Redirecting Reductant Flux into Hydrogen Production via Metabolic Engineering of Fermentative Carbon Metabolism in a Cyanobacterium
Open accessAbstract
Some aquatic microbial oxygenic photoautotrophs (AMOPs) make hydrogen (H 2 ), a carbon-neutral, renewable product derived from water, in low yields during autofermentation (anaerobic metabolism) of intracellular carbohydrates previously stored during aerobic photosynthesis. We have constructed a mutant (the ldhA mutant) of the cyanobacterium Synechococcus sp. strain PCC 7002 lacking the enzyme for the NADH-dependent reduction of pyruvate to d -lactate, the major fermentative reductant sink in this AMOP. Both nuclear magnetic resonance (NMR) spectroscopy and liquid chromatography-mass spectrometry (LC-MS) metabolomic methods have shown that autofermentation by the ldhA mutant resulted in no d -lactate production and higher concentrations of excreted acetate, alanine, succinate, and hydrogen (up to 5-fold) compared to that by the wild type. The measured intracellular NAD(P)(H) concentrations demonstrated that the NAD(P)H/NAD(P) + ratio increased appreciably during autofermentation in the ldhA strain; we propose this to be the principal source of the observed increase in H 2 production via an NADH-dependent, bidirectional [NiFe] hydrogenase. Despite the elevated NAD(P)H/NAD(P) + ratio, no decrease was found in the rate of anaerobic conversion of stored carbohydrates. The measured energy conversion efficiency (ECE) from biomass (as glucose equivalents) converted to hydrogen in the ldhA mutant is 12%. Together with the unimpaired photoautotrophic growth of the ldhA mutant, these attributes reveal that metabolic engineering is an effective strategy to enhance H 2 production in AMOPs without compromising viability.
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Mutants of Synechococcus 7002 lacking lactate dehydrogenase resulted in a fivefold increment of total H2 production compared to wild type.
“The mutants of Synechococcus 7002 lacking lactate dehydrogenase have resulted in a fivefold increment of the total H2 production compared to the wild type (McNeely et al. 2010).”
From Renewable energy from Cyanobacteria: energy production optimization by metabolic pathway engineering (2011) · cites this paper as McNeely et al. 2010
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Cites
Hydrogen production by biological processes: a survey of literature
Das, D. (2001) · International Journal of Hydrogen Energy · doi:10.1016/s0360-3199(00)00058-6 · Cited by 2,097 · see citing works
Hwang, T., & Shaka, A. J. (1995) · Journal of Magnetic Resonance Series A · doi:10.1006/jmra.1995.1047 · Cited by 1,934 · see citing works
Aquatic phototrophs: efficient alternatives to land-based crops for biofuels
Dismukes, G. C., Carrieri, D., Bennette, N., Ananyev, G. M., & Posewitz, M. C. (2008) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2008.05.007 · Cited by 733 · see citing works
Self-citation[7] Chemical procedures for analysis of polysaccharides
Hassid, W. Z., & Abraham, S. (1957) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(57)03345-5 · Cited by 712 · see citing works
The fermentation pathways of Escherichia coli
Clark, D. P. (1989) · FEMS Microbiology Reviews · doi:10.1016/0168-6445(89)90033-8 · Cited by 506 · see citing works
Enhancement of hydrogen production by Enterobacter cloacae IIT-BT 08
Kumar, N., & Das, D. (2000) · Process Biochemistry · doi:10.1016/s0032-9592(99)00109-0 · Cited by 412 · see citing works
Rapid simultaneous lipid extraction and transesterification for fatty acid analyses
Rodríguez‐Ruiz, J., Belarbi, E., Sánchez, J. L. G., & Alonso, D. L. (1998) · Biotechnology Techniques · doi:10.1023/a:1008812904017 · Cited by 354 · see citing works
Plant genetic engineering to improve biomass characteristics for biofuels
Sticklen, M. B. (2006) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2006.05.003 · Cited by 313 · see citing works
