequent strain designs integrated into the C. ljungdahlii chromosome. Iterative strain designs involved increasing translation of a key enzyme by modifying a ribosome binding site, inactivating the gene encoding the first step in the conversion of acetyl-CoA to acetate, disrupting the gene which encodes the primary bifunctional aldehyde/alcohol dehydrogenase for ethanol production, and interrupting the gene for a CoA transferase that potentially represented an alternative route for the production of acetate. These modifications yielded a strain in which ca. 50 or 70% of the carbon and electron flow was diverted to the production of butyrate with H2 or CO as the electron donor, respectively. These results demonstrate the possibility of producing high-value commodities from carbon dioxide with C. ljungdahlii as the catalyst. Importance: The development of a microbial chassis for efficient conversion of carbon dioxide directly to desired organic products would greatly advance the environmentally sustainable production of biofuels and other commodities. Clostridium ljungdahlii is an effective catalyst for microbial electrosynthesis, a technology in which electricity generated with renewable technologies, such as solar or wind, powers the conversion of carbon dioxide and water to organic products. Other electron donors for C. ljungdahlii include carbon monoxide, which can be derived from industrial waste gases or the conversion of recalcitrant biomass to syngas, as well as hydrogen, another syngas component. The finding that carbon and electron flow in C. ljungdahlii can be diverted from the production of acetate to butyrate synthesis is an important step toward the goal of renewable commodity production from carbon dioxide with this organism.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Cre-Lox has been successfully demonstrated in the acetogen C. ljungdahlii.
“Cre-Lox has been successfully demonstrated in the acetogen C. ljungdahlii (Ueki et al., 2014).”
From Gas Fermentation—A Flexible Platform for Commercial Scale Production of Low-Carbon-Fuels and Chemicals from Waste and Renewable Feedstocks (2016) · cites this paper as Ueki et al., 2014
C. ljungdahlii with chromosomal integration of C. acetobutylicum butyrate biosynthetic genes into the pta promoter region produced up to 881 mg/L butyrate under H2/CO2 in bottles.
“| C. ljungdahlii | Chromosomal integration (single crossover recombination) of C. acetobutylicum butyrate biosynthetic genes (thl-crt-bcd-etfB-etfA-hbd-ptb-buk) into pta promoter region | Production of up to 881 mg/L butyrate under H2/CO2 in bottles | Ueki et al., 2014 |”
From Gas Fermentation—A Flexible Platform for Commercial Scale Production of Low-Carbon-Fuels and Chemicals from Waste and Renewable Feedstocks (2016) · cites this paper as Ueki et al., 2014
H2/CO2 gas fermentations mostly produce acetate, though production of ethanol and other products such as acetone or butyrate have been described, albeit at lower productivity compared to CO.
“H2/CO2 gas fermentations mostly produce acetate, though production of ethanol (Mock et al., 2015) and other products such as acetone (Schiel-Bengelsdorf and Dürre, 2012; Hoffmeister et al., 2016) or butyrate (Ueki et al., 2014) have been described, albeit at lower productivity compared to CO.”
From Gas Fermentation—A Flexible Platform for Commercial Scale Production of Low-Carbon-Fuels and Chemicals from Waste and Renewable Feedstocks (2016) · cites this paper as Ueki et al., 2014
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Louis, P., & Flint, H. J. (2009) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2009.01514.x · Cited by 2,179 · see citing works
Nevin, K. P., Woodard, T. L., Franks, A. E., Summers, Z. M., & Lovley, D. R. (2010) · mBio · doi:10.1128/mbio.00103-10 · Cited by 1,068 · see citing works
Self-citationMoo‐Young, M., Bull, A. T., Dalton, H., Cooney, C. L., Humphrey, A. E., Blanch, H. W., Drew, S. W., Wang, D. I. C., Robinson, C. W., Howell, J., et al. (1986) · Annales de l Institut Pasteur Virologie · doi:10.1016/s0769-2617(86)80233-7 · Cited by 982 · see citing works
Buckel, W., & Thauer, R. K. (2013) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2012.07.002 · Cited by 797 · see citing works
Nevin, K. P., Hensley, S. A., Franks, A. E., Summers, Z. M., Ou, J., Woodard, T. L., Snoeyenbos-West, O., & Lovley, D. R. (2011) · Applied and Environmental Microbiology · doi:10.1128/aem.02642-10 · Cited by 722 · see citing works
Self-citation<i>Clostridium ljungdahlii</i> represents a microbial production platform based on syngas
Köpke, M., Held, C., Hujer, S., Liesegang, H., Wiezer, A., Wollherr, A., Ehrenreich, A., Liebl, W., Gottschalk, G., & Dürre, P. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1004716107 · Cited by 660 · see citing works
Potential for Direct Interspecies Electron Transfer in Methanogenic Wastewater Digester Aggregates
Morita, M., Malvankar, N. S., Franks, A. E., Summers, Z. M., Giloteaux, L., Rotaru, A., Rotaru, C., & Lovley, D. R. (2011) · mBio · doi:10.1128/mbio.00159-11 · Cited by 563 · see citing works
Self-citationBiomass-derived syngas fermentation into biofuels: Opportunities and challenges
Munasinghe, P. C., & Khanal, S. K. (2010) · Bioresource Technology · doi:10.1016/j.biortech.2009.12.098 · Cited by 559 · see citing works
Flagella and bacterial pathogenicity
Duan, Q., Zhou, M., Zhu, L., & Zhu, G. (2012) · Journal of Basic Microbiology · doi:10.1002/jobm.201100335 · Cited by 489 · see citing works
A modular system for Clostridium shuttle plasmids
Heap, J. T., Pennington, O. J., Cartman, S. T., & Minton, N. P. (2009) · Journal of Microbiological Methods · doi:10.1016/j.mimet.2009.05.004 · Cited by 489 · see citing works
Sauer, B. (1987) · Molecular and Cellular Biology · doi:10.1128/mcb.7.6.2087 · Cited by 482 · see citing works
Microbiology of synthesis gas fermentation for biofuel production
Henstra, A. M., Sipma, J., Rinzema, A., & Stams, A. J. M. (2007) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2007.03.008 · Cited by 449 · see citing works
Commercial Biomass Syngas Fermentation.
