Abstract
To reduce dependence on fossil fuels and curb greenhouse effect, cyanobacteria have emerged as an important chassis candidate for producing biofuels and chemicals due to their capability to directly utilize sunlight and CO2 as the sole energy and carbon sources, respectively. Recent progresses in developing and applying various synthetic biology tools have led to the successful constructions of novel pathways of several dozen green fuels and chemicals utilizing cyanobacterial chassis. Meanwhile, it is increasingly recognized that in order to enhance productivity of the synthetic cyanobacterial systems, optimizing and engineering more robust and high-efficient cyanobacterial chassis should not be omitted. In recent years, numerous research studies have been conducted to enhance production of green fuels and chemicals through cyanobacterial chassis modifications involving photosynthesis, CO2 uptake and fixation, products exporting, tolerance, and cellular regulation. In this article, we critically reviewed recent progresses and universal strategies in cyanobacterial chassis engineering to make it more robust and effective for bio-chemicals production.
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Akiyama H, Okuhata H, Onizuka T, Kanai S, Hirano M, Tanaka S, Sasaki K, Miyasaka H (2011) Antibiotics-free stable polyhydroxyalkanoate (PHA) production from carbon dioxide by recombinant cyanobacteria. Bioresour Technol 102:11039–11042. doi:10.1016/j.biortech.2011.09.058
Anfelt J, Hallstrom B, Nielsen J, Uhlen M, Hudson EP (2013) Using transcriptomics to improve butanol tolerance of Synechocystis sp. strain PCC 6803. Appl Environ Microbiol 79:7419–7427. doi:10.1128/AEM.02694-13
Anfelt J, Kaczmarzyk D, Shabestary K, Renberg B, Rockberg J, Nielsen J, Uhlén M, Hudson EP (2015) Genetic and nutrient modulation of acetyl-CoA levels in Synechocystis for n-butanol production. Microb Cell Factories 14(1):167. doi:10.1186/s12934-015-0355-9
Angermayr SA, Paszota M, Hellingwerf KJ (2012) Engineering a cyanobacterial cell factory for production of lactic acid. Appl Environ Microbiol 78(19):7098–7106. doi:10.1128/AEM.01587-12
Atsumi S, Higashide W, Liao JC (2009) Direct photosynthetic recycling of carbon dioxide to isobutyraldehyde. Nat Biotechnol 27:1177–1180. doi:10.1038/nbt.1586
Badger MR, Price GD (2003) CO2 concentrating mechanisms in cyanobacteria: molecular components, their diversity and evolution. J Exp Bot 54:609–622. doi:10.1093/jxb/erg076
Bashor CJ, Horwitz AA, Peisajovich SG, Lim WA (2010) Rewiring cells: synthetic biology as a tool to interrogate the organizational principles of living systems. Annu Rev Biophys 39:515–537. doi:10.1146/annurev.biophys.050708.133652
Bentley FK, Zurbriggen A, Melis A (2014) Heterologous expression of the mevalonic acid pathway in cyanobacteria enhances endogenous carbon partitioning to isoprene. Molecular Plant 7:71–86. doi:10.1093/mp/sst134
Berla BM, Saha R, Immethun CM, Maranas CD, Moon TS, Pakrasi HB (2013) Synthetic biology of cyanobacteria: unique challenges and opportunities. Front Microbiol 4:246. doi:10.3389/fmicb.2013.00246
Blankenship RE, Tiede DM, Barber J, Brudvig GW, Fleming G, Ghirardi M, Gunner MR, Junge W, Kramer DM, Melis A, Moore TA, Moser CC, Nocera DG, Nozik AJ, Ort DR, Parson WW, Prince RC, Sayre RT (2011) Comparing photosynthetic and photovoltaic efficiencies and recognizing the potential for improvement. Science 332:805–809. doi:10.1126/science.1200165
Borirak O, de Koning LJ, van der Woude AD, Hoefsloot HC, Dekker HL, Roseboom W, de Koster CG, Hellingwerf KJ (2015) Quantitative proteomics analysis of an ethanol- and a lactate-producing mutant strain of Synechocystis sp. PCC6803. Biotechnol Biofuels 8:111. doi:10.1186/s13068-015-0294-z
Bryant DA, Frigaard NU (2006) Prokaryotic photosynthesis and phototrophy illuminated. Trends Microbiol 14:488–496. doi:10.1016/j.tim.2006.09.001