Stal, L. (1997) · FEMS Microbiology Reviews · doi:10.1016/s0168-6445(97)00056-9 · Cited by 301 · see citing works
Enzymatic production of biohydrogen
Woodward, J., Orr, M. T., Cordray, K., & Greenbaum, E. (2000) · Nature · doi:10.1038/35016633 · Cited by 269 · see citing works
THE PRODUCTION OF HYDROGEN PEROXIDE BY BLUE‐GREEN ALGAE: A SURVEY 1
Stevens, S. E., Patterson, C. O. P., & Myers, J. E. (1973) · Journal of Phycology · doi:10.1111/j.1529-8817.1973.tb04116.x · Cited by 244 · see citing works
Chatterjee, R., Millard, C. S., Champion, K. M., Clark, D. P., & Donnelly, M. I. (2001) · Applied and Environmental Microbiology · doi:10.1128/aem.67.1.148-154.2001 · Cited by 217 · see citing works
Enhanced hydrogen production from glucose by metabolically engineered Escherichia coli
Maeda, T., Sánchez-Torres, V., & Wood, T. K. (2007) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-007-1217-0 · Cited by 196 · see citing works
Nakashimada, Y., Rachman, M. A., Kakizono, T., & Nishio, N. (2002) · International Journal of Hydrogen Energy · doi:10.1016/s0360-3199(02)00128-3 · Cited by 189 · see citing works
Enhanced hydrogen production in altered mixed acid fermentation of glucose by Enterobacter aerogenes
Rachman, M. A., Furutani, Y., Nakashimada, Y., Kakizono, T., & Nishio, N. (1997) · Journal of Fermentation and Bioengineering · doi:10.1016/s0922-338x(97)80142-0 · Cited by 172 · see citing works
Enhanced hydrogen production from glucose using ldh- and frd-inactivated Escherichiacoli strains
Yoshida, A., Nishimura, T., Kawaguchi, H., Inui, M., & Yukawa, H. (2006) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-006-0456-9 · Cited by 164 · see citing works
Becker, A., Schmidt, M., Jäger, W., & Pühler, A. (1995) · Gene · doi:10.1016/0378-1119(95)00313-u · Cited by 145 · see citing works
Ananyev, G., Carrieri, D., & Dismukes, G. C. (2008) · Applied and Environmental Microbiology · doi:10.1128/aem.01078-08 · Cited by 125 · see citing works
Self-citationGutthann, F., Egert, M., Marques, A., & Appel, J. (2006) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2006.12.003 · Cited by 124 · see citing works
The fermentation pathways of Escherichia coli
Clark, D. P. (1989) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.1989.tb03398.x · Cited by 123 · see citing works
Feasibility studies on the fermentative hydrogen production by recombinant Escherichia coli BL-21
Chittibabu, G., Nath, K., & Das, D. (2005) · Process Biochemistry · doi:10.1016/j.procbio.2005.08.020 · Cited by 122 · see citing works
Kengen, S. W. M., & Stams, A. J. M. (1994) · Archives of Microbiology · doi:10.1007/bf00276479 · Cited by 121 · see citing works
Modulation of Acetone-Butanol-Ethanol Fermentation by Carbon Monoxide and Organic Acids
Datta, R., & Zeikus, J. G. (1985) · Applied and Environmental Microbiology · doi:10.1128/aem.49.3.522-529.1985 · Cited by 119 · see citing works
Sakamoto, T., & Bryant, D. A. (1997) · Archives of Microbiology · doi:10.1007/s002030050535 · Cited by 100 · see citing works
Self-citationMultiple mechanisms controlling carbon metabolism in bacteria
Saier, M. H. (1998) · Biotechnology and Bioengineering · doi:10.1002/(sici)1097-0290(19980420)58:2/3 · Cited by 97 · see citing works
Redirection of biochemical pathways for the enhancement of H2 production by Enterobacter cloacae
Kumar, N., Ghosh, A., & Das, D. (2001) · Biotechnology Letters · doi:10.1023/a:1010334803961 · Cited by 95 · see citing works
Wang, X., Falcone, D. L., & Tabita, F. R. (1993) · Journal of Bacteriology · doi:10.1128/jb.175.11.3372-3379.1993 · Cited by 80 · see citing works
Occurrence of poly-beta-hydroxybutyrate in Spirulina species
VINCENZINI, M. T., Sili, C., Philippis, R. D., Ena, A., & Materassi, R. (1990) · Journal of Bacteriology · doi:10.1128/jb.172.5.2791-2792.1990 · Cited by 78 · see citing works
