Abstract
Cyanobacteria are attractive hosts that can be engineered for the photosynthetic production of fuels, fine chemicals, and proteins from CO2. Moreover, the responsiveness of these photoautotrophs towards different environmental signals, such as light, CO2, diurnal cycle, and metals make them potential hosts for the development of biosensors. However, engineering these hosts proves to be a challenging and lengthy process. Synthetic biology can make the process of biological engineering more predictable through the use of standardized biological parts that are well characterized and tools to assemble them. While significant progress has been made with model heterotrophic organisms, many of the parts and tools are not portable in cyanobacteria. Therefore, efforts are underway to develop and characterize parts derived from cyanobacteria. In this review, we discuss the reported parts and tools with the objective to develop cyanobacteria as cell factories or biosensors. We also discuss the issues related to characterization, tunability, portability, and the need to develop enabling technologies to engineer this “green” chassis.
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References
Abe K, Miyake K, Nakamura M, Kojima K, Ferri S, Ikebukuro K, Sode K (2014) Engineering of a green-light inducible gene expression system in Synechocystis sp. PCC 6803. Microb Biotechnol 7:177–183. https://doi.org/10.1111/1751-7915.12098
Adams BL (2016) The next generation of synthetic biology chassis: moving synthetic biology from the laboratory to the field. ACS Synth Biol 5:1328–1330. https://doi.org/10.1021/acssynbio.6b00256
Alagesan S, Gaudana SB, Sinha A, Wangikar PP (2013) Metabolic flux analysis of Cyanothece sp. ATCC 51142 under mixotrophic conditions. Photosynth Res 118:191–198. https://doi.org/10.1007/s11120-013-9911-5
Alagesan S, Gaudana SB, Wangikar PP (2016) Rhythmic oscillations in KaiC1 phosphorylation and ATP/ADP ratio in nitrogen-fixing cyanobacterium Cyanothece sp. ATCC 51142. Biol Rhythm Res 47:285–301. https://doi.org/10.1080/09291016.2015.1116737
Alper H, Fischer C, Nevoigt E, Stephanopoulos G (2005) Tuning genetic control through promoter engineering. Proc Natl Acad Sci U S A 102:12678–12683. https://doi.org/10.1073/pnas.0504604102
Arpino JAJ, Hancock EJ, Anderson J, Barahona M, Stan G-BV, Papachristodoulou A, Polizzi K (2013) Tuning the dials of synthetic biology. Microbiology 159:1236–1253. https://doi.org/10.1099/mic.0.067975-0
Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37:W202–W208. https://doi.org/10.1093/nar/gkp335
Begemann MB, Zess EK, Walters EM, Schmitt EF, Markley AL, Pfleger BF (2013) An organic acid based counter selection system for cyanobacteria. PLoS One 8:e76594. https://doi.org/10.1371/journal.pone.0076594
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. https://doi.org/10.3389/fmicb.2013.00246
Boldt J (2013) Synthetic biology. Humana Press, Totowa
Callura JM, Cantor CR, Collins JJ (2012) Genetic switchboard for synthetic biology applications. Proc Natl Acad Sci 109:5850–5855. https://doi.org/10.1073/pnas.1203808109
Campbell WH, Gowri G (1990) Codon usage in higher plants, green algae, and cyanobacteria. Plant Physiol 92:1–11. https://doi.org/10.1104/pp.92.1.1
Canton B, Labno A, Endy D (2008) Refinement and standardization of synthetic biological parts and devices. Nat Biotechnol 26:787–793. https://doi.org/10.1038/nbt1413
Chen Y-J, Liu P, Nielsen AAK, Brophy JAN, Clancy K, Peterson T, Voigt CA (2013) Characterization of 582 natural and synthetic terminators and quantification of their design constraints. Nat Methods 10:659–664. https://doi.org/10.1038/nmeth.2515
