Oxygen-responsive genetic circuits constructed in Synechocystis sp. PCC 6803

Biotechnology and Bioengineering

Volumn 113, Issue 2, 2016, Pages 433-442

  Immethun, Cheryl M ^a   Ng, Kenneth M ^a   Delorenzo, Drew M ^a   Waldron Feinstein, Ben ^a   Lee, Ying Chiang ^a   Moon, Tae Seok ^a  

^a WASHINGTON UNIVERSITY IN ST LOUIS   (United States)

Author keywords

Cyanobacteria; Genetic circuit; Genetic context; Oxygen sensor; Synthetic biology

Indexed keywords

FLUORESCENCE; GENE EXPRESSION; OXYGEN SENSORS; PROTEINS; TIMING CIRCUITS;

CYANOBACTERIA; CYANOBACTERIAL STRAINS; ENVIRONMENTAL SIGNALS; GENETIC CIRCUITS; GENETIC CONTEXT; HETEROLOGOUS PROTEINS; SYNECHOCYSTIS SP. PCC 6803; SYNTHETIC BIOLOGY;

COMPUTER CIRCUITS;

ANHYDROTETRACYCLINE; OXYGEN; NITROGENASE; PHOTOPROTEIN;

ARTICLE; GENETIC TRANSCRIPTION; NONHUMAN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SENSOR; SYNECHOCYSTIS; SYNTHETIC BIOLOGY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MICROBIAL GENETICS; MOLECULAR BIOLOGY; PROCEDURES; REPORTER GENE; TRANSCRIPTION INITIATION;

GENE EXPRESSION REGULATION, BACTERIAL; GENES, REPORTER; GENETICS, MICROBIAL; LUMINESCENT PROTEINS; MOLECULAR BIOLOGY; NITROGENASE; OXYGEN; SYNECHOCYSTIS; SYNTHETIC BIOLOGY; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION;

EID: 84965098352     PISSN: 00063592     EISSN: 10970290     Source Type: Journal    
DOI: 10.1002/bit.25722     Document Type: Article

References (57)