Yang, Y., San, K., & Bennett, G. N. (1999) · Metabolic Engineering · doi:10.1006/mben.1998.0111 · Cited by 73 · see citing works
Renewable hydrogen production by cyanobacteria: Nickel requirements for optimal hydrogenase activity
Carrieri, D., Ananyev, G., Costas, A. M. G., Bryant, D. A., & Dismukes, G. C. (2008) · International Journal of Hydrogen Energy · doi:10.1016/j.ijhydene.2008.02.022 · Cited by 63 · see citing works
Self-citationNomura, C. T., Persson, S., Shen, G., Inoue‐Sakamoto, K., & Bryant, D. A. (2006) · Photosynthesis Research · doi:10.1007/s11120-005-8533-y · Cited by 48 · see citing works
Self-citationSheremetieva, M. E., Troshina, O. Y., Serebryakova, L. T., & Lindblad, P. C. (2002) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2002.tb11352.x · Cited by 29 · see citing works
Carrieri, D., McNeely, K., Roo, A. C. D., Bennette, N. B., Pelczer, I., & Dismukes, G. C. (2009) · Magnetic Resonance in Chemistry · doi:10.1002/mrc.2420 · Cited by 28 · see citing works
Self-citationAlanine as an end product during fermentation of monosaccharides byClostridium strain P2
�rlygsson, J., Anderson, R. G. G., & Svensson, B. (1995) · Antonie van Leeuwenhoek · doi:10.1007/bf00874136 · Cited by 22 · see citing works
Sode, K., Watanabe, M., Makimoto, H., & Tomiyama, M. (1999) · Humana Press eBooks · doi:10.1007/978-1-4612-1604-9_29 · Cited by 20 · see citing works
Sode, K., Mika, W., Makimoto, H., & Tomiyama, M. (1999) · Applied Biochemistry and Biotechnology · doi:10.1385/abab:77:1-3:317 · Cited by 14 · see citing works
Flagged first, then by citations
1 of the 37 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Interfacing nature’s catalytic machinery with synthetic materials for semi-artificial photosynthesis
Kornienko, N., Zhang, J., Sakimoto, K. K., Yang, P., & Reisner, E. (2018) · Nature Nanotechnology · doi:10.1038/s41565-018-0251-7 · Cited by 531 · see citing works
Engineering cyanobacteria to generate high-value products
Ducat, D. C., Way, J. C., & Silver, P. A. (2011) · Trends in biotechnology · doi:10.1016/j.tibtech.2010.12.003 · Cited by 507 · see citing works
Photosynthetic semiconductor biohybrids for solar-driven biocatalysis
Cestellos-Blanco, S., Zhang, H., Kim, J. M., Shen, Y., & Yang, P. (2020) · Nature Catalysis · doi:10.1038/s41929-020-0428-y · Cited by 462 · see citing works
Yu, J., Liberton, M., Cliften, P. F., Head, R. D., Jacobs, J., Smith, R. D., Koppenaal, D., Brand, J. J., & Pakrasi, H. B. (2015) · Scientific Reports · doi:10.1038/srep08132 · Cited by 372 · see citing works
Renewable energy from Cyanobacteria: energy production optimization by metabolic pathway engineering
Quintana, N., Van der Kooy, F., Van de Rhee, M. D., Voshol, G. P., & Verpoorte, R. (2011) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-011-3394-0 · Cited by 338 · see citing works
Wendt, K. E., Ungerer, J., Cobb, R. E., Zhao, H., & Pakrasi, H. B. (2016) · Microbial Cell Factories · doi:10.1186/s12934-016-0514-7 · Cited by 232 · see citing works
Cyanobacteria: Promising biocatalysts for sustainable chemical production
Knoot, C. J., Ungerer, J., Wangikar, P. P., & Pakrasi, H. B. (2018) · Journal of Biological Chemistry · doi:10.1074/jbc.r117.815886 · Cited by 225 · see citing works
Application of synthetic biology in cyanobacteria and algae
Wang, B., Wang, J., Zhang, W., & Meldrum, D. R. (2012) · Frontiers in Microbiology · doi:10.3389/fmicb.2012.00344 · Cited by 211 · see citing works
Lau, N., Matsui, M., & Abdullah, A. A. (2015) · BioMed Research International · doi:10.1155/2015/754934 · Cited by 196 · see citing works
Metabolic engineering of microorganisms for biofuel production
Majidian, P., Tabatabaei, M., Zeinolabedini, M., Naghshbandi, M. P., & Yusuf Chisti, B. (2017) · Renewable and Sustainable Energy Reviews · doi:10.1016/j.rser.2017.10.085 · Cited by 191 · see citing works
Cofactor engineering for more efficient production of chemicals and biofuels