Choi YN, Park JM (2015) Enhancing biomass and ethanol production by increasing NADPH production in Synechocystis sp. PCC 6803. Bioresour Technol 213:54–57. https://doi.org/10.1016/j.biortech.2016.02.056
Cohen SE, Erb ML, Pogliano J, Golden SS (2015) Best practices for fluorescence microscopy of the cyanobacterial circadian clock. In: Methods in enzymology. pp 211–221
Copeland MF, Politz MC, Pfleger BF (2014) ScienceDirect. Application of TALEs, CRISPR/Cas and sRNAs as trans-acting regulators in prokaryotes. Curr Opin Biotechnol 29:46–54. https://doi.org/10.1016/j.copbio.2014.02.010
Copeland MF, Politz MP, Johnson C, Markley AL, Pfleger BF (2016) A transcription activator-like effector induction system mediated by proteolytic degradation. Nat Chem Biol advance on:1–9. doi: https://doi.org/10.1038/nchembio.2021
Deng M, Coleman JR (1999) Ethanol synthesis by genetic engineering in cyanobacteria. Appl Environ Microbiol 65:523–528
Elhai J (2015) Highly iterated palindromic sequences (HIPs) and their relationship to DNA methyltransferases. Life 5:921–948. https://doi.org/10.3390/life5010921
Endy D (2005) Foundations for engineering biology. Nature 438:449–453. https://doi.org/10.1038/nature04342
Englund E, Liang F, Lindberg P (2016) Evaluation of promoters and ribosome binding sites for biotechnological applications in the unicellular cyanobacterium Synechocystis sp. PCC 6803. Sci Rep 6:36640. https://doi.org/10.1038/srep36640
Fernández-González B, Martínez-Férez IM, Vioque A (1998) Characterization of two carotenoid gene promoters in the cyanobacterium Synechocystis sp. PCC 6803. Biochim Biophys Acta 1443:343–351
Fujisawa T, Narikawa R, Maeda S, Satoru W, Kanesaki Y, Kobayashi K, Nomata J, Hanaoka M, Watanabe M, Ehira S, Suzuki E, Awai K, Nakamura Y (2017) CyanoBase: a large-scale update on its 20th anniversary. Nucleic Acids Res 45:3475–3482. https://doi.org/10.1093/mnras/stw2966
Gaj T, Gersbach CA, Barbas IIICF (2014) ZFN, TALEN and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol 31:397–405. https://doi.org/10.1016/j.tibtech.2013.04.004.ZFN
Gao X, Gao F, Liu D, Zhang H, Nie X, Yang C (2016a) Engineering the methylerythritol phosphate pathway in cyanobacteria for photosynthetic isoprene production from CO2. Energy Environ Sci 9:1400–1411. https://doi.org/10.1039/C5EE03102H
Gao X, Sun T, Pei G, Chen L, Zhang W (2016b) Cyanobacterial chassis engineering for enhancing production of biofuels and chemicals. Appl Microbiol Biotechnol 100:3401–3413. https://doi.org/10.1007/s00253-016-7374-2
Garcia-Dominguez M, Lopez-Maury L, Florencio FJ, Reyes JC (2000) A gene cluster involved in metal homeostasis in the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol 182:1507–1514. https://doi.org/10.1128/JB.182.6.1507-1514.2000
Golden SS (1995) Light-responsive gene expression in cyanobacteria. J Bacteriol 177:1651–1654
Gordon GC, Korosh TC, Cameron JC, Markley AL, Begemann MB, Pfleger BF (2016) CRISPR interference as a titratable, trans-acting regulatory tool for metabolic engineering in the cyanobacterium Synechococcus sp. strain PCC 7002. Metab Eng 38:170–179. https://doi.org/10.1016/j.ymben.2016.07.007
Hendry JI, Prasannan C, Ma F, Möllers KB, Jaiswal D, Digmurti M, Allen DK, Frigaard NU, Dasgupta S, Wangikar PP (2017) Rerouting of carbon flux in a glycogen mutant of cyanobacteria assessed via isotopically non-stationary 13C metabolic flux analysis. Biotechnol Bioeng 114:2298–2308. https://doi.org/10.1002/bit.26350
