Photosynthetic production of the nitrogen-rich compound guanidine

Wang, Bo; Dong, Tao; Myrlie, Aldon; Gu, Liping; Zhu, Huilan; Xiong, Wei; Maness, PinChing; Zhou, Ruanbao; Yu, Jianping

doi:10.1039/C9GC01003C

Title: Photosynthetic production of the nitrogen-rich compound guanidine

Journal Article · Tue Jun 04 00:00:00 EDT 2019 · Green Chemistry

DOI:https://doi.org/10.1039/C9GC01003C· OSTI ID:1528658

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^[1]; Myrlie, Aldon ^[2]; Gu, Liping ^[2]; Zhu, Huilan ^[2];

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Biosciences Center, National Renewable Energy Laboratory, Golden, USA
Department of Biology & Microbiology, South Dakota State University, Brookings, USA

The development of an sustainable economy calls for improved energy utilization and storage technologies. Although battery- and carbon-based routes have gained tremendous attention, nitrogen-based routes have rarely been exploited so far. Guanidine (CH₅N₃) which contains 71.1% nitrogen by mass is an exemplary chemical to explore the nitrogen-based routes of energy utilization and storage. Guanidine has a variety of applications including its use as a slow-release fertilizer, a propellant, or as a precursor to pharmaceuticals and antimicrobial polymers. The conventional chemical synthesis of guanidine through the Frank–Caro process is energy-intensive, consumes fossil fuels, and is detrimental to the environment. Herein, a de novo guanidine biosynthesis (GUB) cycle is proposed with CO₂ and nitrate/ammonium as the carbon and nitrogen sources, respectively. The ATP and NAD(P)H needed to drive the GUB cycle are generated via photosynthesis in an engineered cyanobacterium Synechocystis sp. PCC 6803 expressing an ethylene-forming enzyme (EFE). Up to 586.5 mg L^-1 (9.9 mM) guanidine was produced after seven days of photoautotrophic cultivation, with an average productivity of 83.8 mg L^-1 day^-1. In addition, guanidine was directly biosynthesized from CO₂, N₂ and H₂O in an engineered N₂-fixing cyanobacterium Anabaena sp. PCC 7120 expressing the EFE. This work demonstrates the first biological conversion of renewable solar energy into chemical energy stored in the nitrogen-rich compound guanidine, which could shed light on harnessing the biological nitrogen metabolism for energy utilization and storage.

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Research Organization:: National Renewable Energy Lab. (NREL), Golden, CO (United States)

Sponsoring Organization:: USDOE Office of Energy Efficiency and Renewable Energy (EERE)

Grant/Contract Number:: AC36-08GO28308

OSTI ID:: 1528658

Alternate ID(s):: OSTI ID: 1513042; OSTI ID: 1515762

Report Number(s):: NREL/JA-2700-73223; GRCHFJ

Journal Information:: Green Chemistry, Journal Name: Green Chemistry Vol. 21 Journal Issue: 11; ISSN 1463-9262

Publisher:: Royal Society of Chemistry (RSC)Copyright Statement

Country of Publication:: United Kingdom

Language:: English

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Cited by: 12 works

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References (36)