Wang, M., Chen, B., Fang, Y., & Tan, T. (2017) · Biotechnology Advances · doi:10.1016/j.biotechadv.2017.09.008 · Cited by 171 · see citing works
Development of Synechocystis sp. PCC 6803 as a Phototrophic Cell Factory
Yu, Y., You, L., Liu, D., Hollinshead, W. D., Tang, Y., & Zhang, F. (2013) · Marine Drugs · doi:10.3390/md11082894 · Cited by 154 · see citing works
Emerging Trends in Genetic Engineering of Microalgae for Commercial Applications
Grama, S. B., Liu, Z., & Li, J. (2022) · Marine Drugs · doi:10.3390/md20050285 · Cited by 157 · see citing works
Measuring Methane Production from Ruminants
Hill, J., McSweeney, C. S., Wright, A. G., Bishop-Hurley, G. J., & Kalantar‐Zadeh, K. (2015) · Trends in biotechnology · doi:10.1016/j.tibtech.2015.10.004 · Cited by 150 · see citing works
Zhou, J., Zhang, H., Zhang, Y., Li, Y., & Ma, Y. (2012) · Metabolic Engineering · doi:10.1016/j.ymben.2012.03.005 · Cited by 142 · see citing works
Wang, Y., Sun, T., Gao, X., Shi, M., Wu, L., Chen, L., & Zhang, W. (2015) · Metabolic Engineering · doi:10.1016/j.ymben.2015.10.008 · Cited by 139 · see citing works
Ludwig, M., & Bryant, D. A. (2011) · Frontiers in Microbiology · doi:10.3389/fmicb.2011.00041 · Cited by 136 · see citing works
Self-citationXu, Y., Guerra, T., Li, Z., Ludwig, M., Dismukes, G. C., & Bryant, D. A. (2012) · Metabolic Engineering · doi:10.1016/j.ymben.2012.12.002 · Cited by 131 · see citing works
Self-citationRewiring hydrogenase-dependent redox circuits in cyanobacteria
Ducat, D. C., Sachdeva, G., & Silver, P. A. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1016026108 · Cited by 130 · see citing works
Photoautotrophic production of D-lactic acid in an engineered cyanobacterium
Varman, A. M., Yu, Y., You, L., & Tang, Y. (2013) · Microbial Cell Factories · doi:10.1186/1475-2859-12-117 · Cited by 130 · see citing works
Engineering cyanobacteria as photosynthetic feedstock factories
Hays, S. G., & Ducat, D. C. (2014) · Photosynthesis Research · doi:10.1007/s11120-014-9980-0 · Cited by 122 · see citing works
Jaiswal, D., Sengupta, A., Sohoni, S. V., Sengupta, S., Phadnavis, A. G., Pakrasi, H. B., & Wangikar, P. P. (2018) · Scientific Reports · doi:10.1038/s41598-018-34872-z · Cited by 120 · see citing works
Technologies for Biofuel Production: Current Development, Challenges, and Future Prospects
Kour, D., Rana, K. L., Yadav, N., Yadav, A. N., Rastegari, A. A., Singh, C., Negi, P., Singh, K., & Saxena, A. K. (2019) · Biofuel and Biorefinery Technologies · doi:10.1007/978-3-030-14463-0_1 · Cited by 121 · see citing works
Agarwal, P., Soni, R., Kaur, P., Madan, A., Mishra, R., Pandey, J., Singh, S., & Singh, G. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.939347 · Cited by 118 · see citing works
The role of the bidirectional hydrogenase in cyanobacteria
Carrieri, D., Wawrousek, K., Eckert, C. A., Yu, J., & Maness, P. (2011) · Bioresource Technology · doi:10.1016/j.biortech.2011.03.103 · Cited by 112 · see citing works
Engineered cyanobacteria: Teaching an old bug new tricks
Ruffing, A. M. (2011) · Bioengineered Bugs · doi:10.4161/bbug.2.3.15285 · Cited by 107 · see citing works
Biofilm architecture: An emerging synthetic biology target
Kassinger, S. J., & van Hoek, M. L. (2020) · Synthetic and Systems Biotechnology · doi:10.1016/j.synbio.2020.01.001 · Cited by 102 · see citing works
Microalgal Hydrogen Production
Wang, Y., Yang, H., Zhang, X., Han, F., Tu, W., & Yang, W. (2020) · Small Methods · doi:10.1002/smtd.201900514 · Cited by 101 · see citing works
Work, V. H., D’Adamo, S., Radakovits, R., Jinkerson, R. E., & Posewitz, M. C. (2011) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2011.11.022 · Cited by 96 · see citing works
Microbial paths to renewable hydrogen production
Hallenbeck, P. C. (2011) · Biofuels · doi:10.4155/bfs.11.6 · Cited by 97 · see citing works