Hendry JI, Prasannan CB, Joshi A, Dasgupta S, Wangikar PP (2016) Metabolic model of Synechococcus sp. PCC 7002: prediction of flux distribution and network modification for enhanced biofuel production. Bioresour Technol 213:190–197. https://doi.org/10.1016/j.biortech.2016.02.128
Hentschel E, Will C, Mustafi N, Burkovski A, Rehm N, Frunzke J (2013) Destabilized eYFP variants for dynamic gene expression studies in Corynebacterium glutamicum. Microb Biotechnol 6:196–201. https://doi.org/10.1111/j.1751-7915.2012.00360.x
Hirose Y, Shimada T, Narikawa R, Katayama M, Ikeuchi M (2008) Cyanobacteriochrome CcaS is the green light receptor that induces the expression of phycobilisome linker protein. Proc Natl Acad Sci U S A 105:9528–9533. https://doi.org/10.1073/pnas.0801826105
Holland SC, Artier J, Miller NT, Cano M, Yu J, Ghirardi ML, Burnap RL (2016) Impacts of genetically engineered alterations in carbon sink pathways on photosynthetic performance. Algal Res 20:87–99. https://doi.org/10.1016/j.algal.2016.09.021
Holmqvist M, Stensjö K, Oliveira P, Lindberg P, Lindblad P (2009) Characterization of the hupSL promoter activity in Nostoc punctiforme ATCC 29133. BMC Microbiol 9:54. https://doi.org/10.1186/1471-2180-9-54
Huang CH, Shen CR, Li H, Sung LY, Wu MY, Hu YC (2016) CRISPR interference (CRISPRi) for gene regulation and succinate production in cyanobacterium S. elongatus PCC 7942. Microb Cell Factories 15:1–11. https://doi.org/10.1186/s12934-016-0595-3
Huang H-H, Camsund D, Lindblad P, Heidorn T (2010) Design and characterization of molecular tools for a synthetic biology approach towards developing cyanobacterial biotechnology. Nucleic Acids Res 38:2577–2593. https://doi.org/10.1093/nar/gkq164
Huang H-H, Lindblad P (2013) Wide-dynamic-range promoters engineered for cyanobacteria. J Biol Eng 7:10. https://doi.org/10.1186/1754-1611-7-10
Imamura S, Asayama M (2009) Sigma factors for cyanobacterial transcription. Gene Regul Syst Bio 3:65–87
Immethun CM, DeLorenzo DM, Focht CM, Gupta D, Johnson CB, Moon TS (2017) Physical, chemical, and metabolic state sensors expand the synthetic biology toolbox for Synechocystis sp. PCC 6803. Biotechnol Bioeng 114:1561–1569. https://doi.org/10.1002/bit.26275
Immethun CM, Ng KM, Delorenzo DM, Waldron-Feinstein B, Lee YC, Moon TS (2015) Oxygen-responsive genetic circuits constructed in Synechocystis sp. PCC 6803. Biotechnol Bioeng 113:433–442. https://doi.org/10.1002/bit.25722
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 PCC 7942 cells. Photosynth Res 88:287–297. https://doi.org/10.1007/s11120-006-9048-x
Jaiswal D (2017) Codon. In: Vonk J, Shackelford T (eds) Encyclopedia of animal cognition and behavior. Springer International Publishing, Cham, pp 1–5
Kahl LJ, Endy D (2013) A survey of enabling technologies in synthetic biology. J Biol Eng 7:13. https://doi.org/10.1186/1754-1611-7-13
Kelly JR, Rubin AJ, Davis JH, Ajo-Franklin CM, Cumbers J, Czar MJ, de Mora K, Glieberman AL, Monie DD, Endy D (2009) Measuring the activity of BioBrick promoters using an in vivo reference standard. J Biol Eng 3:4. https://doi.org/10.1186/1754-1611-3-4
Kelwick R, MacDonald JT, Webb AJ, Freemont P (2014) Developments in the tools and methodologies of synthetic biology. Front Bioeng Biotechnol 2:60. https://doi.org/10.3389/fbioe.2014.00060
Kim J, Salvador M, Saunders E, González J, Avignone-Rossa C, Jiménez JI (2016) Properties of alternative microbial hosts used in synthetic biology: towards the design of a modular chassis. Essays Biochem 60:303–313. https://doi.org/10.1042/EBC20160015
Kim WJ, Lee S-M, Um Y, Sim SJ, Woo HM (2017) Development of SyneBrick vectors as a synthetic biology platform for gene expression in Synechococcus elongatus PCC 7942. Front Plant Sci 8:1–9. https://doi.org/10.3389/fpls.2017.00293
