Regulation of β-phellandrene synthase gene expression, recombinant protein accumulation, and monoterpene hydrocarbons production in Synechocystis transformants

Planta

Volumn 240, Issue 2, 2014, Pages 309-324

  Formighieri, Cinzia ^a   Melis, Anastasios ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Biofuels; Cpc; Cyanobacteria; Photosynthesis; Ptrc; Terpene synthesis

Indexed keywords

CYANOBACTERIA; ESCHERICHIA COLI; SYNECHOCYSTIS; SYNECHOCYSTIS SP.;

RECOMBINANT PROTEIN; TERPENE; TERPENE SYNTHASE; TRANSFERASE;

ENZYMOLOGY; GENETICS; METABOLISM; SYNECHOCYSTIS;

ALKYL AND ARYL TRANSFERASES; MONOTERPENES; RECOMBINANT PROTEINS; SYNECHOCYSTIS;

EID: 84904980499     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-014-2080-8     Document Type: Article

References (68)

1. Adir N (2005) Elucidation of the molecular structures of components of the phycobilisome: reconstructing a giant. Photosynth Res 85: 15-32.
2. Amann E, Ochs B, Abel KJ (1988) Tightly regulated tac promoter vectors useful for the expression of unfused and fused protein in Escherichia coli. Gene 69: 301-315.
3. Angermayr SA, Paszota M, Hellingwerf KJ (2012) Engineering a cyanobacterial cell factory for production of lactic acid. Appl Environ Microb 78: 7098-7106.
4. Atsumi S, Higashide W, Liao JC (2009) Direct photosynthetic recycling of carbon dioxide to isobutyraldehyde. Nat Biotechnol 27: 1177-1180.
5. Bailey S, Grossman A (2008) Photoprotection in cyanobacteria: regulation of light harvesting. Photochem Photobiol 84: 1410-1420.
6. Bentley FK, Melis A (2012) Diffusion-based process for carbon dioxide uptake and isoprene emission in gaseous/aqueous two-phase photobioreactors by photosynthetic microorganisms. Biotechnol Bioeng 109: 100-109.
7. Bentley FK, García-Cerdán JG, Chen HC, Melis A (2013) Paradigm of monoterpene (β-phellandrene) hydrocarbons production via photosynthesis in cyanobacteria. BioEnergy Res 6: 917-929.
8. Bohlmann J, Keeling CI (2008) Terpenoid biomaterials. Plant J 54: 656-669.
9. Booker H, Evans LK, Gillam AE (1940) The effect of molecular environment on the absorption spectra of organic compounds in solution. Part I. Conjugated dienes. J Chem Soc 1453-1463. doi: 10. 1039/JR9400001453.
10. Demissie ZA, Sarker LS, Mahmoud SS (2011) Cloning and functional characterization of β-phellandrene synthase from Lavandula angustifolia. Planta 233: 685-696.
11. Deng MD, Coleman JR (1999) Ethanol synthesis by genetic engineering in cyanobacteria. Appl Environ Microbiol 65: 523-528.
12. Dexter J, Fu P (2009) Metabolic engineering of cyanobacteria for ethanol production. Energy Environ Sci 2: 857.
13. Ducat DC, Avelar-Rivas JA, Way JC, Silver PA (2012) Rerouting carbon flux to enhance photosynthetic productivity. Appl Environ Microbiol 78: 2660-2668.
14. Eaton-Rye JJ (2011) Construction of gene interruptions and gene deletions in the cyanobacterium Synechocystis sp. strain PCC 6803. Methods Mol Biol 684: 295-312.
15. Formighieri C, Franck F, Bassi R (2012) Regulation of the pigment optical density of an algal cell: filling the gap between photosynthetic productivity in the laboratory and in mass culture. J Biotechnol 162: 115-123.
16. Gao Z, Zhao H, Li Z, Tan X, Lu X (2012) Photosynthetic production of ethanol from carbon dioxide in genetically engineered cyanobacteria. Energy Environ Sci 5: 9857.
17. Gershenzon J, Dudareva N (2007) The function of terpene natural products in the natural world. Nat Chem Biol 3: 408-414.
18. Glazer AN, Melis A (1987) Photochemical reaction centers: structure, organization and function. Annu Rev Plant Physiol 38: 11-45.
19. Gross KP, Schnepp O (1978) Absorption and circular dichroism spectra of the cis- and trans- butadiene chromophores α- and β-phellandrene. J Chem Phys 68: 2647-2657.
20. Grossman AR, Schaefer MR, Chiang GG, Collier JL (1993) The phycobilisome, a light-harvesting complex responsive to environmental conditions. Microbiol Rev 57: 725-749.