Daniell, J., Köpke, M., & Simpson, S. (2012) · Energies · doi:10.3390/en5125372 · Cited by 444 · see citing works
Li, F., Hinderberger, J., Seedorf, H., Zhang, J., Buckel, W., & Thauer, R. K. (2008) · Journal of Bacteriology · doi:10.1128/jb.01417-07 · Cited by 420 · see citing works
Köpke, M., Mihalcea, C., Liew, F. E., Tizard, J. H., Ali, M., Conolly, J. J., Al‐Sinawi, B., & Simpson, S. D. (2011) · Applied and Environmental Microbiology · doi:10.1128/aem.00355-11 · Cited by 418 · see citing works
Lovley, D. R., & Nevin, K. P. (2013) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2013.02.012 · Cited by 343 · see citing works
Self-citationBiegel, E., Schmidt, S., González, J. M., & Müller, V. (2010) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-010-0555-8 · Cited by 340 · see citing works
Clostridium ljungdahlii sp. nov., an Acetogenic Species in Clostridial rRNA Homology Group I
Tanner, R. S., Miller, L. M., & Yang, D. (1993) · International Journal of Systematic Bacteriology · doi:10.1099/00207713-43-2-232 · Cited by 303 · see citing works
Jang, Y., Lee, J., Lee, J., Park, J. H., Im, J. A., Eom, M., Lee, J., Lee, S.-H., Song, H., Cho, J. H., et al. (2012) · mBio · doi:10.1128/mbio.00314-12 · Cited by 267 · see citing works
Bioconversion of synthesis gas to second generation biofuels: A review
Mohammadi, M., Najafpour, G. D., Younesi, H., Lahijani, P., Uzir, M. H., & Mohamed, A. R. (2011) · Renewable and Sustainable Energy Reviews · doi:10.1016/j.rser.2011.07.124 · Cited by 261 · see citing works
Fast, A. G., & Papoutsakis, E. T. (2012) · Current Opinion in Chemical Engineering · doi:10.1016/j.coche.2012.07.005 · Cited by 247 · see citing works
A shift in the current: New applications and concepts for microbe-electrode electron exchange
Lovley, D. R., & Nevin, K. P. (2011) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2011.01.009 · Cited by 231 · see citing works
Self-citationEvaluating metabolic stress and plasmid stability in plasmid DNA production by Escherichia coli
Silva, F., Queiroz, J. A., & Domingues, F. (2012) · Biotechnology Advances · doi:10.1016/j.biotechadv.2011.12.005 · Cited by 229 · see citing works
Current Progress on Butyric Acid Production by Fermentation
Zhang, C., Yang, H. M., Yang, F., & Ma, Y.-J. (2009) · Current Microbiology · doi:10.1007/s00284-009-9491-y · Cited by 224 · see citing works
Green, E. M., Boynton, Z. L., Harris, L. M., Rudolph, F. B., Papoutsakis, E. T., & Bennett, G. N. (1996) · Microbiology · doi:10.1099/13500872-142-8-2079 · Cited by 216 · see citing works
Bacterial synthesis gas (syngas) fermentation
Bengelsdorf, F. R., Straub, M., & Dürre, P. (2013) · Environmental Technology · doi:10.1080/09593330.2013.827747 · Cited by 211 · see citing works
Tremblay, P., Zhang, T., Dar, S. A., Leang, C., & Lovley, D. R. (2012) · mBio · doi:10.1128/mbio.00406-12 · Cited by 208 · see citing works
Self-citationTripathi, S. A., Olson, D. G., Argyros, D. A., Miller, B. B., Barrett, T. F., Murphy, D. M., McCool, J. D., Warner, A. K., Rajgarhia, V. B., Lynd, L. R., et al. (2010) · Applied and Environmental Microbiology · doi:10.1128/aem.01484-10 · Cited by 207 · see citing works
Plasmid Effects onEscherichia coliMetabolism
Ricci, J. C. D., & Hernández, M. E. (2000) · Critical Reviews in Biotechnology · doi:10.1080/07388550008984167 · Cited by 204 · see citing works
The Future of Butyric Acid in Industry
Dwidar, M., Park, J. Y., Mitchell, R. J., & Sang, B. (2012) · The Scientific World JOURNAL · doi:10.1100/2012/471417 · Cited by 202 · see citing works
Leang, C., Ueki, T., Nevin, K. P., & Lovley, D. R. (2013) · Applied and Environmental Microbiology · doi:10.1128/aem.02891-12 · Cited by 202 · see citing works
Self-citationAdvances in biotechnological production of butyric acid
Zigová, J., & Šturdı́k, E. (2000) · Journal of Industrial Microbiology & Biotechnology · doi:10.1038/sj.jim.2900795 · Cited by 187 · see citing works
Nagarajan, H., Sahin, M., Nogales, J., Latif, H., Lovley, D. R., Ebrahim, A., & Zengler, K. (2013) · Microbial Cell Factories · doi:10.1186/1475-2859-12-118 · Cited by 170 · see citing works
Self-citationRotaru, A., Shrestha, P. M., Liu, F., Ueki, T., Nevin, K., Summers, Z. M., & Lovley, D. R. (2012) · Applied and Environmental Microbiology · doi:10.1128/aem.01946-12 · Cited by 160 · see citing works
Self-citationButyric acid and hydrogen production by Clostridium tyrobutyricum ATCC 25755 and mutants
Liu, X., Zhu, Y., & Yang, S. (2005) · Enzyme and Microbial Technology · doi:10.1016/j.enzmictec.2005.07.008 · Cited by 157 · see citing works