Carrieri D, Broadbent C, Carruth D, Paddock T, Ungerer J, Maness PC, Ghirardi M, Yu J (2015) Enhancing photo-catalytic production of organic acids in the cyanobacterium Synechocystis sp. PCC 6803 DeltaglgC, A strain incapable of glycogen storage. Microb Biotechnol 8:275–280. doi:10.1111/1751-7915.12243
Chen G (2009) A microbial polyhydroxyalkanoates (PHA) based bio- and materials industry. Chem Soc Rev 38:2434–2446. doi:10.1039/b812677c
Chen M, Eggink LL, Hoober JK, Larkum AW (2005) Influence of structure on binding of chlorophylls to peptide ligands. J Am Chem Soc 127:2052–2053. doi:10.1021/ja043462b
Chen L, Wu L, Wang J, Zhang W (2014) Butanol tolerance regulated by a two-component response regulator Slr1037 in photosynthetic Synechocystis sp. PCC 6803. Biotechnol Biofuels 7:89. doi:10.1186/1754-6834-7-89
Cheng Y-C, Fleming GR (2009) Dynamics of Light Harvesting in Photosynthesis. In: Annu. Rev. Phys. Chem., vol 60. Annual Review of Physical Chemistry. pp 241–262. doi:10.1146/annurev.physchem.040808.090259
Cheng AA, Lu TK (2012) Synthetic biology: an emerging engineering discipline. Annu Rev Biomed Eng 14:155–178. doi:10.1146/annurev-bioeng-071811-150118
Chin T, Sano M, Takahashi T, Ohara H, Aso Y (2014) Photosynthetic production of itaconic acid in synechocystis sp. PCC6803. J Biotechnol 195C:43–45. doi:10.1016/j.jbiotec.2014.12.016
Cires S, Alvarez-Roa C, Heimann K (2015) First use of the WAVE disposable rocking bioreactor for enhanced bioproduct synthesis by N2-fixing cyanobacteria. Biotechnol Bioeng 112(3):621–626. doi:10.1002/bit.25455
Clark JH, Luque R, Matharu AS (2012) Green chemistry. Biofuels Biorefinery Annu Rev Chem Biomol Eng 3:183–207. doi:10.1146/annurev-chembioeng-062011-081014
Coelho SM, Simon N, Ahmed S, Cock JM, Partensky F (2013) Ecological and evolutionary genomics of marine photosynthetic organisms. Mol Ecol 22:867–907. doi:10.1111/mec.12000
Davies FK, Work VH, Beliaev AS, Posewitz MC (2014) Engineering Limonene and Bisabolene Production in Wild Type and a Glycogen-Deficient Mutant of Synechococcus sp. PCC 7002. Front Bioeng Biotechnol 2:21. doi:10.3389/fbioe.2014.00021
Deng MD, Coleman JR (1999) Ethanol synthesis by genetic engineering in cyanobacteria. Appl Environ Microbiol 65:523–528
Desai SH, Atsumi S (2013) Photosynthetic approaches to chemical biotechnology. Curr Opin Biotechnol 24:1031–1036. doi:10.1016/j.copbio.2013.03.015
Dexter J, Armshaw P, Sheahan C, Pembroke JT (2015) The state of autotrophic ethanol production in cyanobacteria. J Appl Microbiol 119(1):11–24. doi:10.1111/jam.12821
Dien BS, Cotta MA, Jeffries TW (2003) Bacteria engineered for fuel ethanol production: current status. Appl Microbiol Biotechnol 63:258–266. doi:10.1007/s00253-003-1444-y
Dienst D, Georg J, Abts T, Jakorew L, Kuchmina E, Borner T, Wilde A, Duhring U, Enke H, Hess WR (2014) Transcriptomic response to prolonged ethanol production in the cyanobacterium. Synechocystis sp. PCC6803. Biotechnol Biofuels 7:21. doi:10.1186/1754-6834-7-21
Ducat DC, Way JC, Silver PA (2011) Engineering cyanobacteria to generate high-value products. Trends Biotechnol 29:95–103. doi:10.1016/j.tibtech.2010.12.003
Ducat DC, Avelar-Rivas JA, Way JC, Silver PA (2012) Rerouting carbon flux To enhance photosynthetic productivity. Appl Environ Microbiol 78:2660–2668. doi:10.1128/aem.07901-11
Duhring U, Axmann IM, Hess WR, Wilde A (2006) An internal antisense RNA regulates expression of the photosynthesis gene isiA. Proc Natl Acad Sci U S A 103:7054–7058. doi:10.1073/pnas.0600927103
Dunlop MJ, Dossani ZY, Szmidt HL, Chu HC, Lee TS, Keasling JD, Hadi MZ, Mukhopadhyay A (2011) Engineering microbial biofuel tolerance and export using efflux pumps. Mol Syst Biol 7:487. doi:10.1038/msb.2011.21