Knoot CJ, Ungerer JL, Wangikar PP, Pakrasi HB (2017) Cyanobacteria: promising biocatalysts for sustainable chemical production. J Biol Chem jbc.R117.815886. doi: https://doi.org/10.1074/jbc.R117.815886
Kopka J, Schmidt S, Dethloff F, Pade N, Berendt S, Schottkowski M, Martin N, Dühring U, Kuchmina E, Enke H, Kramer D, Wilde A, Hagemann M, Friedrich A (2017) Systems analysis of ethanol production in the genetically engineered cyanobacterium Synechococcus sp. PCC 7002. Biotechnol Biofuels 10:56. https://doi.org/10.1186/s13068-017-0741-0
Krishnakumar S, Gaudana SB, Digmurti MG, Viswanathan GA, Chetty M, Wangikar PP (2015a) Influence of mixotrophic growth on rhythmic oscillations in expression of metabolic pathways in diazotrophic cyanobacterium Cyanothece sp. ATCC 51142. Bioresour Technol 188:145–152. https://doi.org/10.1016/j.biortech.2015.02.016
Krishnakumar S, Gaudana SB, Vinh NX, Viswanathan GA, Chetty M, Wangikar PP (2015b) Coupling of cellular processes and their coordinated oscillations under continuous light in Cyanothece sp. ATCC 51142, a diazotrophic unicellular cyanobacterium. PLoS One 10:1–23. https://doi.org/10.1371/journal.pone.0125148
Kulkarni RD, Golden SS (1994) Adaptation to high light intensity in Synechococcus sp. strain PCC 7942: regulation of three psbA genes and two forms of the D1 protein. J Bacteriol 176:959–965
Kutsuna S, Nakahira Y, Katayama M, Ishiura M, Kondo T (2005) Transcriptional regulation of the circadian clock operon kaiBC by upstream regions in cyanobacteria. Mol Microbiol 57:1474–1484. https://doi.org/10.1111/j.1365-2958.2005.04781.x
Lan EI, Liao JC (2012) ATP drives direct photosynthetic production of 1-butanol in cyanobacteria. Proc Natl Acad Sci U S A 109:6018–6023. https://doi.org/10.1073/pnas.1200074109
Lee SJ, Lee D-Y, Kim TY, Kim BH, Lee J, Lee SY (2005) Metabolic engineering of Escherichia coli for enhanced production of succinic acid, based on genome comparison and in silico gene knockout simulation. Appl Environ Microbiol 71:7880–7887. https://doi.org/10.1128/AEM.71.12.7880-7887.2005
Li H, Liao JC (2013) Engineering a cyanobacterium as the catalyst for the photosynthetic conversion of CO2 to 1,2-propanediol. Microb Cell Factories 12:4. https://doi.org/10.1186/1475-2859-12-4
Li H, Shen CR, Huang C, Sung L, Wu M, Hu Y (2016) CRISPR-Cas9 for the genome engineering of cyanobacteria and succinate production. Metab Eng 38:293–302. https://doi.org/10.1016/j.ymben.2016.09.006
Li R, Golden SS (1993) Enhancer activity of light-responsive regulatory elements in the untranslated leader regions of cyanobacterial psbA genes. Proc Natl Acad Sci 90:11678–11682. https://doi.org/10.1073/pnas.90.24.11678
Liauw P, Kannchen D, Gasper R, Dyczmons-Nowaczyk N, Nowaczyk MM, Hofmann E (2015) Cloning, expression, crystallization and preliminary X-ray studies of a superfolder GFP fusion of cyanobacterial Psb32. Acta Crystallogr Sect F, Struct Biol Commun 71:409–413. https://doi.org/10.1107/S2053230X15003970
Lin P-C, Saha R, Zhang F, Pakrasi HB (2017) Metabolic engineering of the pentose phosphate pathway for enhanced limonene production in the cyanobacterium Synechocystis sp. PCC 6803. Sci Rep 7:17503. https://doi.org/10.1038/s41598-017-17831-y
Liu BR, Huang Y-W, Lee H-J (2013) Mechanistic studies of intracellular delivery of proteins by cell-penetrating peptides in cyanobacteria. BMC Microbiol 13:57. https://doi.org/10.1186/1471-2180-13-57
Los DA, Zorina A, Sinetova M, Kryazhov S, Mironov K, Zinchenko VV (2010) Stress sensors and signal transducers in cyanobacteria. Sensors 10:2386–2415. https://doi.org/10.3390/s100302386