Bruant, G., Lévesque, M.-J., Peter, C., Guiot, S. R., & Masson, L. (2010) · PLoS ONE · doi:10.1371/journal.pone.0013033 · Cited by 139 · see citing works
Jiang, L., Wang, J., Liang, S., Cai, J., Xu, Z., Cen, P., Yang, S., & Li, S. (2010) · Biotechnology and Bioengineering · doi:10.1002/bit.22927 · Cited by 138 · see citing works
Perez, J. M., Richter, H., Loftus, S. E., & Angenent, L. T. (2013) · Biotechnology and Bioengineering · doi:10.1002/bit.24786 · Cited by 126 · see citing works
Lactose-inducible system for metabolic engineering of Clostridium ljungdahlii
Banerjee, A., Leang, C., Ueki, T., Nevin, K. P., & Lovley, D. R. (2014) · Applied and Environmental Microbiology · doi:10.1128/aem.03666-13 · Cited by 126 · see citing works
Self-citationSynthesis gas as substrate for the biological production of fuels and chemicals
Phillips, J. R., Clausen, E. C., & Gaddy, J. L. (1994) · Applied Biochemistry and Biotechnology · doi:10.1007/bf02941794 · Cited by 122 · see citing works
Al-Hinai, M. A., Fast, A. G., & Papoutsakis, E. T. (2012) · Applied and Environmental Microbiology · doi:10.1128/aem.02214-12 · Cited by 122 · see citing works
Miscibility of bacterial poly(3-hydroxybutyrate) with cellulose esters
Scandola, M., Ceccorulli, G., & Pizzoli, M. (1992) · Macromolecules · doi:10.1021/ma00050a009 · Cited by 120 · see citing works
Jang, Y., Im, J. A., Choi, S. Y., Lee, J. I., & Lee, S. Y. (2014) · Metabolic Engineering · doi:10.1016/j.ymben.2014.03.004 · Cited by 100 · see citing works
Phosphotransbutyrylase from Clostridium acetobutylicum ATCC 824 and its role in acidogenesis
Wiesenborn, D. P., Rudolph, F. B., & Papoutsakis, E. T. (1989) · Applied and Environmental Microbiology · doi:10.1128/aem.55.2.317-322.1989 · Cited by 94 · see citing works
Ukpong, M. N., Atiyeh, H. K., Lorme, M. D., Liu, K., Zhu, X., Tanner, R. S., Wilkins, M. R., & Stevenson, B. S. (2012) · Biotechnology and Bioengineering · doi:10.1002/bit.24549 · Cited by 93 · see citing works
Tolonen, A. C., Chilaka, A. C., & Church, G. M. (2009) · Molecular Microbiology · doi:10.1111/j.1365-2958.2009.06890.x · Cited by 89 · see citing works
Jeon, J.-M., Brigham, C. J., Kim, Y., Kim, H., Yi, D.-H., Kim, H., Rha, C., Sinskey, A. J., & Yang, Y. (2014) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-014-5617-7 · Cited by 86 · see citing works
Kita, A., Iwasaki, Y., Sakai, S., Okuto, S., Takaoka, K., Suzuki, T., Yano, S., Sawayama, S., Tajima, T., Kato, J., et al. (2013) · Journal of Bioscience and Bioengineering · doi:10.1016/j.jbiosc.2012.10.013 · Cited by 75 · see citing works
Intestinal colonization: How key microbial players become established in this dynamic process
Aidy, S. E., den Abbeele, P. V., de Wiele, T. V., Louis, P., & Kleerebezem, M. (2013) · BioEssays · doi:10.1002/bies.201300073 · Cited by 72 · see citing works
Nariya, H., Miyata, S., Suzuki, M., Tamai, E., & Okabe, A. (2010) · Applied and Environmental Microbiology · doi:10.1128/aem.01572-10 · Cited by 61 · see citing works
New insights into the butyric acid metabolism of Clostridium acetobutylicum
Lehmann, D., Radomski, N., & Lütke‐Eversloh, T. (2012) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-012-4109-x · Cited by 60 · see citing works
Butyrate production from carbon monoxide byButyribacterium methylotrophicum
Worden, R. M., Grethlein, A. J., Zeikus, J. G., & Datta, R. (1989) · Applied Biochemistry and Biotechnology · doi:10.1007/bf02936517 · Cited by 59 · see citing works
Tan, Y., Liu, J., Chen, X., Zheng, H., & Li, F. (2013) · Molecular BioSystems · doi:10.1039/c3mb70232d · Cited by 56 · see citing works
Natural flavours production: a biotechnological approach
Armstrong, D. W., & Yamazaki, H. (1986) · Trends in biotechnology · doi:10.1016/0167-7799(86)90190-3 · Cited by 54 · see citing works
Effect of controlled substrate feeding on butyric acid production byClostridium tyrobutyricum
Fayolle, F., Marchal, R., & Ballerini, D. (1990) · Journal of Industrial Microbiology & Biotechnology · doi:10.1007/bf01577693 · Cited by 51 · see citing works
Metabolic engineering of Clostridium acetobutylicum for enhanced production of butyric acid
Jang, Y., Woo, H. M., Im, J. A., Kim, I. H., & Lee, S. Y. (2013) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-013-5161-x · Cited by 47 · see citing works
Baba, S.-I., Tashiro, Y., Shinto, H., & Sonomoto, K. (2011) · Journal of Biotechnology · doi:10.1016/j.jbiotec.2011.06.004 · Cited by 43 · see citing works
Sauer, B. (1987) · Molecular and Cellular Biology · doi:10.1128/mcb.7.6.2087-2096.1987 · Cited by 36 · see citing works
Vandák, D., Tomáška, M., Zigová, J., & Šturdı́k, E. (1995) · World Journal of Microbiology and Biotechnology · doi:10.1007/bf00367124 · Cited by 35 · see citing works