Eisenhut M, Georg J, Klahn S, Sakurai I, Mustila H, Zhang P, Hess WR, Aro EM (2012) The antisense RNA As1_flv4 in the cyanobacterium Synechocystis sp. PCC 6803 prevents premature expression of the flv4-2 operon upon shift in inorganic carbon supply. J Biol Chem 287:33153–33162. doi:10.1074/jbc.M112.391755
Ezeji TC, Qureshi N, Blaschek HP (2004) Butanol fermentation research: upstream and downstream manipulations. Chem Rec 4:305–314. doi:10.1002/tcr.20023
Figge RM, Cassier-Chauvat C, Chauvat F, Cerff R (2001) Characterization and analysis of an NAD(P)H dehydrogenase transcriptional regulator critical for the survival of cyanobacteria facing inorganic carbon starvation and osmotic stress. Mol Microbiol 39:455–468. doi:10.1046/j.1365-2958.2001.02239.x
Formighieri C, Melis A (2015) A phycocyanin. phellandrene synthase fusion enhances recombinant protein expression and beta-phellandrene (monoterpene) hydrocarbons production in Synechocystis (cyanobacteria). Metab Eng 32:116–124. doi:10.1016/j.ymben.2015.09.010
Gaida SM, Al-Hinai MA, Indurthi DC, Nicolaou SA, Papoutsakis ET (2013) Synthetic tolerance: three noncoding small RNAs, DsrA, ArcZ and RprA, acting supra-additively against acid stress. Nucleic Acids Res 41:8726–8737. doi:10.1093/nar/gkt651
Gan F, Zhang S, Rockwell NC, Martin SS, Lagarias JC, Bryant DA (2014) Extensive remodeling of a cyanobacterial photosynthetic apparatus in far-red light. Science 345:1312–1317. doi:10.1126/science.1256963
Gao Z, Zhao H, Li Z, Tan X, Lu X (2012) Photosynthetic production of ethanol from carbon dioxide in genetically engineered cyanobacteria. Energ Environ Sci 5:9857. doi:10.1039/c2ee22675h
Geddes CC, Nieves IU, Ingram LO (2011) Advances in ethanol production. Curr Opin Biotechnol 22:312–319. doi:10.1016/j.copbio.2011.04.012
Giordano M, Beardall J, Raven JA (2005) CO2 concentrating mechanisms in algae: Mechanisms, environmental modulation, and evolution. In: Annu. Rev. Plant Biol., vol 56. Annual Review of Plant Biology. pp 99–131. doi:10.1146/annurev.arplant.56.032604.144052
Gonzalez-Esquer CR, Shubitowski TB, Kerfeld CA (2015) Streamlined construction of the cyanobacterial CO2-fixing organelle via protein domain fusions for use in plant. Synth Biol Plant Cell 27:2637–2644. doi:10.1105/tpc.15.00329
Gudmundsson S, Nogales J (2015) Cyanobacteria as photosynthetic biocatalysts: a systems biology perspective. Mol BioSyst 11:60–70. doi:10.1039/c4mb00335g
Hanna MC, Nozik AJ (2006) Solar conversion efficiency of photovoltaic and photoelectrolysis cells with carrier multiplication absorbers. J Appl Phys 100:074510. doi:10.1063/1.2356795
Hein S, Scholz I, Voss B, Hess WR (2013) Adaptation and modification of three CRISPR loci in two closely related cyanobacteria. RNA Biol 10:852–864. doi:10.4161/rna.24160
Hernandez-Prieto MA, Semeniuk TA, Futschik ME (2014) Toward a systems-level understanding of gene regulatory, protein interaction, and metabolic networks in cyanobacteria. Front Genet 5:191. doi:10.3389/fgene.2014.00191
Hess WR (2011) Cyanobacterial genomics for ecology and biotechnology. Curr Opin Microbiol 14:608–614. doi:10.1016/j.mib.2011.07.024
Hirokawa Y, Suzuki I, Hanai T (2014) Optimization of isopropanol production by engineered cyanobacteria with a synthetic metabolic pathway. J Biosci Bioeng. doi:10.1016/j.jbiosc.2014.10.005
Iijima H, Nakaya Y, Kuwahara A, Hirai MY, Osanai T (2015) Seawater cultivation of freshwater cyanobacterium Synechocystis sp. PCC 6803 drastically alters amino acid composition and glycogen metabolism. Front Microbiol 6:326. doi:10.3389/fmicb.2015.00326
Iwaki T, Haranoh K, Inoue N, Kojima K, Satoh R, Nishino T, Wada S, Ihara H, Tsuyama S, Kobayashi H, Wadano A (2006) Expression of foreign type I ribulose-1, 5-bisphosphate carboxylase/oxygenase (EC 4.1.1.39) stimulates photosynthesis in cyanobacterium Synechococcus PCC7942 cells. Photosynth Res 88:287–297. doi:10.1007/s11120-006-9048-x
