Evaluating Light-Induced Promoters for the Control of Heterologous Gene Expression in Synechocystis sp. PCC 6803

Biotechnology Progress

Volumn 33, Issue 1, 2017, Pages 45-53

  Albers, Stevan C ^a   Peebles, Christie A M ^a,b  

^a Department of Environmental and Radiological Health Sciences   (United States)

^b Engineering Research Center and Hydraulics Laboratory   (United States)

Author keywords

cyanobacteria; diel cycle; heterologous gene expression; light induced control elements; metabolic engineering

Indexed keywords

METABOLIC ENGINEERING; NUCLEOTIDES;

AMERICAN INSTITUTE OF CHEMICAL ENGINEERS; CONTROL ELEMENTS; CYANOBACTERIA; DIEL CYCLES; GENOMIC LOCATIONS; HETEROLOGOUS GENE EXPRESSIONS; NUCLEOTIDE MUTATION; SYNECHOCYSTIS SP. PCC 6803;

GENE EXPRESSION;

GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIGHT; MUTATION; PHOTOPERIODICITY; PHOTOSYNTHESIS; PROMOTER REGION; RADIATION RESPONSE; REPORTER GENE; SYNECHOCYSTIS;

GENE EXPRESSION REGULATION, BACTERIAL; GENES, REPORTER; LIGHT; MUTATION; PHOTOPERIOD; PHOTOSYNTHESIS; PROMOTER REGIONS, GENETIC; SYNECHOCYSTIS; TRANSCRIPTION, GENETIC;

EID: 85006051893     PISSN: 87567938     EISSN: 15206033     Source Type: Journal    
DOI: 10.1002/btpr.2396     Document Type: Article

References (55)