Liu, J., Tan, Y., Xiao-hong, Y., Chen, X., & Li, F. (2013) · Journal of Bioscience and Bioengineering · doi:10.1016/j.jbiosc.2013.04.011 · Cited by 33 · see citing works
Colby, G. D., & Chen, J. S. (1992) · Applied and Environmental Microbiology · doi:10.1128/aem.58.10.3297-3302.1992 · Cited by 29 · see citing works
Continuous cultivation of Clostridium thermobutyricum in a rotary fermentor system
Canganella, F., & Wiegel, J. (2000) · Journal of Industrial Microbiology & Biotechnology · doi:10.1038/sj.jim.2900752 · Cited by 26 · see citing works
Tan, Y., Liu, J., Liu, Z., & Li, F. (2013) · Journal of Basic Microbiology · doi:10.1002/jobm.201300046 · Cited by 22 · see citing works
Carboxymethylcellulose acetate butyrate in water-based automotive paints
Posey-Dowty, J. D., Seo, K., Walker, K., & Wilson, A. S. (2002) · Surface Coatings International Part B Coatings Transactions · doi:10.1007/bf02699510 · Cited by 18 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- [28]Playne MJ. 1985. Propionic and butyric acids, p 731– 759. In Moo-Young M (ed), Comprehensive biotechnology. Pergamon Press, Oxford, United Kingdom
Cited by
Sorted by citations
Singh, V., Lee, G., Son, H., Koh, H., Kim, E. S., Unno, T., & Shin, J. (2023) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.1103836 · Cited by 745 · see citing works
Industrial biomanufacturing: The future of chemical production
Clomburg, J. M., Crumbley, A. M., & González, R. (2017) · Science · doi:10.1126/science.aag0804 · Cited by 555 · see citing works
The ins and outs of microorganism–electrode electron transfer reactions
Kumar, A., Hsu, L. H.-H., Kavanagh, P., Barrière, F., Lens, P. N. L., Lapinsonnière, L., Lienhard, J. H., Schröder, U., Jiang, X., & Leech, D. (2017) · Nature Reviews Chemistry · doi:10.1038/s41570-017-0024 · Cited by 543 · see citing works
Liew, F., Martin, M. E., Tappel, R. C., Heijstra, B. D., Mihalcea, C., & Köpke, M. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.00694 · Cited by 485 · see citing works
Harnessing the power of microbial autotrophy
Claassens, N. J., Sousa, D. Z., dos Santos, V. A. P. M., de Vos, W. M., & John van der, O. O. S. T. (2016) · Nature Reviews Microbiology · doi:10.1038/nrmicro.2016.130 · Cited by 280 · see citing works
Bian, B., Bajracharya, S., Xu, J., Pant, D., & Saikaly, P. E. (2020) · Bioresource Technology · doi:10.1016/j.biortech.2020.122863 · Cited by 279 · see citing works
Bajracharya, S., Srikanth, S., Mohanakrishna, G., Zacharia, R., Strik, D. P. B. T. B., & Pant, D. (2017) · Journal of Power Sources · doi:10.1016/j.jpowsour.2017.04.024 · Cited by 247 · see citing works
C1-carbon sources for chemical and fuel production by microbial gas fermentation
Dürre, P., & Eikmanns, B. J. (2015) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2015.03.008 · Cited by 242 · see citing works
Insights into Butyrate Production in a Controlled Fermentation System via Gene Predictions
Esquivel‐Elizondo, S., Ilhan, Z. E., Garcia-Peña, E. I., & Krajmalnik‐Brown, R. (2017) · mSystems · doi:10.1128/msystems.00051-17 · Cited by 231 · see citing works
Huang, H., Chai, C., Li, N., Rowe, P., Minton, N. P., Yang, S., Jiang, W., & Gu, Y. (2016) · ACS Synthetic Biology · doi:10.1021/acssynbio.6b00044 · Cited by 200 · see citing works
CO2 fixation by anaerobic non-photosynthetic mixotrophy for improved carbon conversion
Jones, S. W., Fast, A. G., Carlson, E. D., Wiedel, C. A., Au, J., Antoniewicz, M. R., Papoutsakis, E. T., & Tracy, B. P. (2016) · Nature Communications · doi:10.1038/ncomms12800 · Cited by 192 · see citing works
Extracellular Electron Uptake: Among Autotrophs and Mediated by Surfaces
Tremblay, P., Angenent, L. T., & Zhang, T. (2016) · Trends in biotechnology · doi:10.1016/j.tibtech.2016.10.004 · Cited by 195 · see citing works
Pollution to products: recycling of ‘above ground’ carbon by gas fermentation
Köpke, M., & Simpson, S. D. (2020) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2020.02.017 · Cited by 196 · see citing works
Richter, H., Molitor, B., Diender, M., Sousa, D. Z., & Angenent, L. T. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.01773 · Cited by 193 · see citing works
Electrifying microbes for the production of chemicals
Tremblay, P., & Zhang, T. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2015.00201 · Cited by 191 · see citing works
Butyric acid: Applications and recent advances in its bioproduction
Jiang, L., Fu, H., Yang, H. K., Xu, W., Wang, J., & Yang, S. (2018) · Biotechnology Advances · doi:10.1016/j.biotechadv.2018.09.005 · Cited by 187 · see citing works
