Effects of overexpressing photosynthetic carbon flux control enzymes in the cyanobacterium Synechocystis PCC 6803

Metabolic Engineering

Volumn 38, Issue , 2016, Pages 56-64

  Liang, Feiyan ^a   Lindblad, Peter ^a  

^a UPPSALA UNIVERSITY   (Sweden)

Author keywords

CcmM; FBA; RuBisCO; SBPase; Synechocystis PCC 6803; TK

Indexed keywords

BIOMASS; CARBON DIOXIDE; ENZYMES; LIGHT; PHOTONS;

BIOMASS ACCUMULATION; CCMM; CYANOBACTERIUM SYNECHOCYSTIS; FRUCTOSE BISPHOSPHATE ALDOLASE; POTENTIAL TARGETS; RUBISCO; SBPASE; SYNECHOCYSTIS PCC 6803;

ECOLOGY;

BACTERIAL ENZYME; CHLOROPHYLL A; FRUCTOSE BISPHOSPHATE ALDOLASE; RIBULOSEBISPHOSPHATE CARBOXYLASE; SEDOHEPTULOSE 1,7 BIPHOSPHATASE; TRANSKETOLASE; UNCLASSIFIED DRUG; CARBON; ENZYME;

ARTICLE; BIOMASS; CARBON METABOLISM; CONJUGATION; CONTROLLED STUDY; GENE OVEREXPRESSION; GENETIC ENGINEERING; NONHUMAN; OXYGEN EVOLUTION; PHENOTYPE; PHOTON; PHOTOSYNTHESIS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SYNECHOCYSTIS; CELL PROLIFERATION; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; LIGHT; METABOLIC ENGINEERING; METABOLIC FLUX ANALYSIS; METABOLISM; PHYSIOLOGY; PROCEDURES; RADIATION RESPONSE; UPREGULATION;

CARBON; CELL PROLIFERATION; ENZYMES; GENE EXPRESSION REGULATION, BACTERIAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; LIGHT; METABOLIC ENGINEERING; METABOLIC FLUX ANALYSIS; METABOLIC NETWORKS AND PATHWAYS; PHOTOSYNTHESIS; SYNECHOCYSTIS; UP-REGULATION;

EID: 84976449618     PISSN: 10967176     EISSN: 10967184     Source Type: Journal    
DOI: 10.1016/j.ymben.2016.06.005     Document Type: Article

References (46)