Jacobsen JH, Frigaard NU (2014) Engineering of photosynthetic mannitol biosynthesis from CO2 in a cyanobacterium. Metab Eng 21:60–70. doi:10.1016/j.ymben.2013.11.004
Jin H, Chen L, Wang J, Zhang W (2014) Engineering biofuel tolerance in non-native producing microorganisms. Biotechnol Adv 32:541–548. doi:10.1016/j.biotechadv.2014.02.001
Joseph A, Aikawa S, Sasaki K, Matsuda F, Hasunuma T, Kondo A (2014) Increased biomass production and glycogen accumulation in apcE gene deleted Synechocystis sp. PCC 6803. AMB Express 4:17. doi:10.1186/s13568-014-0017-z
Kaczmarzyk D, Anfelt J, Sarnegrim A, Hudson EP (2014) Overexpression of sigma factor SigB improves temperature and butanol tolerance of Synechocystis sp. PCC6803. J Biotechnol 182-183:54–60. doi:10.1016/j.jbiotec.2014.04.017
Kamennaya NA, Ahn S, Park H, Bartal R, Sasaki KA, Holman HY, Jansson C (2015) Installing extra bicarbonate transporters in the cyanobacterium Synechocystis sp. PCC6803 enhances biomass production. Metab Eng 29:76–85. doi:10.1016/j.ymben.2015.03.002
Kang Q, Appels L, Tan T, Dewil R (2014) Bioethanol from lignocellulosic biomass: current findings determine research priorities. Sci World J 2014:298153. doi:10.1155/2014/298153
Kirst H, Formighieri C, Melis A (2014) Maximizing photosynthetic efficiency and culture productivity in cyanobacteria upon minimizing the phycobilisome light-harvesting antenna size. Biochim Biophys Acta 1837:1653–1664. doi:10.1016/j.bbabio.2014.07.009
Knoop H, Zilliges Y, Lockau W, Steuer R (2010) The metabolic network of Synechocystis sp. PCC 6803: systemic properties of autotrophic growth. Plant Physiol 154:410–422. doi:10.1104/pp.110.157198
Kobayashi M, Ishizuka T, Katayama M, Kanehisa M, Bhattacharyya-Pakrasi M, Pakrasi HB, Ikeuchi M (2004) Response to oxidative stress involves a novel peroxiredoxin gene in the unicellular cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol 45:290–299. doi:10.1093/pcp/pch034
Koksharova OA, Wolk CP (2002) Genetic tools for cyanobacteria. Appl Microbiol Biotechnol 58:123–137. doi:10.1007/s00253-001-0864-9
Komatsu M, Uchiyama T, Omura S, Cane DE, Ikeda H (2010) Genome-minimized Streptomyces host for the heterologous expression of secondary metabolism. Proc Natl Acad Sci U S A 107:2646–2651. doi:10.1073/pnas.0914833107
Kopf M, Hess WR (2015) Regulatory RNAs in photosynthetic cyanobacteria. FEMS Microbiol Rev 39:301–315. doi:10.1093/femsre/fuv017
Lan EI, Ro SY, Liao JC (2013) Oxygen-tolerant coenzyme A-acylating aldehyde dehydrogenase facilitates efficient photosynthetic n-butanol biosynthesis in cyanobacteria energy. Environ Sci 6:2672. doi:10.1039/c3ee41405a
Lee SY, Park JH, Jang SH, Nielsen LK, Kim J, Jung KS (2008) Fermentative butanol production by clostridia. Biotechnol Bioeng 101:209–228. doi:10.1002/bit.22003
Li H, Liao JC (2013) Engineering a cyanobacterium as the catalyst for the photosynthetic conversion of CO2 to 1,2-propanediol. Microb Cell Factories 12. doi:10.1186/1475-2859-12-4
Li X, Shen CR, Liao JC (2014) Isobutanol production as an alternative metabolic sink to rescue the growth deficiency of the glycogen mutant of Synechococcus elongatus PCC 7942. Photosynth Res 120:301–310. doi:10.1007/s11120-014-9987-6
Li C, Tao F, Ni J, Wang Y, Yao F, Xu P (2015) Enhancing the light-driven production of d-lactate by engineering cyanobacterium using a combinational strategy. Sci Rep 5:9777. doi:10.1038/srep09777
Lin MT, Occhialini A, Andralojc PJ, Parry MA, Hanson MR (2014) A faster rubisco with potential to increase photosynthesis in crops. Nature 513:547–550. doi:10.1038/nature13776
Liu X, Fallon S, Sheng J, Curtiss R 3rd (2011) CO2-limitation-inducible green recovery of fatty acids from cyanobacterial biomass. Proc Natl Acad Sci U S A 108:6905–6908. doi:10.1073/pnas.1103016108
Liu J, Chen L, Wang J, Qiao J, Zhang W (2012) Proteomic analysis reveals resistance mechanism against biofuel hexane in Synechocystis sp PCC 6803. Biotechnol Biofuels 5 doi:10.1186/1754-6834-5-68