Carbon recovery by fermentation of CO-rich off gases – Turning steel mills into biorefineries
Molitor, B., Richter, H., Martin, M. E., Jensen, R. O., Juminaga, A., Mihalcea, C., & Angenent, L. T. (2016) · Bioresource Technology · doi:10.1016/j.biortech.2016.03.094 · Cited by 183 · see citing works
Fackler, N., Heijstra, B. D., Rasor, B. J., Brown, H., Martin, J. P., Ni, Z., Shebek, K. M., Rosin, R. R., Simpson, S. D., Tyo, K. E. J., et al. (2021) · Annual Review of Chemical and Biomolecular Engineering · doi:10.1146/annurev-chembioeng-120120-021122 · Cited by 169 · see citing works
Bacterial Anaerobic Synthesis Gas (Syngas) and CO 2 + H 2 Fermentation
Bengelsdorf, F. R., Beck, M. H., Erz, C., Hoffmeister, S., Karl, M. M., Riegler, P., Wirth, S., Poehlein, A., Weuster‐Botz, D., & Dürre, P. (2018) · Advances in applied microbiology · doi:10.1016/bs.aambs.2018.01.002 · Cited by 164 · see citing works
Simplifying microbial electrosynthesis reactor design
Giddings, C. G. S., Nevin, K. P., & Woodward, T. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2015.00468 · Cited by 146 · see citing works
Self-citationLuo, H., Yang, R., Zhao, Y., Wang, Z., Zheng, L., Huang, M., & Zeng, Q. (2018) · Bioresource Technology · doi:10.1016/j.biortech.2018.01.007 · Cited by 144 · see citing works
Chiranjeevi, P., & Patil, S. A. (2019) · Biotechnology Advances · doi:10.1016/j.biotechadv.2019.107468 · Cited by 139 · see citing works
Acetone production with metabolically engineered strains of Acetobacterium woodii
Hoffmeister, S., Gerdom, M., Bengelsdorf, F. R., Linder, S., Flüchter, S., Öztürk, H., Blümke, W., May, A., Fischer, R.-J., Bahl, H., et al. (2016) · Metabolic Engineering · doi:10.1016/j.ymben.2016.03.001 · Cited by 139 · see citing works
Abubackar, H. N., Veiga, M. C., & Kennes, C. (2015) · Bioresource Technology · doi:10.1016/j.biortech.2015.02.113 · Cited by 136 · see citing works
Baumann, I., & Westermann, P. (2016) · BioMed Research International · doi:10.1155/2016/8469357 · Cited by 122 · see citing works
Towards sustainable feedstocks: A guide to electron donors for microbial carbon fixation
Claassens, N. J., Sánchez‐Andrea, I., Sousa, D. Z., & Bar‐Even, A. (2018) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2018.01.019 · Cited by 120 · see citing works
Acetogenic mixotrophy: novel options for yield improvement in biofuels and biochemicals production
Fast, A. G., Schmidt, E. D., Jones, S. W., & Tracy, B. P. (2014) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2014.11.014 · Cited by 117 · see citing works
Zhang, S., Jiang, J., Wang, H., Li, F., Hua, T., & Wang, W. (2021) · Journal of CO2 Utilization · doi:10.1016/j.jcou.2021.101640 · Cited by 116 · see citing works
Li, F., Li, Y., Sun, L., Chen, X., An, X., Yin, C., Cao, Y., Wu, H. C., & Song, H. (2018) · ACS Synthetic Biology · doi:10.1021/acssynbio.7b00390 · Cited by 115 · see citing works
Industrial Acetogenic Biocatalysts: A Comparative Metabolic and Genomic Analysis
Bengelsdorf, F. R., Poehlein, A., Linder, S., Erz, C., Hummel, T., Hoffmeister, S., Daniel, R., & Dürre, P. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.01036 · Cited by 112 · see citing works
Shen, Y., Jarboe, L. R., Brown, R. C., & Wen, Z. (2015) · Biotechnology Advances · doi:10.1016/j.biotechadv.2015.10.006 · Cited by 110 · see citing works
Electro-stimulated microbial factory for value added product synthesis
Roy, S., Schievano, A., & Pant, D. (2016) · Bioresource Technology · doi:10.1016/j.biortech.2016.03.052 · Cited by 109 · see citing works
Rediverting carbon flux in Clostridium ljungdahlii using CRISPR interference (CRISPRi)
Woolston, B. M., Emerson, D. F., Currie, D. H., & Stephanopoulos, G. N. (2018) · Metabolic Engineering · doi:10.1016/j.ymben.2018.06.006 · Cited by 105 · see citing works
Advances in metabolic engineering in the microbial production of fuels and chemicals from C1 gas
Humphreys, C. M., & Minton, N. P. (2018) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2017.12.023 · Cited by 104 · see citing works
Mayer, F., Enzmann, F., Lopez, A. M., & Holtmann, D. (2019) · Bioresource Technology · doi:10.1016/j.biortech.2019.121706 · Cited by 104 · see citing works
Kong, F., Ren, H., Pavlostathis, S. G., Nan, J., Ren, N., & Wang, A. (2020) · Renewable and Sustainable Energy Reviews · doi:10.1016/j.rser.2020.109816 · Cited by 104 · see citing works
Kondaveeti, S., Abu-Reesh, I. M., Mohanakrishna, G., Bulut, M., & Pant, D. (2020) · Frontiers in Energy Research · doi:10.3389/fenrg.2020.00094 · Cited by 98 · see citing works