Aikawa, S., Nishida, A., Ho, S., Chang, J., Hasunuma, T., & Kondo, A. (2014) · Biotechnology for Biofuels · doi:10.1186/1754-6834-7-88 · Cited by 97 · see citing works
Metabolic engineering of cyanobacteria for the photosynthetic production of succinate
Lan, E. I., & Wei, C. T. (2016) · Metabolic Engineering · doi:10.1016/j.ymben.2016.10.014 · Cited by 94 · see citing works
An overview on progress, advances, and future outlook for biohydrogen production technology
Brar, K. K., Cortez, A. A., Pellegrini, V. O. A., Amulya, K., Polikarpov, I., Magdouli, S., Kumar, M., Yang, Y., Bhatia, S. K., & Brar, S. K. (2022) · International Journal of Hydrogen Energy · doi:10.1016/j.ijhydene.2022.01.156 · Cited by 93 · see citing works
Carrieri, D., Momot, D., Brasg, I. A., Ananyev, G., Lenz, O., Bryant, D. A., & Dismukes, G. C. (2010) · Applied and Environmental Microbiology · doi:10.1128/aem.00975-10 · Cited by 91 · see citing works
Self-citationPhotobiological hydrogen production: Bioenergetics and challenges for its practical application
Sakurai, H., Masukawa, H., Kitashima, M., & Inoue, K. (2013) · Journal of Photochemistry and Photobiology C Photochemistry Reviews · doi:10.1016/j.jphotochemrev.2013.05.001 · Cited by 91 · see citing works
Cyanobacteria as Chassis for Industrial Biotechnology: Progress and Prospects
Al‐Haj, L., Lui, Y. T., Abed, R. M. M., Gomaa, M., & Purton, S. (2016) · Life · doi:10.3390/life6040042 · Cited by 90 · see citing works
The fourth generation of biofuel
Moravvej, Z., Makarem, M. A., & Rahimpour, M. R. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-815162-4.00020-3 · Cited by 87 · see citing works
Cyanobacterial Hydrogenases and Hydrogen Metabolism Revisited: Recent Progress and Future Prospects
Khanna, N., & Lindblad, P. C. (2015) · International Journal of Molecular Sciences · doi:10.3390/ijms160510537 · Cited by 86 · see citing works
Proteomic analysis reveals resistance mechanism against biofuel hexane in Synechocystis sp. PCC 6803
Liu, J., Chen, L., Wang, J., Qiao, J., & Zhang, W. (2012) · Biotechnology for Biofuels · doi:10.1186/1754-6834-5-68 · Cited by 83 · see citing works
Bennette, N. B., Eng, J. F., & Dismukes, G. C. (2011) · Analytical Chemistry · doi:10.1021/ac200108a · Cited by 83 · see citing works
Self-citationBiological hydrogen with industrial potential: Improvement and prospection in biohydrogen production
Chen, W., Li, T., Ren, Y., Wang, J., Chen, H., & Wang, Q. (2022) · Journal of Cleaner Production · doi:10.1016/j.jclepro.2022.135777 · Cited by 83 · see citing works
Osanai, T., Shirai, T., Iijima, H., Nakaya, Y., Okamoto, M., Kondo, A., & Hirai, M. Y. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2015.01064 · Cited by 81 · see citing works
Hasunuma, T., Matsuda, M., Kato, Y., Vavricka, C. J., & Kondo, A. (2018) · Metabolic Engineering · doi:10.1016/j.ymben.2018.05.013 · Cited by 77 · see citing works
Recent Applications of Metabolomics Toward Cyanobacteria
Schwarz, D., Orf, I., Kopka, J., & Hagemann, M. (2013) · Metabolites · doi:10.3390/metabo3010072 · Cited by 80 · see citing works
Cyanobacterial nitrogenases: phylogenetic diversity, regulation and functional predictions
Esteves-Ferreira, A. A., Cavalcanti, J. H. F., Vaz, M. G. M. V., de Alvarenga, L. V., Nunes‐Nesi, A., & Araújo, W. L. (2017) · Genetics and Molecular Biology · doi:10.1590/1678-4685-gmb-2016-0050 · Cited by 80 · see citing works
An extended siderophore suite from Synechococcus sp. PCC 7002 revealed by LC-ICPMS-ESIMS
Boiteau, R. M., & Repeta, D. J. (2015) · Metallomics · doi:10.1039/c5mt00005j · Cited by 76 · see citing works
Hasunuma, T., Matsuda, M., & Kondo, A. (2016) · Metabolic Engineering Communications · doi:10.1016/j.meteno.2016.04.003 · Cited by 72 · see citing works
Hendry, J. I., Prasannan, C. B., Ma, F., Möllers, K. B., Jaiswal, D., Digmurti, M. G., Allen, D. K., Frigaard, N., Dasgupta, S., & Wangikar, P. P. (2017) · Biotechnology and Bioengineering · doi:10.1002/bit.26350 · Cited by 74 · see citing works