Liu ZX, Li HC, Wei YP, Chu WY, Chong YL, Long XH, Liu ZP, Qin S, Shao HB (2013) Signal transduction pathways in Synechocystis sp. PCC 6803 and biotechnological implications under abiotic stress. Crit Rev Biotechnol 35:269–280. doi:10.3109/07388551.2013.838662
Los DA, Zorina A, Sinetova M, Kryazhov S, Mironov K, Zinchenko VV (2010) Stress sensors and signal transducers in cyanobacteria. Sensors 10:2386–2415. doi:10.3390/s100302386
Ludwig M, Bryant DA (2011) Transcription Profiling of the Model Cyanobacterium Synechococcus sp. Strain PCC 7002 by Next-Gen (SOLiD) Sequencing of cDNA. Front Microbiol 2:41. doi:10.3389/fmicb.2011.00041
Markley AL, Begemann MB, Clarke RE, Gordon GC, Pfleger BF (2015) Synthetic biology toolbox for controlling gene expression in the cyanobacterium Synechococcus sp. strain PCC 7002. ACS Synthetic Biology 4:595–603. doi:10.1021/sb500260k
Markov SA (2012) Hydrogen production in bioreactors: current trends. Energy Procedia 29:394–400. doi:10.1016/j.egypro.2012.09.046
Melis A (2009) Solar energy conversion efficiencies in photosynthesis: minimizing the chlorophyll antennae to maximize efficiency. Plant Sci 177:272–280. doi:10.1016/j.plantsci.2009.06.005
Melis A (2013) Carbon partitioning in photosynthesis. Curr Opin Chem Biol 17:453–456. doi:10.1016/j.cbpa.2013.03.010
Minty JJ, Lesnefsky AA, Lin F, Chen Y, Zaroff TA, Veloso AB, Xie B, McConnell CA, Ward RJ, Schwartz DR, Rouillard JM, Gao Y, Gulari E, Lin XN (2011) Evolution combined with genomic study elucidates genetic bases of isobutanol tolerance in Escherichia coli. Microb Cell Fact 10:18. doi:10.1186/1475-2859-10-18
Mitschke J, Georg J, Scholz I, Sharma CM, Dienst D, Bantscheff J, Voss B, Steglich C, Wilde A, Vogel J, Hess WR (2011) An experimentally anchored map of transcriptional start sites in the model cyanobacterium Synechocystis sp. PCC6803. Proc Natl Acad Sci U S A 108:2124–2129. doi:10.1073/pnas.1015154108
Miyashita H, Ikemoto H, Kurano N, Adachi K, Chihara M, Miyachi S (1996) Chlorophyll d as a major pigment. Nature 383:402–402. doi:10.1038/383402a0
Mullineaux CW (2014) Electron transport and light-harvesting switches in cyanobacteria. Front Plant Sci 5:7. doi:10.3389/fpls.2014.00007
Muro-Pastor AM, Herrero A, Flores E (2001) Nitrogen-regulated group 2 sigma factor from Synechocystis sp. strain PCC 6803 involved in survival under nitrogen stress. J Bacteriol 183:1090–1095. doi:10.1128/JB.183.3.1090-1095.2001
Na D, Yoo SM, Chung H, Park H, Park JH, Lee SY (2013) Metabolic engineering of Escherichia coli using synthetic small regulatory RNAs. Nat Biotechnol 31:170–174. doi:10.1038/nbt.2461
Nikkinen HL, Hakkila K, Gunnelius L, Huokko T, Pollari M, Tyystjarvi T (2012) The SigB sigma factor regulates multiple salt acclimation responses of the cyanobacterium Synechocystis sp. PCC 6803. Plant Physiol 158:514–523. doi:10.1104/pp.111.190058
Niu X, Zhu Y, Pei G, Wu L, Chen L, Zhang W (2015) Elucidating butanol tolerance mediated by a response regulator Sll0039 in Synechocystis sp. PCC 6803 using a metabolomic approach. Appl Microbiol Biotechnol 99:1845–1857. doi:10.1007/s00253-015-6374-y
Nogales J, Gudmundsson S, Knight EM, Palsson BO, Thiele I (2012) Detailing the optimality of photosynthesis in cyanobacteria through systems biology analysis. Proc Natl Acad Sci U S A 109:2678–2683. doi:10.1073/pnas.1117907109
Ogawa T, Kaplan A (2003) Inorganic carbon acquisition systems in cyanobacteria. Photosynth Res 77:105–115. doi:10.1023/A:1025865500026
Oliver JW, Atsumi S (2014) Metabolic design for cyanobacterial chemical synthesis. Photosynth Res 120:249–261. doi:10.1007/s11120-014-9997-4
Oliver JW, Machado IM, Yoneda H, Atsumi S (2013) Cyanobacterial conversion of carbon dioxide to 2,3-butanediol. Proc Natl Acad Sci U S A 110:1249–1254. doi:10.1073/pnas.1213024110