21. 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: e50470.
22. Hellingwerf KJ, Teixeira de Mattos MJ (2009) Alternative routes to biofuels: light-driven biofuel formation from CO2 and water based on the "photanol" approach. J Biotechnol 142: 87-90.
23. Horie Y, Ito Y, Ono M, Moriwaki N, Kato H, Hamakubo Y, Amano T, Wachi M, Shirai M, Asayama M (2007) Dark-induced mRNA instability involves RNase E/G-type endoribonuclease cleavage at the AU-box and SD sequences in cyanobacteria. Mol Genet Genomics 278: 331-346.
24. 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: 2577-2593.
25. Imashimizu M, Fujiwara S, Tanigawa R, Tanaka K, Hirokawa T, Nakajima Y, Higo J (2003) Thymine at -5 is crucial for cpc promoter activity of Synechocystis sp. strain PCC 6714. J Bacteriol 185: 6477-6480.
26. Jansson C, Salih G, Eriksson J, Wiklund R, Ghebramedhin H (1998) Use of Synechocystis 6803 to study expression of a psbA gene family. Methods Enzymol 297: 166-182.
27. Kirilovsky D, Kerfeld CA (2012) The orange carotenoid protein in photoprotection of photosystem II in cyanobacteria. Biochim Biophys Acta 1817: 158-166.
28. Kuroda H, Maliga P (2001a) Complementarity of the 16S rRNA penultimate stem with sequences downstream of the AUG destabilizes the plastid mRNAs. Nucleic Acids Res 29: 970-975.
29. Kuroda H, Maliga P (2001b) Sequences downstream of the translation initiation codon are important determinants of translation efficiency in chloroplasts. Plant Physiol 125: 430-436.
30. Lan EI, Liao JC (2012) ATP drives direct photosynthetic production of 1-butanol in cyanobacteria. Proc Natl Acad Sci USA 109: 6018-6023.
31. 2 to 1, 2-propanediol. Microb Cell Fact 12: 4.
32. Lichtenthaler HK (2000) Sterols and isoprenoids. Biochem Soc Trans 28: 785-789.
33. Lindberg P, Park S, Melis A (2010) Engineering a platform for photosynthetic isoprene production in cyanobacteria, using Synechocystis as the model organism. Metab Eng 12: 70-79.
34. Liu X, Sheng J, Curtiss R (2011) Fatty acid production in genetically modified cyanobacteria. Proc Natl Acad Sci USA 108: 6899-6904.
35. MacBeth AK, Smith GE, West TF (1938) β-Phellandrene. J Chem Soc 119-123. doi: 10. 1039/JR9380000119.
36. MacColl R (1998) Cyanobacterial phycobilisomes. J Struct Biol 124: 311-334.
37. McNevin D, von Caemmerer S, Graham Farquhar G (2006) Determining RuBisCO activation kinetics and other rate and equilibrium constants by simultaneous multiple non-linear regression of a kinetic model. J Exp Bot 57: 3883-3900.
38. Meeks JK, Castenholz RW (1971) Growth and photosynthesis in an extreme thermophile, Synechococcus lividus (Cyanophyta). Arch Microbiol 78: 25-41.
39. Melis A (1999) Photosystem-II damage and repair cycle in chloroplasts: what modulates the rate of photodamage in vivo?. Trends Plant Sci 4: 130-135.
40. Melis A (2009) Solar energy conversion efficiencies in photosynthesis: minimizing the chlorophyll antennae to maximize efficiency. Plant Sci 177: 272-280.
41. Melis A (2012) Photosynthesis-to-fuels: from sunlight to hydrogen, isoprene, and botryococcene production. Energy Environ Sci 5: 5531-5539.
42. Melis A (2013) Carbon partitioning in photosynthesis. Curr Opin Cheml Biol 17: 453-456.
43. Melis A, Neidhardt J, Benemann JR (1999) Dunaliella salina (Chlorophyta) with small chlorophyll antenna sizes exhibit higher photosynthetic productivities and photon use efficiencies than normally pigmented cells. J Appl Phycol 10: 515-525.
44. Mohamed A, Eriksson J, Osiewacz HD, Jansson C (1993) Differential expression of the psbA genes in the cyanobacterium Synechocystis 6803. Mol Gen Genet 238: 161-168.
45. Mulo P, Sakurai I, Aro EM (2012) Strategies for psbA gene expression in cyanobacteria, green algae and higher plants: from transcription to PSII repair. Biochim Biophys Acta 1817: 247-257.