Vijayakumar, S., Rahman, P. K. S. M., & Angione, C. (2020) · iScience · doi:10.1016/j.isci.2020.101818 · Cited by 69 · see citing works
Potential of Hydrogen Production From Biomass
Singh, V., & Das, D. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-814251-6.00003-4 · Cited by 67 · see citing works
Computational evaluation of Synechococcus sp. PCC 7002 metabolism for chemical production
Vu, T. T., Hill, E. A., Kucek, L. A., Konopka, A. E., Beliaev, A. S., & Reed, J. L. (2013) · Biotechnology Journal · doi:10.1002/biot.201200315 · Cited by 67 · see citing works
Metabolomics-assisted synthetic biology
Ellis, D. I., & Goodacre, R. (2011) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2011.10.014 · Cited by 66 · see citing works
Baran, R., Ivanova, N., Jose, N., García‐Pichel, F., Kyrpides, N. C., Gugger, M. F., & Northen, T. R. (2013) · Marine Drugs · doi:10.3390/md11103617 · Cited by 61 · see citing works
Sarma, M. K., Kaushik, S., & Goswami, P. (2016) · Biomass and Bioenergy · doi:10.1016/j.biombioe.2016.03.043 · Cited by 60 · see citing works
Hydrogen Production by Cyanobacteria
Hallenbeck, P. C. (2011) · Springer eBooks · doi:10.1007/978-1-4614-1208-3_2 · Cited by 58 · see citing works
Metabolic and genetic engineering of cyanobacteria for enhanced hydrogen production
Khetkorn, W., Khanna, N., Incharoensakdi, A., & Lindblad, P. C. (2013) · Biofuels · doi:10.4155/bfs.13.41 · Cited by 57 · see citing works
Kumaraswamy, G. K., Guerra, T., Qian, X., Zhang, S., Bryant, D. A., & Dismukes, G. C. (2013) · Energy & Environmental Science · doi:10.1039/c3ee42206b · Cited by 56 · see citing works
Self-citationRecent advances and challenges of the use of cyanobacteria towards the production of biofuels
Singh, V., Chaudhary, D. K., Mani, I., & Dhar, P. K. (2016) · Renewable and Sustainable Energy Reviews · doi:10.1016/j.rser.2016.01.099 · Cited by 55 · see citing works
Renewable Hydrogen from Biomass: Technological Pathways and Economic Perspectives
Rey, J. R. C., Mateos-Pedrero, C., Longo, A., Rijo, B., Brito, P., Ferreira, P., & Nobre, C. (2024) · Energies · doi:10.3390/en17143530 · Cited by 53 · see citing works
Sarkar, D., & Shimizu, K. (2015) · Bioresources and Bioprocessing · doi:10.1186/s40643-015-0045-9 · Cited by 55 · see citing works
Kumar, A., & Singh, J. S. (2017) · Springer eBooks · doi:10.1007/978-3-319-49727-3_4 · Cited by 53 · see citing works
Skizim, N. J., Ananyev, G., Krishnan, A., & Dismukes, G. C. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.302125 · Cited by 50 · see citing works
Self-citationMony, C., Kaur, P., Rookes, J. E., Callahan, D. L., Eswaran, S. V., Yang, W. R., & Manna, P. K. (2022) · Environmental Science Nano · doi:10.1039/d2en00451h · Cited by 48 · see citing works
Guerra, T., Xu, Y., Bennette, N. B., McNeely, K., Bryant, D. A., & Dismukes, G. C. (2013) · Journal of Biotechnology · doi:10.1016/j.jbiotec.2013.04.005 · Cited by 47 · see citing works
Self-citationQian, X., Kim, M. K., Kumaraswamy, G. K., Agarwal, A., Lun, D. S., & Dismukes, G. C. (2016) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2016.12.007 · Cited by 46 · see citing works
Self-citationKamshybayeva, G. K., Kossalbayev, B. D., Sadvakasova, A. K., Kakimova, A. B., Bauenova, M. O., Zayadan, B. K., Lan, C.-W., Alwasel, S. H., Tomo, T., Chang, J., et al. (2023) · International Journal of Hydrogen Energy · doi:10.1016/j.ijhydene.2022.12.342 · Cited by 44 · see citing works
Hidese, R., Matsuda, M., Osanai, T., Hasunuma, T., & Kondo, A. (2020) · ACS Synthetic Biology · doi:10.1021/acssynbio.9b00281 · Cited by 43 · see citing works
Ueda, S., Kawamura, Y., Iijima, H., Nakajima, M., Shirai, T., Okamoto, M., Kondo, A., Hirai, M. Y., & Osanai, T. (2016) · Scientific Reports · doi:10.1038/srep32354 · Cited by 42 · see citing works
Cofactor engineering in cyanobacteria to overcome imbalance between NADPH and NADH: A mini review