Osanai T, Oikawa A, Azuma M, Tanaka K, Saito K, Hirai MY, Ikeuchi M (2011) Genetic engineering of group 2 sigma factor SigE widely activates expressions of sugar catabolic genes in Synechocystis species PCC 6803. J Biol Chem 286(35):30962–30971. doi:10.1074/jbc.M111.231183
Osanai T, Numata K, Oikawa A, Kuwahara A, Iijima H, Doi Y, Tanaka K, Saito K, Hirai MY (2013) Increased bioplastic production with an RNA polymerase sigma factor SigE during nitrogen starvation in Synechocystis sp. PCC 6803. DNA Res: Int J Rapid Publ Rep Genes Genomes 20(6):525–535. doi:10.1093/dnares/dst028
Osanai T, Oikawa A, Numata K, Kuwahara A, Iijima H, Doi Y, Saito K, Hirai MY (2014) Pathway-level acceleration of glycogen catabolism by a response regulator in the cyanobacterium Synechocystis species PCC 6803. Plant Physiol 164(4):1831–1841. doi:10.1104/pp.113.232025
Osanai T, Shirai T, Iijima H, Nakaya Y, Okamoto M, Kondo A, Hirai MY (2015) Genetic manipulation of a metabolic enzyme and a transcriptional regulator increasing succinate excretion from unicellular cyanobacterium. Front Microbiol 6:1064. doi:10.3389/fmicb.2015.01064
Piven I, Friedrich A, Dühring U, Uliczka F, Baier K, Inaba M, Shi T, Wang K, Enke H, Kramer D (2014) Cyanobacterium sp. for Production of Compounds. Patent Publication, Number: US 20140178958 A1
Price GD (2011) Inorganic carbon transporters of the cyanobacterial CO2 concentrating mechanism. Photosynth Res 109:47–57. doi:10.1007/s11120-010-9608-y
Price GD, Badger MR, Woodger FJ, Long BM (2008) Advances in understanding the cyanobacterial CO2-concentrating-mechanism (CCM): functional components, Ci transporters, diversity, genetic regulation and prospects for engineering into plants. J Exp Bot 59:1441–1461. doi:10.1093/jxb/erm112
Qi LS, Larson MH, Gilbert LA, Doudna JA, Weissman JS, Arkin AP, Lim WA (2013) Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell 152:1173–1183 doi:10.1016/j.cell.2013.02.022
Qiao J, Wang J, Chen L, Tian X, Huang S, Ren X, Zhang W (2012) Quantitative iTRAQ LC-MS/MS proteomics reveals metabolic responses to biofuel ethanol in cyanobacterial Synechocystis sp. PCC 6803. J Proteome Res 11:5286–5300. doi:10.1021/pr300504w
Qiao J, Huang S, Te R, Wang J, Chen L, Zhang W (2013) Integrated proteomic and transcriptomic analysis reveals novel genes and regulatory mechanisms involved in salt stress responses in Synechocystis sp. PCC 6803. Appl Microbiol Biotechnol 97(18):8253–8264. doi:10.1007/s00253-013-5139-8
Robertson DE, Jacobson SA, Morgan F, Berry D, Church GM, Afeyan NB (2011) A new dawn for industrial photosynthesis. Photosynth Res 107:269–277. doi:10.1007/s11120-011-9631-7
Ruffing AM (2014) Improved Free Fatty Acid Production in Cyanobacteria with Synechococcus sp. PCC 7002 as Host. Front Bioeng Biotechnol 2:17. doi:10.3389/fbioe.2014.00017
Ruffing AM, Trahan CA (2014) Biofuel toxicity and mechanisms of biofuel tolerance in three model cyanobacteria. Algal Res 5:121–132. doi:10.1016/j.algal.2014.07.006
Sakurai I, Stazic D, Eisenhut M, Vuorio E, Steglich C, Hess WR, Aro EM (2012) Positive regulation of psbA gene expression by cis-encoded antisense RNAs in Synechocystis sp. PCC 6803. Plant Physiol 160:1000–1010. doi:10.1104/pp.112.202127
Savakis P, Hellingwerf KJ (2014) Engineering cyanobacteria for direct biofuel production from CO. Curr Opin Biotechnol 33C:8–14. doi:10.1016/j.copbio.2014.09.007
Savakis P, Tan X, Du W, Branco dos Santos F, Lu X, Hellingwerf KJ (2015) Photosynthetic production of glycerol by a recombinant cyanobacterium. J Biotechnol 195:46–51. doi:10.1016/j.jbiotec.2014.12.015
Scholz I, Lange SJ, Hein S, Hess WR, Backofen R (2013) CRISPR-cas systems in the cyanobacterium Synechocystis sp. PCC6803 exhibit distinct processing pathways involving at least two Cas6 and a Cmr2 protein. PLoS one 8:e56470. doi:10.1371/journal.pone.0056470
Scully S, Orlygsson J (2014) Recent advances in second generation ethanol production by thermophilic bacteria. Energies 8(1):1–30. doi:10.3390/en8010001