Ma AT, Schmidt CM, Golden JW (2014) Regulation of gene expression in diverse cyanobacterial species by using theophylline-responsive riboswitches. Appl Environ Microbiol 80:6704–6713. https://doi.org/10.1128/AEM.01697-14
Ma X, Zhu Q, Chen Y, Liu Y-G, Y-g L (2016) CRISPR/Cas9 platforms for genome editing in plants: developments and applications. Mol Plant 9:1–32. https://doi.org/10.1016/j.molp.2016.04.009
Mackey SR, Ditty JL, Clerico EM, Golden SS (2007) Detection of rhythmic bioluminescence from luciferase reporters in cyanobacteria. Methods Mol Biol 362:115–129. https://doi.org/10.1007/978-1-59745-257-1_8
Mao F, Dam P, Chou J, Olman V, Xu Y (2009) DOOR: a database for prokaryotic operons. Nucleic Acids Res 37:D459–D463. https://doi.org/10.1093/nar/gkn757
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 Synth Biol 4:595–603. https://doi.org/10.1021/sb500260k
Mehrotra P (2016) Biosensors and their applications—a review. J Oral Biol Craniofacial Res 6:153–159. https://doi.org/10.1016/j.jobcr.2015.12.002
Memon D, Singh AK, Pakrasi HB, Wangikar PP (2013) A global analysis of adaptive evolution of operons in cyanobacteria. Antonie Van Leeuwenhoek 103:331–346. https://doi.org/10.1007/s10482-012-9813-0
Moon TS, Lou C, Tamsir A, Stanton BC, Voigt CA (2012) Genetic programs constructed from layered logic gates in single cells. Nature 491:249–253. https://doi.org/10.1038/nature11516
Muramatsu M, Hihara Y (2006) Characterization of high-light-responsive promoters of the psaAB genes in Synechocystis sp. PCC 6803. Plant Cell Physiol 47:878–890. https://doi.org/10.1093/pcp/pcj060
Nakahira Y, Ogawa A, Asano H, Oyama T, Tozawa Y (2013) Theophylline-dependent riboswitch as a novel genetic tool for strict regulation of protein expression in cyanobacterium Synechococcus elongatus PCC 7942. Plant Cell Physiol 54:1724–1735. https://doi.org/10.1093/pcp/pct115
Ng AH, Berla BM, Pakrasi HB (2015) Fine-tuning of photoautotrophic protein production by combining promoters and neutral sites in the cyanobacterium Synechocystis sp. strain PCC 6803. Appl Environ Microbiol 81:6857–6863. https://doi.org/10.1128/AEM.01349-15
Nielsen J, Fussenegger M, Keasling J, Lee SY, Liao JC, Prather K, Palsson B (2014) Engineering synergy in biotechnology. Nat Chem Biol 10:319–322. https://doi.org/10.1038/nchembio.1519
Nozzi NE, Atsumi S (2015) Genome engineering of the 2,3-butanediol biosynthetic pathway for tight regulation in cyanobacteria. ACS Synth Biol 4:1197–1204. https://doi.org/10.1021/acssynbio.5b00057
Ohbayashi R, Akai H, Yoshikawa H, Hess WR, Watanabe S (2016) A tightly inducible riboswitch system in Synechocystis sp. PCC 6803. J Gen Appl Microbiol 62:154–159. https://doi.org/10.2323/jgam.2016.02.002
Oliver JWK, Machado IMP, Yoneda H, Atsumi S (2014) Combinatorial optimization of cyanobacterial 2,3-butanediol production. Metab Eng 22:76–82. https://doi.org/10.1016/j.ymben.2014.01.001
Onizuka T, Akiyama H, Endo S, Kanai S, Hirano M, Tanaka S, Miyasaka H (2002) CO2 response element and corresponding trans-acting factor of the promoter for ribulose-1,5-bisphosphate carboxylase/oxygenase genes in Synechococcus sp. PCC7002 found by an improved electrophoretic mobility shift assay. Plant Cell Physiol 43:660–667
Pasotti L, Politi N, Zucca S, Cusella de Angelis MG, Magni P (2012) Bottom-up engineering of biological systems through standard bricks: a modularity study on basic parts and devices. PLoS One 7:1–10. https://doi.org/10.1371/journal.pone.0039407
Pisciotta JM, Zou Y, Baskakov IV (2010) Light-dependent electrogenic activity of cyanobacteria. PLoS One 5:e10821. https://doi.org/10.1371/journal.pone.0010821