Metabolism of Free Guanidine in Bacteria Is Regulated by a Widespread Riboswitch Class Nelson, James W.; Atilho, Ruben M.; Sherlock, Madeline E. Molecular Cell, Vol. 65, Issue 2 https://doi.org/10.1016/j.molcel.2016.11.019	journal	January 2017
Outdoor cultivation of a nitrogen-fixing marine cyanobacterium, Anabaena sp. ATCC 33047 Moreno, J. Biomolecular Engineering, Vol. 20, Issue 4-6 https://doi.org/10.1016/S1389-0344(03)00051-0	journal	July 2003
A simple approach to constructing antibacterial and anti-biofouling nanofibrous membranes Mei, Yan; Yao, Chen; Li, Xinsong Biofouling, Vol. 30, Issue 3 https://doi.org/10.1080/08927014.2013.871540	journal	January 2014
Ammonia Triggers Photodamage of Photosystem II in the Cyanobacterium Synechocystis sp. Strain PCC 6803 Drath, Miriam; Kloft, Nicole; Batschauer, Alfred Plant Physiology, Vol. 147, Issue 1 https://doi.org/10.1104/pp.108.117218	journal	March 2008
Biodegradation of guanidinium ion in aerobic soil samples Mitchell, Wayne R. Bulletin of Environmental Contamination and Toxicology, Vol. 39, Issue 6 https://doi.org/10.1007/BF01689587	journal	December 1987
The cyanobacterial ornithine–ammonia cycle involves an arginine dihydrolase Zhang, Hao; Liu, Yujie; Nie, Xiaoqun Nature Chemical Biology, Vol. 14, Issue 6 https://doi.org/10.1038/s41589-018-0038-z	journal	April 2018
Analysis of guanidine in high salt and protein matrices by cation-exchange chromatography and UV detection Qiu, Jinshu; Lee, Hans; Zhou, Chengfeng Journal of Chromatography A, Vol. 1073, Issue 1-2 https://doi.org/10.1016/j.chroma.2004.10.045	journal	May 2005
Ethylene Synthesis and Regulated Expression of Recombinant Protein in Synechocystis sp. PCC 6803 Guerrero, Fernando; Carbonell, Verónica; Cossu, Matteo PLoS ONE, Vol. 7, Issue 11 https://doi.org/10.1371/journal.pone.0050470	journal	November 2012
The nitrogen economy: Economic feasibility analysis of nitrogen-based fuels as energy carriers Elishav, Oren; Lewin, Daniel R.; Shter, Gennady E. Applied Energy, Vol. 185 https://doi.org/10.1016/j.apenergy.2016.10.088	journal	January 2017
Water-resistant cellulosic filter containing non-leaching antimicrobial starch for water purification and disinfection Heydarifard, Solmaz; Pan, Yuanfeng; Xiao, Huining Carbohydrate Polymers, Vol. 163 https://doi.org/10.1016/j.carbpol.2017.01.063	journal	May 2017
Guanidinium export is the primal function of SMR family transporters Kermani, Ali A.; Macdonald, Christian B.; Gundepudi, Roja Proceedings of the National Academy of Sciences, Vol. 115, Issue 12 https://doi.org/10.1073/pnas.1719187115	journal	March 2018
A quantitative evaluation of ethylene production in the recombinant cyanobacterium Synechocystis sp. PCC 6803 harboring the ethylene-forming enzyme by membrane inlet mass spectrometry Zavřel, Tomáš; Knoop, Henning; Steuer, Ralf Bioresource Technology, Vol. 202 https://doi.org/10.1016/j.biortech.2015.11.062	journal	February 2016
A Genetic Toolbox for Modulating the Expression of Heterologous Genes in the Cyanobacterium Synechocystis sp. PCC 6803 Wang, Bo; Eckert, Carrie; Maness, Pin-Ching ACS Synthetic Biology, Vol. 7, Issue 1 https://doi.org/10.1021/acssynbio.7b00297	journal	August 2017
Effects of global transcription factor NtcA on photosynthetic production of ethylene in recombinant Synechocystis sp. PCC 6803 Mo, Huilin; Xie, Xiaoman; Zhu, Tao Biotechnology for Biofuels, Vol. 10, Issue 1 https://doi.org/10.1186/s13068-017-0832-y	journal	June 2017
Life cycle energy and greenhouse gas profile of a process for the production of ammonium sulfate from nitrogen-fixing photosynthetic cyanobacteria Razon, Luis F. Bioresource Technology, Vol. 107 https://doi.org/10.1016/j.biortech.2011.12.075	journal	March 2012
Engineering cyanobacteria for photosynthetic production of 3-hydroxybutyrate directly from CO2 Wang, Bo; Pugh, Shawn; Nielsen, David R. Metabolic Engineering, Vol. 16 https://doi.org/10.1016/j.ymben.2013.01.001	journal	March 2013
Ammonium assimilation in cyanobacteria Muro-Pastor, M. Isabel; Reyes, Jose C.; Florencio, Francisco J. Photosynthesis Research, Vol. 83, Issue 2 https://doi.org/10.1007/s11120-004-2082-7	journal	February 2005
The plasticity of cyanobacterial metabolism supports direct CO2 conversion to ethylene Xiong, Wei; Morgan, John A.; Ungerer, Justin Nature Plants, Vol. 1, Issue 5 https://doi.org/10.1038/nplants.2015.53	journal	April 2015
Sustained photosynthetic conversion of CO₂ to ethylene in recombinant cyanobacterium Synechocystis 6803 Ungerer, Justin; Tao, Ling; Davis, Mark Energy & Environmental Science, Vol. 5, Issue 10, p. 8998-9006 https://doi.org/10.1039/c2ee22555g	journal	January 2012
Ethylene production with engineered Synechocystis sp PCC 6803 strains Veetil, Vinod Puthan; Angermayr, S. Andreas; Hellingwerf, Klaas J. Microbial Cell Factories, Vol. 16, Issue 1 https://doi.org/10.1186/s12934-017-0645-5	journal	February 2017