Shen CR, Liao JC (2012) Photosynthetic production of 2-methyl-1-butanol from CO2 in cyanobacterium Synechococcus elongatus PCC7942 and characterization of the native acetohydroxyacid synthase. Energ Environ Sci 5:9574–9583. doi:10.1039/c2ee23148d
Sheng J, Kim HW, Badalamenti JP, Zhou C, Sridharakrishnan S, Krajmalnik-Brown R, Rittmann BE, Vannela R (2011) Effects of temperature shifts on growth rate and lipid characteristics of Synechocystis sp. PCC6803 in a bench-top photobioreactor. Bioresour Technol 102:11218–11225. doi:10.1016/j.biortech.2011.09.083
Song Z, Chen L, Wang J, Lu Y, Jiang W, Zhang W (2014) A transcriptional regulator Sll0794 regulates tolerance to biofuel ethanol in photosynthetic Synechocystis sp. PCC 6803. Mol Cell Proteomics 13:3519–3532. doi:10.1074/mcp.M113.035675
Stanier RY, Cohen-Bazire G (1977) Phototrophic Prokaryotes: the cyanobacteria. Annu Rev Microbiol 31:225–274. doi:10.1146/annurev.mi.31.100177.001301
Tamoi M, Miyazaki T, Fukamizo T, Shigeoka S (2005) The Calvin cycle in cyanobacteria is regulated by CP12 via the NAD(H)/NADP(H) ratio under light/dark conditions. Plant J: Cell Mol Biol 42(4):504–513. doi:10.1111/j.1365-313X.2005.02391.x
Tian X, Chen L, Wang J, Qiao J, Zhang W (2013) Quantitative proteomics reveals dynamic responses of Synechocystis sp. PCC 6803 to next-generation biofuel butanol. J Proteome 78:326–345. doi:10.1016/j.jprot.2012.10.002
Uchiyama J, Kanesaki Y, Iwata N, Asakura R, Funamizu K, Tasaki R, Agatsuma M, Tahara H, Matsuhashi A, Yoshikawa H, Ogawa S, Ohta H 2015) Genomic analysis of parallel-evolved cyanobacterium Synechocystis sp. PCC 6803 under acid stress. Photosynth Res 125:243–254. doi:10.1007/s11120-015-0111-3
van der Woude AD, Angermayr SA, Puthan Veetil V, Osnato A, Hellingwerf KJ (2014) Carbon sink removal: increased photosynthetic production of lactic acid by Synechocystis sp. PCC6803 in a glycogen storage mutant. J Biotechnol 184:100–102. doi:10.1016/j.jbiotec.2014.04.029
Varman AM, Yu Y, You L, Tang YJ (2013) Photoautotrophic production of D-lactic acid in an engineered cyanobacterium. Microb Cell Fact 12:117. doi:10.1186/1475-2859-12-117
Vermaas WFJ (2001) Photosynthesis and Respiration in Cyanobacteria. In: eLS. John Wiley & Sons, Ltd. doi:10.1038/npg.els.0001670
Voss B, Georg J, Schon V, Ude S, Hess WR (2009) Biocomputational prediction of non-coding RNAs in model cyanobacteria. BMC Genomics 10:123. doi:10.1186/1471-2164-10-123
Wallace-Salinas V, Gorwa-Grauslund MF (2013) Adaptive evolution of an industrial strain of Saccharomyces cerevisiae for combined tolerance to inhibitors and temperature. Biotechnol Biofuels 6:151. doi:10.1186/1754-6834-6-151
Wang B, Wang J, Zhang W, Meldrum DR (2012a) Application of synthetic biology in cyanobacteria and algae. Front Microbiol 3:344. doi:10.3389/fmicb.2012.00344
Wang J, Chen L, Huang S, Liu J, Ren X, Tian X, Qiao J, Zhang W (2012b) RNA-seq based identification and mutant validation of gene targets related to ethanol resistance in cyanobacterial Synechocystis sp PCC 6803 biotechnol. Biofuels 5:89. doi:10.1186/1754-6834-5-89
Wang B, Pugh S, Nielsen DR, Zhang W, Meldrum DR (2013a) Engineering cyanobacteria for photosynthetic production of 3-hydroxybutyrate directly from CO2. Metab Eng 16:68–77. doi:10.1016/j.ymben.2013.01.001
Wang W, Liu X, Lu X (2013b) Engineering cyanobacteria to improve photosynthetic production of alka(e)nes. Biotechnol Biofuels 6:69. doi:10.1186/1754-6834-6-69
Wang Y, Shi M, Niu X, Zhang X, Gao L, Chen L, Wang J, Zhang W (2014) Metabolomic basis of laboratory evolution of butanol tolerance in photosynthetic Synechocystis sp. PCC 6803. Microb Cell Factories 13:151. doi:10.1186/s12934-014-0151-y
Wang Y, Sun T, Gao X, Shi M, Wu L, Chen L, Zhang W (2015) Biosynthesis of platform chemical 3-hydroxypropionic acid (3-HP) directly from CO in cyanobacterium Synechocystis sp. PCC 6803. Metab Eng. doi:10.1016/j.ymben.2015.10.008