1. Meier-Kolthoff J, Hahnke R, Petersen J, Scheuner C, Michael V, Fiebig A, Rohde C, Rohde M, Fartmann B, Goodwin L, Chertkov O, Reddy T, Pati A, Ivanova N, Markowitz V, Kyrpides N, Woyke T, Goker M, Klenk HP. Complete genome sequence of DSM 30083T, the type strain (U5/41T) of Escherichia coli, and a proposal for delineating subspecies in microbial taxonomy. Standards in Genom Sci 2014; 9:2.
2. Summerfield TC, Sherman LA. Role of sigma factors in controlling global gene expression in light/dark transitions in the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol 2007; 189:7829–7840.
3. Osanai T, Azuma M, Tanaka K. Sugar catabolism regulated by light- and nitrogen-status in the cyanobacterium Synechocystis sp. PCC 6803. Photochem Photobiol Sci 2007; 6:508–514.
4. Scanlan DJ, Sundaram S, Newman J, Mann NH, Carr NG. Characterization of a zwf mutant of Synechococcus sp. strain PCC 7942. J Bacteriol 1995; 177:2550–2553.
5. Suzuki E, Ohkawa H, Moriya K, Matsubara T, Nagaike Y, Iwasaki I, Fujiwara S, Tsuzuki M, Nakamura Y. Carbohydrate metabolism in mutants of the cyanobacterium Synechococcus elongatus PCC 7942 defective in glycogen synthesis. Appl Environ Microbiol 2010; 76:3153–3159.
6. Aro EM, Virgin I, Andersson B. Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1993; 1143:113–134.
7. Takahashi S, Murata N. How do environmental stresses accelerate photoinhibition?. Trends in Plant Sci 2008; 13:178–182.
8. Tyystjarvi T, Aro Em Fau - Jansson C, Jansson C, Fau-Maenpaa P, Maenpaa P. Changes of amino acid sequence in PEST-like area and QEEET motif affect degradation rate of D1 polypeptide in photosystem II. J Plant Mol Biol 1994; 25:517–526. 0167-4412 (Print),
9. Tyystjärvi T, Herranen M, Aro EM. Regulation of translation elongation in cyanobacteria: Membrane targeting of the ribosome nascent-chain complexes controls the synthesis of D1 protein. Mol Microbiol 2001; 40:476–484.
10. Mohamed A, Eriksson J, Fau - Osiewacz HD, Osiewacz Hd Fau - Jansson C, Jansson C. Differential expression of the psbA genes in the cyanobacterium Synechocystis 6803. Mol Genet Genom 1993; 238:(0026-8925 (Print)), 161–168.
11. Mohamed A, Jansson C. Influence of light on accumulation of photosynthesis-specific transcripts in the cyanobacterium Synechocystis 6803. Plant Mol Biol 1989; 13:693–700.
12. Mulo P, Laakso S, Mäenpää P, Aro EM. Stepwise photoinhibition of photosystem II studies with Synechocystis species PCC 6803 mutants with a modified DE loop of the reaction center polypeptide D1. Plant Physiol 1998; 117:483–490.
13. Osiewacz HD, McIntosh L. Nucleotide sequence of a member of the psbA multigene family from the unicellular cyanobacterium Synechocystis 6803. Nucleic Acid Res 1987; 15:10585.
14. Salih GF, Jansson C. Activation of the silent psbA1 gene in the cyanobacterium Synechocystis sp strain 6803 produces a novel and functional D1 protein. Plant Cell 1997; 9:869–878. United States, Vol. pp
15. Bouyoub A, Vernotte C, Astier C. Functional analysis of the two homologous psbA gene copies in Synechocystis PCC 6714 and PCC 6803. Plant Mol Biol 1993; 21:249–258.
16. Tyystjarvi T, Tuominen I, Herranen M, Aro EM, Tyystjarvi E. Action spectrum of psbA gene transcription is similar to that of photoinhibition in Synechocystis sp. PCC 6803. FEBS Lett 2002; 516:167–171. Netherlands, Vol. pp
17. Herranen M, Aro EM, Tyystjarvi T. Two distinct mechanisms regulate the transcription of photosystem II genes in Synechocystis sp. PCC 6803. Physiol Plant 2001; 112:531–539. Vol. pp
18. Bentley FK, Zurbriggen A, Melis A. Heterologous expression of the mevalonic acid pathway in cyanobacteria enhances endogenous carbon partitioning to isoprene. Mol Plant 2014; 7:71–86. England, Vol. pp
19. Englund E, Andersen-Ranberg J, Miao R, Hamberger B, Lindberg P. Metabolic engineering of Synechocystis sp. PCC 6803 for production of the plant diterpenoid manoyl oxide. ACS Synth Biol 2015; 4:1270–1278.
20. Formighieri C, Melis A. Regulation of β-phellandrene synthase gene expression, recombinant protein accumulation, and monoterpene hydrocarbons production in Synechocystis transformants. Planta 2014; 240:309–324.
21. Lagarde D, Beuf L, Vermaas W. Increased production of zeaxanthin and other pigments by application of genetic engineering techniques to Synechocystis sp. Strain PCC 6803. Appl Environ Microbiol 2000; 66:64–72.
22. Stanier RY, Kunisawa R, Mandel M, Cohen-Bazire G. Purification and properties of unicellular blue-green algae (order Chroococcales). Bacteriol Rev 1971; 35:171–205.
23. Kunert A, Hagemann M, Erdmann N. Construction of promoter probe vectors for Synechocystis sp. PCC 6803 using the light-emitting reporter systems Gfp and LuxAB. J Microbiol Methods 2000; 41:185–194.
24. Cheah YE, Albers SC, Peebles CAM. A novel counter-selection method for markerless genetic modification in Synechocystis sp. PCC 6803. Biotechnol Prog 2013; 29:23–30.
25. Chiu J, March PE, Lee R, Tillett D. Site-directed, ligase-independent mutagenesis (SLIM): A single-tube methodology approaching 100% efficiency in 4 h. Nucleic Acids Res 2004; 32:e174–e174.
26. Cormack BP, Valdivia RH, Falkow S. FACS-optimized mutants of the green fluorescent protein (GFP). Gene 1996; 173:33–38.
27. Andersen JB, Sternberg C, Poulsen LK, Bjørn SP, Givskov M, Molin S. New unstable variants of green fluorescent protein for studies of transient gene expression in bacteria. Appl Environ Microbiol 1998; 64:2240–2246.