46. Münch R, Hiller K, Grote A, Scheer M, Klein J, Schobert M, Jahn D (2005) Virtual footprint and PRODORIC: an integrative framework for regulon prediction in prokaryotes. Bioinformatics 21: 4187-4189.
47. Nakajima Y, Ueda R (1997) Improvement of photosynthesis in dense microalgal suspension by reduction of light harvesting pigments. J Appl Phycol 9: 503-510.
48. Nakajima Y, Ueda R (1999) Improvement of microalgal photosynthetic productivity by reducing the content of light harvesting pigment. J Appl Phycol 11: 195-201.
49. Nakajima Y, Fujiwara S, Sawai H, Imashimizu M, Tsuzuki M (2001) A phycocyanin-deficient mutant of Synechocystis PCC 6714 with a single-base substitution upstream of the cpc operon. Plant Cell Physiol 42: 992-998.
50. Nixon P, Jansson C (1996) Cyanobacterial transformation and gene regulation. In: Andersson B, Salter AH, Barber J (eds) Molecular genetics of photosynthesis. Oxford University Press, Oxford, UK, pp 197-224.
51. Oliver JWK, Machado IMP, Yoneda H, Atsumi S (2013) Cyanobacterial conversion of carbon dioxide to 2, 3-butanediol. Proc Natl Acad Sci USA 110: 1249-1254.
52. Peralta-Yahya PP, Ouellet M, Chan R, Mukhopadhyay A, Keasling JD, Lee TS (2011) Identification and microbial production of a terpene-based advanced biofuel. Nat Commun 2: 483.
53. Rakhimberdieva MG, Elanskaya IV, Vermaas WF, Karapetyan NV (2010) Carotenoid-triggered energy dissipation in phycobilisomes of Synechocystis sp. PCC 6803 diverts excitation away from reaction centers of both photosystems. Biochim Biophys Acta 1797: 241-249.
54. Reinsvold RE, Jinkerson RE, Radakovits R, Posewitz MC, Basu C (2011) The production of the sesquiterpene β-caryophyllene in a transgenic strain of the cyanobacterium Synechocystis. J Plant Physiol 168: 848-852.
55. 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.
56. Sasaki K, Ohara K, Yazaki K (2005) Gene expression and characterization of isoprene synthase from Populus alba. FEBS Lett 579: 2514-2518.
57. Sprengart ML, Fuchs E, Porter AG (1996) The downstream box: an efficient and independent translation initiation signal in Escherichia coli. EMBO J 15: 665-674.
58. Takahama K, Matsuoka M, Nagahama K, Ogawa T (2003) Construction and analysis of a recombinant cyanobacterium expressing a chromosomally inserted gene for an ethylene-forming enzyme at the psbAI locus. J Biosci Bioeng 95: 302-305.
59. Tan X, Yao L, Gao Q, Wang W, Qi F, Lu X (2011) Photosynthesis driven conversion of carbon dioxide to fatty alcohols and hydrocarbons in cyanobacteria. Metab Eng 13: 169-176.
60. Tian L, van Stokkum IHM, Koehorst RBM, van Amerongen H (2012) Light harvesting and blue-green light induced non-photochemical quenching in two different c-phycocyanin mutants of Synechocystis PCC 6803. J Phys Chem 117: 11000-11006.
61. van Wagoner RM, Drummond AK, Wright JLC (2007) Biogenetic diversity of cyanobacterial metabolites. Adv Appl Microbiol 61: 89-217.
62. Varman AM, Xiao Y, Pakrasi HB, Tang YJ (2013) Metabolic engineering of Synechocystis sp. strain PCC 6803 for isobutanol production. Appl Environ Microbiol 79: 3908-3914.
63. 2. Metab Eng 16: 68-77.
64. Wijffels RH, Kruse O, Hellingwerf KJ (2013) Potential of industrial biotechnology with cyanobacteria and eukaryotic microalgae. Curr Opin Biotechnol 24: 405-413.
65. Williams JGK (1988) Construction of specific mutations in photosystem II photosynthetic reaction center by genetic engineering methods in Synechocystis 6803. Methods Enzymol 167: 766-778.
66. Wilson A, Ajlani G, Verbavatz JM, Vass I, Kerfeld CA, Kirilovsky D (2006) A soluble carotenoid protein involved in phycobilisome-related energy dissipation in cyanobacteria. Plant Cell 18: 992-1007.
67. 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.
68. Zurbriggen A, Kirst H, Melis A (2012) Isoprene production via the mevalonic acid pathway in Escherichia coli (Bacteria). BioEnergy Res 5: 814-828.