Wirth TE, Gray CB, Podesta JD (2003) The future of energy policy. Foreign Aff 82:132–155. doi:10.2307/20033654
Xiong W, Morgan JA, Ungerer J, Wang B, Maness P-C, Yu J (2015) The plasticity of cyanobacterial metabolism supports direct CO2 conversion to ethylene. Nature Plants 1:15053. doi:10.1038/nplants.2015.53
Xue Y, Zhang Y, Cheng D, Daddy S, He Q (2014) Genetically engineering Synechocystis sp. Pasteur culture collection 6803 for the sustainable production of the plant secondary metabolite p-coumaric acid. Proc Natl Acad Sci U S A 111:9449–9454. doi:10.1073/pnas.1323725111
Yao L, Qi F, Tan X, Lu X (2014) Improved production of fatty alcohols in cyanobacteria by metabolic engineering. Biotechnol Biofuels 7:94. doi:10.1186/1754-6834-7-94
Yao L, Cengic I, Anfelt J, Hudson EP (2015) Multiple Gene Repression in Cyanobacteria Using CRISPRi. ACS Synthetic Biology. doi:10.1021/acssynbio.5b00264
Yoo SM, Na D, Lee SY (2013) Design and use of synthetic regulatory small RNAs to control gene expression in Escherichia coli. Nat Protocols 8:1694–1707. doi:10.1038/nprot.2013.105
Yu J, Shen G, Wang T, Bryant DA, Golbeck JH, McIntosh L (2003) Suppressor mutations in the study of photosystem I biogenesis: sll0088 is a previously unidentified gene involved in reaction center accumulation in Synechocystis sp. strain PCC 6803. J Bacteriol 185:3878–3887. doi:10.1128/JB.185.13.3878-3887.2003
Zess EK, Begemann MB, Pfleger BF (2015) Construction of new synthetic biology tools for the control of gene expression in the cyanobacterium Synechococcus sp. strain PCC 7002. Biotechnol Bioeng. doi:10.1002/bit.25713
Zhang F, Rodriguez S, Keasling JD (2011) Metabolic engineering of microbial pathways for advanced biofuels production. Curr Opin Biotechnol 22:775–783. doi:10.1016/j.copbio.2011.04.024
Zhang Y, Niu X, Shi M, Pei G, Zhang X, Chen L, Zhang W (2015) Identification of a transporter Slr0982 involved in ethanol tolerance in cyanobacterium Synechocystis sp. PCC 6803. Front Microbiol 6:487. doi:10.3389/fmicb.2015.00487
Zhou J, Zhang H, Zhang Y, Li Y, Ma Y (2012) Designing and creating a modularized synthetic pathway in cyanobacterium Synechocystis enables production of acetone from carbon dioxide. Metab Eng 14:394–400. doi:10.1016/j.ymben.2012.03.005
Zhou J, Zhang HF, Meng HK, Zhang YP, Li Y (2014) Production of optically pure D-lactate from CO2 by blocking the PHB and acetate pathways and expressing D-lactate dehydrogenase in cyanobacterium Synechocystis sp PCC 6803. Process Biochem 49:2071–2077. doi:10.1016/j.procbio.2014.09.007
Zhu H, Ren X, Wang J, Song Z, Shi M, Qiao J, Tian X, Liu J, Chen L, Zhang W (2013) Integrated OMICS guided engineering of biofuel butanol-tolerance in photosynthetic Synechocystis sp PCC 6803. Biotechnol Biofuels 6:106. doi:10.1186/1754-6834-6-106
Zhu Y, Pei G, Niu X, Shi M, Zhang M, Chen L, Zhang W (2014) Metabolomic analysis reveals functional overlapping of three signal transduction proteins in regulating ethanol tolerance in cyanobacterium Synechocystis sp. PCC 6803. Mol Biosyst. doi:10.1039/c4mb00651h
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The work was supported by grants from the Natural Science Foundation of China (NSFC) (No. 31,470,217), the National Basic Research Program of China (National “973” program, project No. 2011CBA00803 and No. 2014CB745101), and the National High-tech RD Program of China (National “863” program) (No. 2012AA02A707).
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Gao, X., Sun, T., Pei, G. et al. Cyanobacterial chassis engineering for enhancing production of biofuels and chemicals. Appl Microbiol Biotechnol 100, 3401–3413 (2016). https://doi.org/10.1007/s00253-016-7374-2
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DOI: https://doi.org/10.1007/s00253-016-7374-2