Prabha R, Singh DP, Sinha S, Ahmad K, Rai A (2017) Genome-wide comparative analysis of codon usage bias and codon context patterns among cyanobacterial genomes. Mar Genomics 32:31–39. https://doi.org/10.1016/j.margen.2016.10.001
Puerta-Fernandez E, Vioque A (2011) Hfq is required for optimal nitrate assimilation in the cyanobacterium Anabaena sp. strain PCC 7120. J Bacteriol 193:3546–3555. https://doi.org/10.1128/JB.00254-11
Ramey CJ, Barón-Sola Á, Aucoin HR, Boyle NR (2015) Genome engineering in cyanobacteria: where we are and where we need to go. ACS Synth Biol 4:1186–1196. https://doi.org/10.1021/acssynbio.5b00043
Robinson NJ, Robinson PJ, Gupta A, Bleasby AJ, Whitton BA, Morby AP (1995) Singular over-representation of an octameric palindrome, HIP1, in DNA from many cyanobacteria. Nucleic Acids Res 23:729–735. https://doi.org/10.1093/nar/23.5.729
Rosato E (2007) Circadian rhythms methods and protocols
Rubin BE, Wetmore KM, Price MN, Diamond S, Shultzaberger RK, Lowe LC, Curtin G, Arkin AP, Deutschbauer A, Golden SS (2015) The essential gene set of a photosynthetic organism. Proc Natl Acad Sci 112:E6634–E6643. https://doi.org/10.1073/pnas.1519220112
Ruffing AM (2014) Improved free fatty acid production in cyanobacteria with Synechococcus sp. PCC 7002 as host. Front Bioeng Biotechnol 2:17. https://doi.org/10.3389/fbioe.2014.00017
Salis HM, Mirsky EA, Voigt CA (2009) Automated design of synthetic ribosome binding sites to control protein expression. Nat Biotechnol 27:946–950. https://doi.org/10.1038/nbt.1568
Seo SW, Yang J-S, Kim I, Yang J, Min BE, Kim S, Jung GY (2013) Predictive design of mRNA translation initiation region to control prokaryotic translation efficiency. Metab Eng 15:67–74. https://doi.org/10.1016/j.ymben.2012.10.006
Shabestary K, Hudson EP (2016) Computational metabolic engineering strategies for growth-coupled biofuel production by Synechocystis. Metab Eng Commun 3:216–226
Shao CY, Howe CJ, Porter AJR, Glover LA (2002) Novel cyanobacterial biosensor for detection of herbicides. Appl Environ Microbiol 68:5026–5033. https://doi.org/10.1128/AEM.68.10.5026-5033.2002
Singh AK, Kishore GM, Pakrasi HB (2018) Emerging platforms for co-utilization of one-carbon substrates by photosynthetic organisms. Curr Opin Biotechnol 53:201–208
Stanton BC, Nielsen AAK, Tamsir A, Clancy K, Peterson T, Voigt CA (2014) Genomic mining of prokaryotic repressors for orthogonal logic gates. Nat Chem Biol 10:99–105. https://doi.org/10.1038/nchembio.1411
Stockel J, Welsh EA, Liberton M, Kunnvakkam R, Aurora R, Pakrasi HB (2008) Global transcriptomic analysis of Cyanothece 51142 reveals robust diurnal oscillation of central metabolic processes. ProcNatlAcadSciUSA 105:6156–6161. https://doi.org/10.1073/pnas.0711068105
Taton A, Lis E, Adin DM, Dong G, Cookson S, Kay SA, Golden SS, Golden JW (2012) Gene transfer in Leptolyngbya sp. strain BL0902, a cyanobacterium suitable for production of biomass and bioproducts. PLoS One 7:e30901. https://doi.org/10.1371/journal.pone.0030901
Taton A, Ma AT, Ota M, Golden SS, Golden JW (2017) NOT gate genetic circuits to control gene expression in cyanobacteria. ACS Synth Biol acssynbio.7b00203. doi: https://doi.org/10.1021/acssynbio.7b00203
Ungerer J, Pakrasi HB (2016) Cpf1 is a versatile tool for CRISPR genome editing across diverse species of cyanobacteria. Sci Rep 6:39681. https://doi.org/10.1038/srep39681
van Hijum SAFT, Medema MH, Kuipers OP (2009) Mechanisms and evolution of control logic in prokaryotic transcriptional regulation. Microbiol Mol Biol Rev 73:481–509, Table of Contents. https://doi.org/10.1128/MMBR.00037-08