Das, S., Diels, L., Pant, D., Patil, S. A., & Ghangrekar, M. M. (2020) · Journal of The Electrochemical Society · doi:10.1149/1945-7111/abb836 · Cited by 97 · see citing works
Valorization of C1 gases to value-added chemicals using acetogenic biocatalysts
Bae, J., Song, Y., Lee, H., Shin, J., Jin, S., Kang, S., & Cho, B. (2021) · Chemical Engineering Journal · doi:10.1016/j.cej.2021.131325 · Cited by 93 · see citing works
Kracke, F., Lai, B., Yu, S., & Krömer, J. O. (2017) · Metabolic Engineering · doi:10.1016/j.ymben.2017.12.003 · Cited by 95 · see citing works
Metabolic engineering in chemolithoautotrophic hosts for the production of fuels and chemicals
Nybo, S. E., Khan, N. E., Woolston, B. M., & Curtis, W. R. (2015) · Metabolic Engineering · doi:10.1016/j.ymben.2015.04.008 · Cited by 94 · see citing works
Gas fermentation: cellular engineering possibilities and scale up
Heijstra, B. D., Leang, C., & Juminaga, A. (2017) · Microbial Cell Factories · doi:10.1186/s12934-017-0676-y · Cited by 92 · see citing works
Mohanakrishna, G., Vanbroekhoven, K., & Pant, D. (2018) · Reaction Chemistry & Engineering · doi:10.1039/c7re00220c · Cited by 92 · see citing works
Reversing an Extracellular Electron Transfer Pathway for Electrode-Driven Acetoin Reduction
Tefft, N. M., & TerAvest, M. A. (2019) · ACS Synthetic Biology · doi:10.1021/acssynbio.8b00498 · Cited by 87 · see citing works
Kremp, F., & Müller, V. (2020) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuaa040 · Cited by 83 · see citing works
Efficient production of lycopene from CO2 via microbial electrosynthesis
Wu, H., Pan, H., Li, Z., Liu, T., Liu, F., Xiu, S., Wang, J., Wang, H., Hou, Y., Yang, B., et al. (2021) · Chemical Engineering Journal · doi:10.1016/j.cej.2021.132943 · Cited by 85 · see citing works
Huang, H., Chai, C., Yang, S., Jiang, W., & Gu, Y. (2019) · Metabolic Engineering · doi:10.1016/j.ymben.2019.01.005 · Cited by 85 · see citing works
Philips, J., Rabaey, K., Lovley, D. R., & Vargas, M. (2017) · PLoS ONE · doi:10.1371/journal.pone.0170406 · Cited by 75 · see citing works
Self-citationSynthetic Biology on Acetogenic Bacteria for Highly Efficient Conversion of C1 Gases to Biochemicals
Jin, S., Bae, J., Song, Y., Pearcy, N., Shin, J., Kang, S., Minton, N. P., Soucaille, P., & Cho, B. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21207639 · Cited by 72 · see citing works
Luan, L., Ji, X., Guo, B., Cai, J., Dong, W., Huang, Y., & Zhang, S. (2023) · Biotechnology Advances · doi:10.1016/j.biotechadv.2023.108098 · Cited by 75 · see citing works
Genetic and metabolic engineering challenges of C1-gas fermenting acetogenic chassis organisms
Bourgade, B., Minton, N. P., & Islam, M. A. (2021) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuab008 · Cited by 66 · see citing works
Engineering Acetogenic Bacteria for Efficient One-Carbon Utilization
Lee, H., Bae, J., Jin, S., Kang, S., & Cho, B. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.865168 · Cited by 69 · see citing works
Modestra, J. A., Katakojwala, R., & Mohan, S. V. (2020) · Chemical Engineering Journal · doi:10.1016/j.cej.2020.124759 · Cited by 66 · see citing works
An insight into the bioelectrochemical photoreduction of CO2 to value-added chemicals
Gupta, P., Noori, M. T., Esteve‐Núñez, A., & Verma, N. (2021) · iScience · doi:10.1016/j.isci.2021.102294 · Cited by 64 · see citing works
A Targetron-Recombinase System for Large-Scale Genome Engineering of Clostridia
Cerisy, T., Rostain, W., Chhun, A., Boutard, M., Salanoubat, M., & Tolonen, A. C. (2019) · mSphere · doi:10.1128/msphere.00710-19 · Cited by 64 · see citing works
Expanding the molecular toolkit for the homoacetogen Clostridium ljungdahlii
Molitor, B., Kirchner, K., Henrich, A., Schmitz, S., & Rosenbaum, M. A. (2016) · Scientific Reports · doi:10.1038/srep31518 · Cited by 61 · see citing works
Zhang, L., Zhao, R., Jia, D., Jiang, W., & Gu, Y. (2020) · Current Opinion in Chemical Biology · doi:10.1016/j.cbpa.2020.04.010 · Cited by 61 · see citing works
Charubin, K., Modla, S., Caplan, J. L., & Papoutsakis, E. T. (2020) · mBio · doi:10.1128/mbio.02030-20 · Cited by 59 · see citing works
Lauer, I., Philipps, G., & Jennewein, S. (2022) · Microbial Cell Factories · doi:10.1186/s12934-022-01802-8 · Cited by 59 · see citing works
Jia, D., He, M., Yi, T., Shen, S., Zhu, X., Wang, Y., Zhuang, Y., Jiang, W., & Gu, Y. (2021) · ACS Synthetic Biology · doi:10.1021/acssynbio.1c00235 · Cited by 58 · see citing works
Guo, S., Asset, T., & Atanassov, P. B. (2021) · ACS Catalysis · doi:10.1021/acscatal.0c04862 · Cited by 58 · see citing works
Production of organics from CO2 by microbial electrosynthesis ( MES ) at high temperature