Park, J., & Choi, Y. (2017) · Frontiers of Chemical Science and Engineering · doi:10.1007/s11705-016-1591-1 · Cited by 41 · see citing works
Therien, J., Zadvornyy, O. A., Posewitz, M. C., Bryant, D. A., & Peters, J. W. (2014) · Biotechnology for Biofuels · doi:10.1186/s13068-014-0154-2 · Cited by 41 · see citing works
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Self-citationIsolation of wild microalgae from natural water bodies for high hydrogen producing strains
He, M., Li, L., & Liu, J. (2011) · International Journal of Hydrogen Energy · doi:10.1016/j.ijhydene.2011.11.089 · Cited by 36 · see citing works
Production of Bioplastic Compounds by Genetically Manipulated and Metabolic Engineered Cyanobacteria
Katayama, N., Iijima, H., & Osanai, T. (2018) · Advances in experimental medicine and biology · doi:10.1007/978-981-13-0854-3_7 · Cited by 36 · see citing works
Khan, A. Z., Bilal, M., Mehmood, S., Sharma, A. K., & Iqbal, H. M. N. (2019) · Life · doi:10.3390/life9030054 · Cited by 36 · see citing works
Nanotechnology in Plant Nanobionics: Mechanisms, Applications, and Future Perspectives
Gautam, K., Singh, H., & Sinha, A. K. (2025) · Advanced Biology · doi:10.1002/adbi.202400589 · Cited by 35 · see citing works
Enhancement of bio-hydrogen generation by spirulina via an electrochemical photo-bioreactor (EPBR)
Hasnaoui, S., Pauss, A., Abdi, N., Grib, H., & Mameri, N. (2020) · International Journal of Hydrogen Energy · doi:10.1016/j.ijhydene.2019.12.144 · Cited by 35 · see citing works
Lai, M. J., Tsai, J. C., & Lan, E. I. (2022) · Bioresource Technology · doi:10.1016/j.biortech.2022.128131 · Cited by 35 · see citing works
Srimongkol, P., Thongchul, N., Phunpruch, S., & Karnchanatat, A. (2018) · Agricultural Water Management · doi:10.1016/j.agwat.2018.09.006 · Cited by 33 · see citing works
Enhancing biological hydrogen production from cyanobacteria by removal of excreted products
Ananyev, G., Skizim, N. J., & Dismukes, G. C. (2012) · Journal of Biotechnology · doi:10.1016/j.jbiotec.2012.03.026 · Cited by 33 · see citing works
Self-citationIijima, H., Watanabe, A., Sukigara, H., Iwazumi, K., Shirai, T., Kondo, A., & Osanai, T. (2021) · Metabolic Engineering · doi:10.1016/j.ymben.2021.03.007 · Cited by 32 · see citing works
Taikhao, S., Incharoensakdi, A., & Phunpruch, S. (2014) · Journal of Applied Phycology · doi:10.1007/s10811-014-0292-8 · Cited by 31 · see citing works
Chin, T., Okuda, Y., & Ikeuchi, M. (2018) · Journal of Biotechnology · doi:10.1016/j.jbiotec.2018.04.004 · Cited by 30 · see citing works
Pinto, F., van Elburg, K. A., Pacheco, C. C., Lopo, M., Noirel, J., Montagud, A., Urchueguía, J. F., Wright, P. C., & Tamagnini, P. (2011) · Microbiology · doi:10.1099/mic.0.052282-0 · Cited by 30 · see citing works
Lauric Acid Production in a Glycogen-Less Strain of Synechococcus sp. PCC 7002
Work, V. H., Melnicki, M. R., Hill, E. A., Davies, F. K., Kucek, L. A., Beliaev, A. S., & Posewitz, M. C. (2015) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2015.00048 · Cited by 29 · see citing works
Yusuf Chisti, B. (2019) · Elsevier eBooks · doi:10.1016/b978-0-444-64192-2.00001-9 · Cited by 27 · see citing works
Burrows, E. H., Chaplen, F. W. R., & Ely, R. L. (2010) · Bioresource Technology · doi:10.1016/j.biortech.2010.10.042 · Cited by 27 · see citing works
Maximizing reductant flow into microbial H2 production
Kontur, W. S., Noguera, D. R., & Donohue, T. J. (2011) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2011.10.003 · Cited by 26 · see citing works
Vargas, S. R., Zaiat, M., & Calijuri, M. D. C. (2020) · International Journal of Hydrogen Energy · doi:10.1016/j.ijhydene.2020.08.072 · Cited by 25 · see citing works
Sigma Factor Modulation for Cyanobacterial Metabolic Engineering
Srivastava, A., Varshney, R. K., & Shukla, P. (2020) · Trends in Microbiology · doi:10.1016/j.tim.2020.10.012 · Cited by 25 · see citing works