1. Atsumi S., Higashide W., Liao J.C. Direct photosynthetic recycling of carbon dioxide to isobutyraldehyde. Nat. Biotechnol. 2009, 27:1177-1180.
2. 2 concentrating mechanism. J. Exp. Bot. 2006, 57:249-265.
3. Bi H., Wang M., Dong X., Ai X. Cloning and expression analysis of transketolase gene in Cucumis sativus L. Plant Physiol. Biochem. 2013, 70:512-521.
4. Cameron J.C., Wilson S.C., Bernstein S.L., Kerfeld C.A. Biogenesis of a bacterial organelle: the carboxysome assembly pathway. Cell 2013, 155:1131-1140.
5. Durall C., Lindblad P. Mechanisms of carbon fixation and engineering for increased carbon fixation in cyanobacteria. Algal Res. 2015, 11:263-270.
6. Durall C., Rukminasari N., Lindblad P. Enhanced growth at low light intensity in the cyanobacterium Synechocystis PCC 6803 by overexpressing phosphenolpyruvate carboxylase. Algal Res. 2016, 16:275-281.
7. Ellis R.J. The most abundant protein in the world. Trends Biochem. Sci. 1979, 4:241-244.
8. Espie G.S., Kimber M.S. Carboxysomes: cyanobacterial RubisCO comes in small packages. Photosynth. Res. 2011, 109:7-20.
9. 2 assimilation in leaves of C3 species. Planta 1980, 149:78-90.
10. Greene D.N., Whitney S.M., Matsumura I. Artificially evolved Synechococcus PCC6301 Rubisco variants exhibit improvements in folding and catalytic efficiency. Biochem. J. 2007, 404:517-524.
11. Haake V., Geiger M., Walch-Liu P., Of Engels C., Zrenner R., Stitt M. Changes in aldolase activity in wildtype potato plants are important for acclimation to growth irradiance and carbon dioxide concentration, because plastid aldolase exerts control over the ambient rate of photosynthesis across a range of growth conditions. Plant J. 1999, 17:479-489.
12. Haake V., Zrenner R., Sonnewald U., Stitt M. A moderate decrease of plastid aldolase activity inhibits photosynthesis, alters the levels of sugars and starch, and inhibits growth of potato plants. Plant J. 1998, 14:147-157.
13. Henkes S., Sonnewald U., Badur R., Flachmann R., Stitt M. A small decrease of plastid transketolase activity in antisense tobacco transformants has dramatic effects on photosynthesis and phenylpropanoid metabolism. Plant Cell 2001, 13:535-551.
14. Huang H.-H., Camsund D., Lindblad P., Heidorn T. Design and characterization of molecular tools for a synthetic biology approach towards developing cyanobacterial biotechnology. Nucl. Acids Res. 2010, 38:2577-25793.
15. Hudson G.S., Evans J.R., von Caemmerer S., Arvidsson Y.B., Andrews T.J. Reduction of ribulose-1, 5-bisphosphate carboxylase/oxygenase content by antisense RNA reduces photosynthesis in transgenic tobacco plants. Plant Physiol. 1992, 98:294-302.
16. Ivleva N.B., Golden S.S. Protein Extraction, Fractionation, and Purification from Cyanobacteria. Circadian Rhythms 2007, 365-373. Humana Press Inc., Totowa NJ, USA.
17. Iwaki T., Haranoh K., Inoue N., Kojima K., Satoh R., Nishino T., Wada S., Ihara H., Tsuyama S., Kobayashi H., Wadano A. 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. 2006, 88:287-297.
18. Kaneko T., Sato S., Kotani H., Tanaka A., Asamizu E., Nakamura Y., Miyajima N., Hirosawa M., Sugiura M., Sasamoto S., Kimura T., Hosouchi T., Matsuno A., Muraki A., Nakazaki N., Naruo K., Okumura S., Shimpo S., Takeuchi C., Wada T., Watanabe A., Yamada M., Yasuda M., Tabata S. Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res. 1996, 3:109-136.
19. Khozaei M., Fisk S., Lawson T., Gibon Y., Sulpice R., Stitt M., Lefebvre S.C., Raines C.A. Overexpression of plastid transketolase in tobacco results in a thiamine auxotrophic phenotype. Plant Cell 2015, 27:432-447.
20. Kochetov G. Functional flexibility of the transketolase molecule. Biochemistry 2001, 66:1077-1085.
21. Lefebvre S., Lawson T., Zakhleniuk O.V., Lloyd J.C., Raines C.A. Increased sedoheptulose-1,7-bisphosphatase activity in transgenic tobacco plants stimulates photosynthesis and growth from an early stage in development. Plant Physiol. 2005, 138:451-460.
22. Lin M.T., Occhialini A., Andralojc P.J., Parry M.A., Hanson M.R. A faster Rubisco with potential to increase photosynthesis in crops. Nature 2014, 513:547-550.
23. Ma W., Shi D., Wang Q., Wei L., Chen H. Exogenous expression of the wheat chloroplastic fructose-1,6-bisphosphatase gene enhances photosynthesis in the transgenic cyanobacterium, Anabaena PCC7120. J. Appl. Phycol. 2005, 17:273-280.