1. Angermayr SA, Paszota M, Hellingwerf KJ. 2012. Engineering a cyanobacterial cell factory for production of lactic acid. Appl Environ Microbiol 78(19):7098-7106.
2. Aoki R, Takeda T, Omata T, Ihara K, Fujita Y. 2012. MarR-type transcriptional regulator ChlR activates expression of tetrapyrrole biosynthesis genes in response to low-oxygen conditions in cyanobacteria. J Biol Chem 287(16):13500-13507.
3. Arkin A. 2008. Setting the standard in synthetic biology. Nat Biotechnol 26(7):771-774.
4. Aryal UK, Callister SJ, Mishra S, Zhang X, Shutthanandan JI, Angel TE, Shukla AK, Monroe ME, Moore RJ, Koppenaal DW. 2013. Proteome analyses of strains ATCC 51142 and PCC 7822 of the diazotrophic cyanobacterium Cyanothece sp. under culture conditions resulting in enhanced H(2) production. Appl Environ Microbiol 79(4):1070-1077.
5. Bandyopadhyay A, Stockel J, Min H, Sherman LA, Pakrasi HB. 2010. High rates of photobiological H2 production by a cyanobacterium under aerobic conditions. Nat Commun 1:139.
6. Berla BM, Pakrasi HB. 2012. Upregulation of plasmid genes during stationary phase in Synechocystis sp. strain PCC 6803, a cyanobacterium. Appl Environ Microbiol 78(15):5448-5451.
7. 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.
8. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL. 2009. The MIQE guidelines: Minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55(4):611-622.
9. Camsund D, Heidorn T, Lindblad P. 2014. Design and analysis of LacI-repressed promoters and DNA-looping in a cyanobacterium. J Biol Eng 8(1):4.
10. Crack JC, Green J, Thomson AJ, Le Brun NE. 2012. Iron-sulfur cluster sensor-regulators. Curr Opin Chem Biol 16(1-2):35-44.
11. Drepper T, Eggert T, Circolone F, Heck A, Krauss U, Guterl JK, Wendorff M, Losi A, Gartner W, Jaeger KE. 2007. Reporter proteins for in vivo fluorescence without oxygen. Nat Biotechnol 25(4):443-445.
12. Ducat DC, Way JC, Silver PA. 2011. Engineering cyanobacteria to generate high-value products. Trends Biotechnol 29(2):95-103.
13. Ejima K, Kawaharada T, Inoue S, Kojima K, Nishiyama Y. 2012. A change in the sensitivity of elongation factor G to oxidation protects photosystem II from photoinhibition in Synechocystis sp. PCC 6803. FEBS Lett 586(6):778-783.
14. Engler C, Kandzia R, Marillonnet S. 2008. A one pot, one step, precision cloning method with high throughput capability. PLoS ONE 3(11):e3647.
15. Englund E, Andersen-Ranberg J, Miao R, Hamberger B, Lindberg P. 2015. Metabolic Engineering of Synechocystis sp. PCC 6803 for Production of the Plant Diterpenoid Manoyl Oxide. ACS Synth Biol
16. Espah Borujeni A, Channarasappa AS, Salis HM. 2014. Translation rate is controlled by coupled trade-offs between site accessibility, selective RNA unfolding and sliding at upstream standby sites. Nucleic Acids Res 42(4):2646-2659.
17. French CS, Smith JHC, Virgin HI, Airth RL. 1956. Fluorescence-Spectrum Curves of Chlorophylls, Pheophytins, Phycoerythrins, Phycocyanins and Hypericin. Plant Physiol 31(5):369-374.
18. Gimpel JA, Specht EA, Georgianna DR, Mayfield SP. 2013. Advances in microalgae engineering and synthetic biology applications for biofuel production. Curr Opin Chem Biol 17(3):489-495.
19. Golden SS, Brusslan J, Haselkorn R. 1987. Genetic engineering of the cyanobacterial chromosome. Methods Enzymol 153:215-231.
20. Grainger DC, Aiba H, Hurd D, Browning DF, Busby SJ. 2007. Transcription factor distribution in Escherichia coli: Studies with FNR protein. Nucleic Acids Res 35(1):269-278.
21. Griese M, Lange C, Soppa J. 2011. Ploidy in cyanobacteria. FEMS Microbiol Lett 323(2):124-131.
22. Gronenberg LS, Marcheschi RJ, Liao JC. 2013. Next generation biofuel engineering in prokaryotes. Curr Opin Chem Biol 17(3):462-471.
23. Guerrero F, Carbonell V, Cossu M, Correddu D, Jones PR. 2012. Ethylene synthesis and regulated expression of recombinant protein in Synechocystis sp. PCC 6803. PLoS ONE 7(11):e50470.
24. Heidorn T, Camsund D, Huang HH, Lindberg P, Oliveira P, Stensjo K, Lindblad P. 2011. Synthetic biology in cyanobacteria engineering and analyzing novel functions. Methods Enzymol 497:539-579.
25. Huang HH, 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(8):2577-2593.
26. Huang HH, Lindblad P. 2013. Wide-dynamic-range promoters engineered for cyanobacteria. J Biol Eng 7(1):10.
27. Imashimizu M, Tanaka K, Shimamoto N. 2011. Comparative Study of Cyanobacterial and E. coli RNA Polymerases: Misincorporation, Abortive Transcription, and Dependence on Divalent Cations. Genet Res Int 2011:572689.
28. Kang Y, Weber KD, Qiu Y, Kiley PJ, Blattner FR. 2005. Genome-wide expression analysis indicates that FNR of Escherichia coli K-12 regulates a large number of genes of unknown function. J Bacteriol 187(3):1135-1160.
29. Kittleson JT, Cheung S, Anderson JC. 2011. Rapid optimization of gene dosage in E. coli using DIAL strains. J Biol Eng 5:10.