Veetil VP, Angermayr SA, Hellingwerf KJ (2017) Ethylene production with engineered Synechocystis sp. PCC 6803 strains. Microb Cell Factories 16:1–11. https://doi.org/10.1186/s12934-017-0645-5
Vijayan V, Jain IH, O’Shea EK (2011) A high resolution map of a cyanobacterial transcriptome. Genome Biol 12:R47. https://doi.org/10.1186/gb-2011-12-5-r47
Vijayan V, O’Shea EK (2013) Sequence determinants of circadian gene expression phase in cyanobacteria. J Bacteriol 195:665–671. https://doi.org/10.1128/JB.02012-12
Vijayan V, Zuzow R, O’Shea EK (2009) Oscillations in supercoiling drive circadian gene expression in cyanobacteria. Proc Natl Acad Sci U S A 106:22564–22568. https://doi.org/10.1073/pnas.0912673106
Voigt C, Heidorn T, Camsund D, Huang H, Lindberg P, Oliveira P, Stensjö K, Lindblad P (2011) Synthetic biology in cyanobacteria
Wang B, Eckert C, Maness P-C, Yu J (2017) A genetic toolbox for modulating the expression of heterologous genes in the cyanobacterium Synechocystis sp. PCC 6803. ACS Synth Biol 6803:acssynbio.7b00297. doi: https://doi.org/10.1021/acssynbio.7b00297
Wang B, Wang J, Meldrum DR (2012) Application of synthetic biology in cyanobacteria and algae. Front Microbiol 3:1–15
Wendt KE, Ungerer J, Cobb RE, Zhao H, Pakrasi HB (2016) CRISPR/Cas9 mediated targeted mutagenesis of the fast growing cyanobacterium Synechococcus elongatus UTEX 2973. Microb Cell Factories 15:115. https://doi.org/10.1186/s12934-016-0514-7
Xiong W, Cano M, Wang B, Douchi D, Yu J (2017) The plasticity of cyanobacterial carbon metabolism. Curr Opin Chem Biol 41:12–19. https://doi.org/10.1016/j.cbpa.2017.09.004
Yao L, Cengic I, Anfelt J, Hudson EP (2016) Multiple gene repression in cyanobacteria using CRISPRi. ACS Synth Biol 5:207–212. https://doi.org/10.1021/acssynbio.5b00264
Yu J, Liberton M, Cliften PF, Head RD, Jacobs JM, Smith RD, Koppenaal DW, Brand JJ, Pakrasi HB (2015) Synechococcus elongatus UTEX 2973, a fast growing cyanobacterial chassis for biosynthesis using light and CO2. Sci Rep 5:8132. https://doi.org/10.1038/srep08132
Zess EK, Begemann MB, Pfleger BF (2016) Construction of new synthetic biology tools for the control of gene expression in the cyanobacterium Synechococcus sp. strain PCC 7002. Biotechnol Bioeng 113:424–432. https://doi.org/10.1002/bit.25713
Zhang F, Keasling J (2011) Biosensors and their applications in microbial metabolic engineering. Trends Microbiol 19:323–329. https://doi.org/10.1016/j.tim.2011.05.003
Zhou J, Zhang H, Meng H, Zhu Y, Bao G, Zhang Y, Li Y, Ma Y (2015) Discovery of a super-strong promoter enables efficient production of heterologous proteins in cyanobacteria. Sci Rep 4:4500. https://doi.org/10.1038/srep04500
Acknowledgements
Authors acknowledge useful discussions with Sandeep B. Gaudana, Badrish Soni, and Shinjinee Sengupta.
Funding
This work was funded by a research grants provided by the Department of Biotechnology, Government of India (Grant No: BT/EB/PAN IIT/2012) to PPW, the Indo-US Science and Technology Forum for Indo-US Advanced Bioenergy Consortium (IUABC) (Grant No: IUSSTF/JCERDC-SGB/IUABC-IITB/2016) to PPW, and HBP and Office of Science, Department of Energy-BER to HBP.
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PPW, HBP, and AS designed the research. AS performed the research. PPW, HBP, and AS wrote the paper.
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Sengupta, A., Pakrasi, H.B. & Wangikar, P.P. Recent advances in synthetic biology of cyanobacteria. Appl Microbiol Biotechnol 102, 5457–5471 (2018). https://doi.org/10.1007/s00253-018-9046-x
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DOI: https://doi.org/10.1007/s00253-018-9046-x