Unlocking the photobiological conversion of CO ₂ to ( R )-3-hydroxybutyrate in cyanobacteria Wang, Bo; Xiong, Wei; Yu, Jianping Green Chemistry, Vol. 20, Issue 16 https://doi.org/10.1039/C8GC01208C	journal	January 2018
The chemistry and biology of guanidine natural products Berlinck, Roberto G. S.; Bertonha, Ariane F.; Takaki, Mirelle Natural Product Reports, Vol. 34, Issue 11 https://doi.org/10.1039/C7NP00037E	journal	January 2017
Two reactions are simultaneously catalyzed by a single enzyme: The arginine-dependent simultaneous formation of two products, ethylene and succinate, from 2-oxoglutarate by an enzyme from Pseudomonas syringae Fukuda, Hideo; Ogawa, Takahira; Tazaki, Masato Biochemical and Biophysical Research Communications, Vol. 188, Issue 2 https://doi.org/10.1016/0006-291X(92)91081-Z	journal	October 1992
Structural and stereoelectronic insights into oxygenase-catalyzed formation of ethylene from 2-oxoglutarate Zhang, Zhihong; Smart, Tristan J.; Choi, Hwanho Proceedings of the National Academy of Sciences, Vol. 114, Issue 18 https://doi.org/10.1073/pnas.1617760114	journal	April 2017
Ballistic properties and burning behaviour of an ammonium perchlorate/guanidine nitrate/sodium nitrate airbag solid propellant Ulas, A.; Risha, G. A.; Kuo, K. K. Fuel, Vol. 85, Issue 14-15 https://doi.org/10.1016/j.fuel.2006.03.026	journal	October 2006
Photosynthetic nitrate assimilation in cyanobacteria Flores, Enrique; Frías, José E.; Rubio, Luis M. Photosynthesis Research, Vol. 83, Issue 2 https://doi.org/10.1007/s11120-004-5830-9	journal	February 2005
Metabolic engineering of microorganisms for the production of L-arginine and its derivatives Shin, Jae Ho; Lee, Sang Yup Microbial Cell Factories, Vol. 13, Issue 1 https://doi.org/10.1186/s12934-014-0166-4	journal	December 2014
Engineering cyanobacteria for the production of a cyclic hydrocarbon fuel from CO ₂ and H ₂ O Halfmann, Charles; Gu, Liping; Zhou, Ruanbao Green Chem., Vol. 16, Issue 6 https://doi.org/10.1039/C3GC42591F	journal	January 2014
Promising silicones modified with cationic biocides for the development of antimicrobial medical devices Ghamrawi, Sarah; Bouchara, Jean-Philippe; Tarasyuk, Oksana Materials Science and Engineering: C, Vol. 75 https://doi.org/10.1016/j.msec.2017.03.013	journal	June 2017
Ammonia and hydrogen production by immobilized cyanobacteria Brouers, Michel; Hall, David O. Journal of Biotechnology, Vol. 3, Issue 5-6 https://doi.org/10.1016/0168-1656(86)90012-X	journal	April 1986
Guanidine sulphate: Slow release of mineral nitrogen during incubation in soil Zhang, Z.; Nyborg, M.; Worsley, M. Communications in Soil Science and Plant Analysis, Vol. 23, Issue 5-6 https://doi.org/10.1080/00103629209368601	journal	March 1992
Synergistic effects of guanidine-grafted CMC on enhancing antimicrobial activity and dry strength of paper Liu, Kai; Xu, Yaoguang; Lin, Xinxing Carbohydrate Polymers, Vol. 110 https://doi.org/10.1016/j.carbpol.2014.03.086	journal	September 2014
Structures and Mechanisms of the Non-Heme Fe(II)- and 2-Oxoglutarate-Dependent Ethylene-Forming Enzyme: Substrate Binding Creates a Twist Martinez, Salette; Fellner, Matthias; Herr, Caitlyn Q. Journal of the American Chemical Society, Vol. 139, Issue 34 https://doi.org/10.1021/jacs.7b06186	journal	August 2017
Ethylene-forming enzyme and bioethylene production Eckert, Carrie; Xu, Wu; Xiong, Wei Biotechnology for Biofuels, Vol. 7, Issue 1 https://doi.org/10.1186/1754-6834-7-33	journal	January 2014
Sequence Analysis of the Genome of the Unicellular Cyanobacterium Synechocystis sp. Strain PCC6803. II. Sequence Determination of the Entire Genome and Assignment of Potential Protein-coding Regions Kaneko, T.; Sato, S.; Kotani, H. DNA Research, Vol. 3, Issue 3 https://doi.org/10.1093/dnares/3.3.109	journal	January 1996
The Biology of Free Guanidine As Revealed by Riboswitches Breaker, Ronald R.; Atilho, Ruben M.; Malkowski, Sarah N. Biochemistry, Vol. 56, Issue 2 https://doi.org/10.1021/acs.biochem.6b01269	journal	January 2017

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Monomer sequence design at two solvent interface enables the synthesis of highly photoactive carbon nitride Dolai, Susmita; Karjule, Neeta; Azoulay, Adi RSC Advances, Vol. 9, Issue 45 https://doi.org/10.1039/c9ra05264j	journal	January 2019
Increased ethylene production by overexpressing phosphoenolpyruvate carboxylase in the cyanobacterium Synechocystis PCC 6803 Durall, Claudia; Lindberg, Pia; Yu, Jianping Biotechnology for Biofuels, Vol. 13, Issue 1 https://doi.org/10.1186/s13068-020-1653-y	journal	January 2020

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37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
guanidine
cyanobacterium
nitrogen fixation
synechocystis
Anabaena

Title: Photosynthetic production of the nitrogen-rich compound guanidine

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