28. Gibson DG, Smith HO, Hutchison CA, Venter JC, Merryman C. Chemical synthesis of the mouse mitochondrial genome. Nat Meth 2010; 7:901–903.
29. Nakamoto H, Suzuki M, Kojima K. Targeted inactivation of the hrcA repressor gene in cyanobacteria. FEBS Lett 2003; 549:57–62.
30. Kojima K, Nakamoto H. A novel light- and heat-responsive regulation of the groE transcription in the absence of HrcA or CIRCE in cyanobacteria. Febs Lett 2007; 581:1871–1880.
31. Dühring U, Irrgang KD, Lünser K, Kehr J, Wilde A. Analysis of photosynthetic complexes from a cyanobacterial ycf37 mutant. Biochim Biophys Acta 2006; 1757:3–11.
32. Pinto FL, Thapper A, Sontheim W, Lindblad P. Analysis of current and alternative phenol based RNA extraction methodologies for cyanobacteria. BMC Mol Biol 2009; 10:79. England, Vol. p
33. Peebles CAM, Hughes EH, Shanks JV, San KY. Transcriptional response of the terpenoid indole alkaloid pathway to the overexpression of ORCA3 along with jasmonic acid elicitation of Catharanthus roseus hairy roots over time. Metabol Eng 2009; 11:76–86.
34. Huang HH, Camsund D, Lindblad P, Heidorn T. Design and characterization of molecular tools for a Synthetic Biology approach towards developing cyanobacterial biotechnology. Nucleic Acids Res 2010; 38:2577–2593.
35. Huang HH, Lindblad P. Wide-dynamic-range promoters engineered for cyanobacteria. J Biol Eng 2013; 7:10.
36. Eriksson J, Salih GF, Ghebramedhin H, Jansson C. Deletion mutagenesis of the 5' psbA2 region in Synechocystis 6803: Identification of a putative cis element involved in photoregulation. Mol Cell Biol Res Commun 2000;3:292–298.
37. Glatz A, Horvath I, Varvasovszki V, Kovacs E, Torok Z, Vigh L. Chaperonin genes of the Synechocystis PCC 6803 are differentially regulated under light-dark transition during heat stress. Biochem Biophys Res Commun 1997; 239:291–297.
38. Imamura S, Asayama M, Takahashi H, Tanaka K, Takahashi H, Shirai M. Antagonistic dark/light-induced SigB/SigD, group 2 sigma factors, expression through redox potential and their roles in cyanobacteria. FEBS Lett 2003; 554:357–362.
39. Imamura S, Yoshihara S, Nakano S, Shiozaki N, Yamada A, Tanaka K, Takahashi H, Asayama M, Shirai M. Purification, characterization, and gene expression of all sigma factors of RNA polymerase in a cyanobacterium. J Mol Biol 2003; 325:857–872.
40. Sobczyk A, Schyns G, Tandeau de Marsac N, Houmard J. Transduction of the light signal during complementary chromatic adaptation in the cyanobacterium Calothrix sp. PCC 7601: DNA-binding proteins and modulation by phosphorylation. EMBO J 1993; 12:997–1004.
41. Sobczyk A, Bely A, de Marsac NT, Houmard J. A phosphorylated DNA-binding protein is specific for the red-light signal during complementary chromatic adaptation in cyanobacteria. Mol Microbiol 1994; 13:875–885.
42. Muramatsu M, Hihara Y. Characterization of high-light-responsive promoters of the psaAB genes in Synechocystis sp. PCC 6803. Plant Cell Physiol 2006; 47:878–890. Japan, Vol. pp
43. Muramatsu M, Hihara Y. Coordinated high-light response of genes encoding subunits of photosystem I is achieved by AT-rich upstream sequences in the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol 2007; 189:2750–2758. United States, Vol. pp
44. Seino Y, Takahashi T, Hihara Y. The response regulator RpaB binds to the upstream element of photosystem I genes to work for positive regulation under low-light conditions in Synechocystis sp. Strain PCC 6803. J Bacteriol 2009; 191:1581–1586.
45. Pinto F, Pacheco CC, Ferreira D, Moradas-Ferreira P, Tamagnini P. Selection of suitable reference genes for RT-qPCR analyses in cyanobacteria. PLoS One 2012; 7:e34983. United States, Vol. p
46. Albers SC, Gallegos VA, Peebles CA. Engineering of genetic control tools in Synechocystis sp. PCC 6803 using rational design techniques. J Biotechnol 2015; 216:36–46.
47. Smith GR. DNA supercoiling: Another level for regulating gene expression. Cell 1981; 24:599–600.
48. Hatfield GW, Benham CJ. DNA topology-mediated control of global gene expression in Escherichia coli. Annu Rev Genet 2002; 36:175–203.
49. Dorman CJ. DNA supercoiling and environmental regulation of gene expression in pathogenic bacteria. Infect Immun 1991; 59:745–749.
50. Vijayan V, Zuzow R, O'Shea EK. Oscillations in supercoiling drive circadian gene expression in cyanobacteria. Proc Natl Acad Sci USA 2009; 106:22564–22568.
51. Prakash JSS, Sinetova M, Zorina A, Kupriyanova E, Suzuki I, Murata N, Los DA. DNA supercoiling regulates the stress-inducible expression of genes in the cyanobacterium Synechocystis. Mol BioSyst 2009; 5:1904–1912.
52. Zorina AA, Mironov KS, Stepanchenko NS, Sinetova MA, Koroban NV, Zinchenko VV, Kupriyanova EV, Allakhverdiev SI, Los DA. Regulation systems for stress responses in cyanobacteria. Russ J Plant Physiol 2011; 58:749–767.
53. Gourse RL, Ross W, Gaal T. UPs and downs in bacterial transcription initiation: The role of the alpha subunit of RNA polymerase in promoter recognition. Mol Microbiol 2000; 37:687–695.
54. Shibato J, Agrawal GK, Kato H, Asayama M, Shirai M. The 5'-upstream cis-acting sequences of a cyanobacterial psbA gene: Analysis of their roles in basal, light-dependent and circadian transcription. Mol Genet Genomics 2002; 267:684–694.
55. Igarashi K, Ishihama A. Bipartite functional map of the E. coli RNA polymerase alpha subunit: Involvement of the C-terminal region in transcription activation by cAMP-CRP. Cell 1991;65:1015–1022.