24. Maurady A., Zdanov A., de Moissac D., Beaudry D., Sygusch J. A conserved glutamate residue exhibits multifunctional catalytic roles in d-fructose-1, 6-bisphosphate aldolases. J. Biol. Chem. 2002, 277:9474-9483.
25. Miyagawa Y., Tamoi M., Shigeoka S. Overexpression of a cyanobacterial fructose-1, 6-/sedoheptulose-1, 7-bisphosphatase in tobacco enhances photosynthesis and growth. Nat. Biotechnol. 2001, 19:965-969.
26. Nakahara K., Yamamoto H., Miyake C., Yokota A. Purification and characterization of class-I and class-II fructose-1, 6-bisphosphate aldolases from the cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol. 2003, 44:326-333.
27. Ogawa T., Tamoi M., Kimura A., Mine A., Sakuyama H., Yoshida E., Maruta T., Suzuki K., Ishikawa, Shigeoka S. Enhancement of photosynthetic capacity in Euglena gracilis by expression of cyanobacterial fructose-1,6-/sedoheptulose-1,7-bisphosphatase leads to increases in biomass and wax ester production. Biotechnol. Biofuels 2015, 8:80.
28. Quick W., Schurr U., Fichtner K., Schulze E., Rodermel S.R., Bogorad L., Stitt M. The impact of decreased Rubisco on photosynthesis, growth, allocation and storage in tobacco plants which have been transformed with antisense rbcS. Plant J. 1991, 1:51-58.
29. Raines C.A. The Calvin cycle revisited. Photosynth. Res. 2003, 75:1-10.
30. Raines C.A. Increasing photosynthetic carbon assimilation in C3 plants to improve crop yield: current and future strategies. Plant Physiol. 2011, 155:36-42.
31. Reinfelder J.R. Carbon concentrating mechanisms in eukaryotic marine phytoplankton. Mar. Sci. 2011, 3.
32. Rosenthal D.M., Locke A.M., Khozaei M., Raines C.A., Long S.P. Over-expressing the C(3) photosynthesis cycle enzyme Sedoheptulose-1-7 bisphosphatase improves photosynthetic carbon gain and yield under fully open air CO(2) fumigation (FACE). BMC Plant Biol. 2011, 11:123.
33. Ruffing A.M. Improved free fatty acid production in cyanobacteria with Synechococcus sp. PCC 7002 as host. Front. Bioeng. Biotechnol. 2014, 2:17.
34. Sanderson K. Lignocellulose: a chewy problem. Nature 2011, 474:S12-S14.
35. Stanier R., Kunisawa R., Mandel M., Cohen-Bazire G. Purification and properties of unicellular blue-green algae (order Chroococcales). Bacteriol. Rev. 1971, 35:171.
36. Stec B. Structural mechanism of RuBisCO activation by carbamylation of the active site lysine. Proc. Nat. Acad. Sci. USA 2012, 109:18785-18790.
37. 2 levels and their potential significance for carbon flow in photosynthetic cells. Plant Cell Environ. 1991, 14:741-762.
38. Stitt M., Schulze D. Does Rubisco control the rate of photosynthesis and plant growth? An exercise in molecular ecophysiology. Plant Cell Environ. 1994, 17:465-487.
39. Tamoi M., Nagaoka M., Miyagawa Y., Shigeoka S. Contribution of fructose-1,6-bisphosphatase and sedoheptulose-1,7-bisphosphatase to the photosynthetic rate and carbon flow in the Calvin cycle in transgenic plants. Plant Cell Physiol. 2006, 47:380-390.
40. Tamoi M., Takeda T., Shigeoka S. Functional analysis of fructose-1, 6-bisphosphatase isozymes (fbp-I and fbp-II gene products) in cyanobacteria. Plant Cell Physiol. 1999, 40:257-261.
41. Tcherkez G.G., Farquhar G.D., Andrews T.J. Despite slow catalysis and confused substrate specificity, all ribulose bisphosphate carboxylases may be nearly perfectly optimized. Proc. Nat. Acad. Sci. USA 2006, 103:7246-7251.
42. Uematsu K., Suzuki N., Iwamae T., Inui M., Yukawa H. Increased fructose 1, 6-bisphosphate aldolase in plastids enhances growth and photosynthesis of tobacco plants. J. Exp. Bot. 2012, 63:3001-3009.
43. Von Caemmerer S. Biochemical Models of Leaf Photosynthesis 2000, Csiro Publishing, Collingwood VIC, Australia.
44. 2-sequestering enzyme, Rubisco. Plant Physiol. 2011, 155:27-35.
45. Willige B.C., Kutzer M., Tebartz F., Bartels D. Subcellular localization and enzymatic properties of differentially expressed transketolase genes isolated from the desiccation tolerant resurrection plant Craterostigma plantagineum. Planta 2009, 229:659-666.
46. Zhu X.G., de Sturler E., Long S.P. Optimizing the distribution of resources between enzymes of carbon metabolism can dramatically increase photosynthetic rate: a numerical simulation using an evolutionary algorithm. Plant Physiol. 2007, 145:513-526.