Faraghiparapari, N., & Zengler, K. (2016) · Journal of Chemical Technology & Biotechnology · doi:10.1002/jctb.5015 · Cited by 57 · see citing works
Gas Biological Conversions: The Potential of Syngas and Carbon Dioxide as Production Platforms
Gavala, H. N., Grimalt‐Alemany, A., Asimakopoulos, K., & Skiadas, I. V. (2021) · Waste and Biomass Valorization · doi:10.1007/s12649-020-01332-7 · Cited by 56 · see citing works
A genetic approach for microbial electrosynthesis system as biocommodities production platform
Shin, H. J., Jung, K. A., Nam, C. W., & Park, J. M. (2017) · Bioresource Technology · doi:10.1016/j.biortech.2017.05.077 · Cited by 54 · see citing works
Emerson, D. F., Woolston, B. M., Liu, N., Donnelly, M., Currie, D. H., & Stephanopoulos, G. N. (2018) · Biotechnology and Bioengineering · doi:10.1002/bit.26847 · Cited by 55 · see citing works
Exploiting the potential of gas fermentation
Redl, S., Diender, M., Jensen, T. Ø., Sousa, D. Z., & Nielsen, A. T. (2016) · Industrial Crops and Products · doi:10.1016/j.indcrop.2016.11.015 · Cited by 53 · see citing works
Metabolic engineering of clostridia for the production of chemicals
Cho, C., Jang, Y., Moon, H. G., Lee, J., & Lee, S. Y. (2014) · Biofuels Bioproducts and Biorefining · doi:10.1002/bbb.1531 · Cited by 52 · see citing works
Banerjee, I., Burrell, B., Reed, C., West, A. C., & Banta, S. A. (2017) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2017.03.009 · Cited by 52 · see citing works
Poehlein, A., Zeldes, B. M., Flaiz, M., Böer, T., Lüschen, A., Höfele, F., Baur, K. S., Molitor, B., Kröly, C., Wang, M., et al. (2024) · Bioresource Technology · doi:10.1016/j.biortech.2024.131913 · Cited by 51 · see citing works
Lehtinen, T., Efimova, E., Tremblay, P., Santala, S., Zhang, T., & Santala, V. P. (2017) · Bioresource Technology · doi:10.1016/j.biortech.2017.06.073 · Cited by 51 · see citing works
Metabolic regulation in solventogenic clostridia: regulators, mechanisms and engineering
Yang, Y., Nie, X., Jiang, Y., Yang, C., Gu, Y., & Jiang, W. (2018) · Biotechnology Advances · doi:10.1016/j.biotechadv.2018.02.012 · Cited by 51 · see citing works
Zou, L., Qiao, Y., & Li, C. M. (2018) · Electrochemical Energy Reviews · doi:10.1007/s41918-018-0020-1 · Cited by 51 · see citing works
Reprogramming Acetogenic Bacteria with CRISPR-Targeted Base Editing via Deamination
Xia, P., Casini, I., Schulz, S., Klask, C.-M., Angenent, L. T., & Molitor, B. (2020) · ACS Synthetic Biology · doi:10.1021/acssynbio.0c00226 · Cited by 48 · see citing works
Syngas Biorefinery and Syngas Utilization
Tissera, S. L. D., Köpke, M., Simpson, S. D., Humphreys, C. M., Minton, N. P., & Dürre, P. (2017) · Advances in biochemical engineering, biotechnology · doi:10.1007/10_2017_5 · Cited by 50 · see citing works
Guo, X., Fu, H., Feng, J., Hu, J., & Wang, J. (2020) · Bioresource Technology · doi:10.1016/j.biortech.2020.122764 · Cited by 50 · see citing works
Klask, C.-M., Kliem-Kuster, N., Molitor, B., & Angenent, L. T. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.00724 · Cited by 49 · see citing works
Metabolic response of Clostridium ljungdahlii to oxygen exposure
Whitham, J. M., Tirado-Acevedo, O., Chinn, M. S., Pawlak, J. J., & Grunden, A. M. (2015) · Applied and Environmental Microbiology · doi:10.1128/aem.02491-15 · Cited by 47 · see citing works
Lips, D., Schuurmans, J. M., dos Santos, F. B., & Hellingwerf, K. J. (2017) · Energy & Environmental Science · doi:10.1039/c7ee02212c · Cited by 47 · see citing works
Clostridia: a flexible microbial platform for the production of alcohols
Ren, C., Wen, Z., Xu, Y., Jiang, W., & Gu, Y. (2016) · Current Opinion in Chemical Biology · doi:10.1016/j.cbpa.2016.08.024 · Cited by 47 · see citing works
Kim, B. C., Baek, G., Kim, C., Lee, S. Y., Yang, E., Lee, S., Kim, T., Nam, J.-Y., Lee, C., Chae, K., et al. (2024) · ACS ES&T Engineering · doi:10.1021/acsestengg.4c00077 · Cited by 45 · see citing works
Loder, A. J., Han, Y., Hawkins, A. S., Lian, H., Lipscomb, G. L., Schut, G. J., Keller, M. W., Adams, M. W. W., & Kelly, R. M. (2016) · Metabolic Engineering · doi:10.1016/j.ymben.2016.10.009 · Cited by 44 · see citing works
Syngas and Methanol‐Based Biorefinery Concepts
Frazão, C. J. R., & Walther, T. (2020) · Chemie Ingenieur Technik · doi:10.1002/cite.202000108 · Cited by 44 · see citing works
In silico metabolic engineering of Clostridium ljungdahlii for synthesis gas fermentation
Chen, J., & Henson, M. A. (2016) · Metabolic Engineering · doi:10.1016/j.ymben.2016.10.002 · Cited by 43 · see citing works
Producing next-generation biofuels from filamentous cyanobacteria: An economic feasibility analysis