30. Kunert A, Hagemann M, Erdmann N. 2000. Construction of promoter probe vectors for Synechocystis sp. PCC 6803 using the light-emitting reporter systems Gfp and LuxAB. J Microbiol Methods 41(3):185-194.
31. Landry BP, Stockel J, Pakrasi HB. 2013. Use of Degradation Tags To Control Protein Levels in the Cyanobacterium Synechocystis sp. Strain PCC 6803. Appl Environ Microbiol 79(8):2833-2835.
32. Lou C, Stanton B, Chen Y-J, Munsky B, Voigt CA. 2012. Ribozyme-based insulator parts buffer synthetic circuits from genetic context. Nat Biotech 30(11):1137-1142.
33. Maier T, Guell M, Serrano L. 2009. Correlation of mRNA and protein in complex biological samples. FEBS Lett 583(24):3966-3973.
34. Markley AL, Begemann MB, Clarke RE, Gordon GC, Pfleger BF. 2014. Synthetic Biology Toolbox for Controlling Gene Expression in the Cyanobacterium Synechococcus sp. strain PCC 7002. ACS Synth Biol.
35. Mitschke J, Georg J, Scholz I, Sharma CM, Dienst D, Bantscheff J, Voss B, Steglich C, Wilde A, Vogel J. 2011. An experimentally anchored map of transcriptional start sites in the model cyanobacterium Synechocystis sp. P CC6803. Proc Natl Acad Sci USA 108(5):2124-2129.
36. Mohamed A, Eriksson J, Osiewacz HD, Jansson C. 1993. Differential expression of the psbA genes in the cyanobacterium Synechocystis 6803. Mol Gen Genet 238(1-2)):161-168.
37. Moon TS, Lou C, Tamsir A, Stanton BC, Voigt CA. 2012. Genetic programs constructed from layered logic gates in single cells. Nature 491(7423):249-253.
38. Mukherjee A, Weyant KB, Walker J, Schroeder CM. 2012. Directed evolution of bright mutants of an oxygen-independent flavin-binding fluorescent protein from Pseudomonas putida. J Biol Eng 6(1):20.
39. Oliver JW, Machado IM, Yoneda H, Atsumi S. 2013. Cyanobacterial conversion of carbon dioxide to 2, 3-butanediol. Proc Natl Acad Sci USA 110(4):1249-1254.
40. Oliver JWK, Atsumi S. 2014. Metabolic design for cyanobacterial chemical synthesis. Photosynth Res 120(3):249-261.
41. Pinto F, Pacheco CC, Ferreira D, Moradas-Ferreira P, Tamagnini P. 2012. Selection of suitable reference genes for RT-qPCR analyses in cyanobacteria. PLoS ONE 7(4):e34983.
42. Pitt FD, Mazard S, Humphreys L, Scanlan DJ. 2010. Functional characterization of synechocystis sp. strain PCC 6803 pst1 and pst2 gene clusters reveals a novel strategy for phosphate uptake in a freshwater cyanobacterium. J Bacteriol 192(13):3512-3523.
43. Rubio LM, Ludden PW. 2005. Maturation of nitrogenase: A biochemical puzzle. J Bacteriol 187(2):405-414.
44. Salis HM, Mirsky EA, Voigt CA. 2009. Automated design of synthetic ribosome binding sites to control protein expression. Nat Biotechnol 27(10):946-950.
45. Schyns G, Jia L, Coursin T, Tandeau de Marsac N, Houmard J. 1998. Promoter recognition by a cyanobacterial RNA polymerase: In vitro studies with the Calothrix sp. PCC 7601 transcriptional factors RcaA and RcaD. Plant Mol Biol 36(5):649-659.
46. 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. Proc Natl Acad Sci USA 105(16):6156-6161.
47. Summerfield TC, Nagarajan S, Sherman LA. 2011. Gene expression under low-oxygen conditions in the cyanobacterium Synechocystis sp. PCC 6803 demonstrates Hik31-dependent and -independent responses. Microbiology 157(Pt 2):301-312.
48. Taton A, Unglaub F, Wright NE, Zeng WY, Paz-Yepes J, Brahamsha B, Palenik B, Peterson TC, Haerizadeh F, Golden SS. 2014. Broad-host-range vector system for synthetic biology and biotechnology in cyanobacteria. Nucleic Acids Res 42(17):e136.
49. Varman AM, Xiao Y, Pakrasi HB, Tang YJ. 2013a. Metabolic engineering of Synechocystis sp. strain PCC 6803 for isobutanol production. Appl Environ Microbiol 79(3):908-914.
50. Varman AM, Yu Y, You L, Tang YJ. 2013b. Photoautotrophic production of D-lactic acid in an engineered cyanobacterium. Microb Cell Fact 12:117.
51. Viola S, Ruhle T, Leister D. 2014. A single vector-based strategy for marker-less gene replacement in Synechocystis sp. PCC 6803. Microb Cell Fact 13:4.
52. Wang B, Pugh S, Nielsen DR, Zhang W, Meldrum DR. 2013. Engineering cyanobacteria for photosynthetic production of 3-hydroxybutyrate directly from CO2. Metab Eng 16:68-77.
53. Welsh EA, Liberton M, Stockel J, Loh T, Elvitigala T, Wang C, Wollam A, Fulton RS, Clifton SW, Jacobs JM. 2008. The genome of Cyanothece 51142, a unicellular diazotrophic cyanobacterium important in the marine nitrogen cycle. Proc Natl Acad Sci USA 105(39):15094-15099.
54. Willems E, Leyns L, Vandesompele J. 2008. Standardization of real-time PCR gene expression data from independent biological replicates. Anal Biochem 379(1):127-129.
55. Yang F, Moss LG, Phillips GN, Jr. 1996. The molecular structure of green fluorescent protein. Nat Biotechnol 14(10):1246-1251.
56. Yu Y, You L, Liu D, Hollinshead W, Tang YJ, Zhang F. 2013. Development of Synechocystis sp. PCC 6803 as a phototrophic cell factory. Marine Drugs 11(8):2894-2916.
57. Zang X, Liu B, Liu S, Arunakumara KK, Zhang X. 2007. Optimum conditions for transformation of Synechocystis sp. PCC 6803. J Microbiol 45(3):241-245.