Andrews, F., Faulkner, M., Toogood, H. S., & Scrutton, N. S. (2021) · Biotechnology for Biofuels · doi:10.1186/s13068-021-02091-w · Cited by 23 · see citing works
Metabolic transformation of cyanobacteria for biofuel production
Velmurugan, R., & Incharoensakdi, A. (2022) · Chemosphere · doi:10.1016/j.chemosphere.2022.134342 · Cited by 23 · see citing works
Shirai, T., Osanai, T., & Kondo, A. (2016) · Microbial Cell Factories · doi:10.1186/s12934-016-0416-8 · Cited by 22 · see citing works
Advances in Utilizing Cyanobacteria for Hydrogen Production
Kufryk, G. I. (2013) · Advances in Microbiology · doi:10.4236/aim.2013.36a008 · Cited by 22 · see citing works
Angermayr, S. A., van der Woude, A. D., Correddu, D., Kern, R., Hagemann, M., & Hellingwerf, K. J. (2015) · Applied and Environmental Microbiology · doi:10.1128/aem.03379-15 · Cited by 22 · see citing works
Distribution of Hydrogenases in Cyanobacteria: A Phylum-Wide Genomic Survey
Puggioni, V., Tempel, S., & Latifi, A. (2016) · Frontiers in Genetics · doi:10.3389/fgene.2016.00223 · Cited by 22 · see citing works
do Amaral, S. C., Santos, A. V., Schneider, M. P. C., da Silva, J. K. R., & Xavier, L. P. (2020) · Molecules · doi:10.3390/molecules25204744 · Cited by 21 · see citing works
Krishnan, A., Qian, X., Ananyev, G., Lun, D. S., & Dismukes, G. C. (2018) · Advances in Experimental Medicine and Biology · doi:10.1007/978-981-13-0854-3_8 · Cited by 20 · see citing works
Self-citationProduction of Clean Energy from Cyanobacterial Biochemical Products
Hossain, M. F. (2016) · Strategic Planning for Energy and the Environment · doi:10.1080/10485236.2017.11810168 · Cited by 20 · see citing works
Gu, H., Jinkerson, R. E., Davies, F. K., Sisson, L. A., Schneider, P. E., & Posewitz, M. C. (2016) · Frontiers in Plant Science · doi:10.3389/fpls.2016.00690 · Cited by 19 · see citing works
Qiao, L., Chang, Z., Li, J., Chen, Z., Yang, L., & Luo, Q. (2019) · Aquaculture Research · doi:10.1111/are.14213 · Cited by 18 · see citing works
- Authors
- McNeely, K., Xu, Y., Bennette, N., Bryant, D. A., & Dismukes, G. C.
- Affiliations
- Rutgers, The State University of New Jersey (US)
- Pennsylvania State University (US)
- Venue
- Applied and Environmental Microbiology
- Publisher
- American Society for Microbiology
- Published
- 2010-08
- Volume
- 76
- Issue
- 15
- Pages
- 5032-5038
- ISSN
- 0099-2240 (ISSN-L)
- 1098-5336
- PMC
- PMC2916493
- OpenAlex
- W2114089350
- Cited by
- 168
- References
- 37
- Citations by year
- 2026: 7 · 2025: 10 · 2024: 5 · 2023: 7 · 2022: 15 · 2021: 3 · 2020: 12 · 2019: 6 · 2018: 9 · 2017: 8 · 2016: 20 · 2015: 13 · 2014: 10 · 2013: 16 · 2012: 7
- FWCI
- 5.60
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Applied and Environmental Microbiology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Multidisciplinary University Research Initiative (FA9550-05-1-0365)
- Air Force Office of Scientific Research (FA9550-, FA-9550-05-1-0365)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial Metabolic Engineering and Bioproduction
- Physical Sciences › Energy › Renewable Energy, Sustainability and the Environment › Algal biology and biofuel production
- Physical Sciences › Energy › Renewable Energy, Sustainability and the Environment › Metalloenzymes and iron-sulfur proteins
- Keywords
- hydrogen production, cyanobacteria, Synechococcus sp. PCC 7002, metabolic engineering, D-lactate, NADH, [NiFe] hydrogenase, acetate, energy conversion efficiency, photoautotrophic growth, fermentative metabolism
- MeSH terms
- Acetates, Alanine, Bacterial Proteins, Carbohydrate Dehydrogenases, Carbon, Chromatography, Liquid, Genetic Engineering, Hydrogen, Magnetic Resonance Spectroscopy, Oxidation-Reduction, Mass Spectrometry, Pyruvic Acid, Lactic Acid, Succinic Acid, Synechococcus, Metabolic Networks and Pathways, Metabolome
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