Johnson, T. J., Jahandideh, A., Johnson, M. D., Fields, K. H., Richardson, J. W., Muthukumarappan, K., Cao, Y., Gu, Z., Halfmann, C. T., Zhou, R., et al. (2016) · Algal Research · doi:10.1016/j.algal.2016.10.020 · Cited by 43 · see citing works
Yang, G., Jia, D., Jin, L., Jiang, Y., Wang, Y., Jiang, W., & Gu, Y. (2017) · ACS Synthetic Biology · doi:10.1021/acssynbio.7b00155 · Cited by 42 · see citing works
Igarashi, K., & Kato, S. (2017) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-017-8421-3 · Cited by 41 · see citing works
Xie, B., Liu, Z., Tian, L., Li, F., & Xiaohua, C. (2014) · Bioresource Technology · doi:10.1016/j.biortech.2014.11.101 · Cited by 40 · see citing works
The emerging role of aldehyde:ferredoxin oxidoreductases in microbially-catalyzed alcohol production
Nissen, L. S., & Basen, M. (2019) · Journal of Biotechnology · doi:10.1016/j.jbiotec.2019.09.005 · Cited by 40 · see citing works
Lee, J., Lee, J. W., Chae, C. G., Kwon, S. J., Kim, Y. J., Lee, J.-H., & Lee, H. S. (2019) · Biotechnology for Biofuels · doi:10.1186/s13068-019-1570-0 · Cited by 40 · see citing works
Charubin, K., Streett, H., & Papoutsakis, E. T. (2020) · Applied and Environmental Microbiology · doi:10.1128/aem.01271-20 · Cited by 40 · see citing works
Acetogen and acetogenesis for biological syngas valorization
Kim, J.-Y., Lee, M., Oh, S., Kang, B., Yasin, M., & Chang, I. S. (2023) · Bioresource Technology · doi:10.1016/j.biortech.2023.129368 · Cited by 40 · see citing works
Kim, K., Choe, D., Song, Y., Kang, M., Lee, S., Lee, D., & Cho, B. (2021) · Metabolic Engineering · doi:10.1016/j.ymben.2021.10.005 · Cited by 38 · see citing works
Johnson, T. J., Gibbons, J., Gu, L., Zhou, R., & Gibbons, W. R. (2016) · Biotechnology Progress · doi:10.1002/btpr.2358 · Cited by 38 · see citing works
Aklujkar, M., Leang, C., Shrestha, P. M., Shrestha, M., & Lovley, D. R. (2017) · Scientific Reports · doi:10.1038/s41598-017-12712-w · Cited by 39 · see citing works
Self-citationXiu, S., Yao, J., Wu, G., Huang, Y., Yang, B., Huang, Y., Lei, L., Li, Z., & Hou, Y. (2019) · Energy Technology · doi:10.1002/ente.201800987 · Cited by 40 · see citing works
Chen, G., Wang, R., Sun, M., Chen, J., Eheneden, I., & Zhao, J. (2023) · Chemosphere · doi:10.1016/j.chemosphere.2023.140251 · Cited by 38 · see citing works
Song, T., Guan, X., Wang, X., Qu, S., Zhang, S., Hui, W., Men, L., & Chen, X. (2021) · The FASEB Journal · doi:10.1096/fj.201903129rrr · Cited by 34 · see citing works
A fluorescent reporter system for anaerobic thermophiles
Hocq, R., Bottone, S., Gautier, A., & Pflügl, S. (2023) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2023.1226889 · Cited by 29 · see citing works
Biotransforming CO2 into valuable chemicals
Xia, Q. X., Yang, J., Hu, L., Zhao, H., & Lu, Y. (2023) · Journal of Cleaner Production · doi:10.1016/j.jclepro.2023.140185 · Cited by 31 · see citing works
Butler, C. S., & Lovley, D. R. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.01879 · Cited by 31 · see citing works
Self-citation
- Authors
- Ueki, T., Nevin, K. P., Woodard, T. L., & Lovley, D. R.
- Affiliations
- University of Massachusetts Amherst (US)
- Corresponding author
- Ueki, Toshiyuki
- Venue
- mBio
- Publisher
- American Society for Microbiology
- Published
- 2014-10-31
- Volume
- 5
- Issue
- 5
- Pages
- e01636-14
- ISSN
- 2150-7511 (ISSN-L)
- 2161-2129
- PMC
- PMC4212834
- OpenAlex
- W2106450419
- Cited by
- 175
- References
- 64
- Citations by year
- 2026: 5 · 2025: 11 · 2024: 15 · 2023: 14 · 2022: 10 · 2021: 24 · 2020: 17 · 2019: 11 · 2018: 13 · 2017: 20 · 2016: 22 · 2015: 10 · 2014: 3
- FWCI
- 7.52
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- mBio (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion, cc-by-nc-sa)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- U.S. Department of Energy (DEAR0000159)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial Metabolic Engineering and Bioproduction
- Physical Sciences › Environmental Science › Environmental Engineering › Microbial Fuel Cells and Bioremediation
- Physical Sciences › Engineering › Biomedical Engineering › Biofuel production and bioconversion
- Keywords
- Clostridium ljungdahlii, butyrate production, CO2 conversion, acetogenic bacteria, microbial electrosynthesis, metabolic engineering, ribosome binding site optimization, aldehyde/alcohol dehydrogenase, CoA transferase, acetate production
- MeSH terms
- Acetyl Coenzyme A, Butyrates, Carbon Dioxide, Clostridium, Recombinant Proteins, Metabolic Networks and Pathways, Metabolic Engineering, Metabolic Flux Analysis
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
