Applied Microbiology and Biotechnology

, Volume 100, Issue 18, pp 7865–7875 | Cite as

The potential of Synechococcus elongatus UTEX 2973 for sugar feedstock production

Biotechnological products and process engineering


It is important to obtain abundant sugar feedstocks economically and sustainably for bio-fermentation industry, especially for producing cheap biofuels and biochemicals. Besides plant biomass, photosynthetic cyanobacteria have also been considered to be potential microbe candidates for sustainable production of carbohydrate feedstocks. As the fastest growing cyanobacterium reported so far, Synechococcus elongatus UTEX 2973 (Syn2973) might have huge potential for bioproduction. In this study, we explored the potentials of this strain as photo-bioreactors for sucrose and glycogen production. Under nitrogen-replete condition, Syn2973 could accumulate glycogen with a rate of 0.75 g L−1 day−1 at the exponential phase and reach a glycogen content as high as 51 % of the dry cell weight (DCW) at the stationary phase. By introducing a sucrose transporter CscB, Syn2973 was endowed with an ability to secrete over 94 % sucrose out of cells under salt stress condition. The highest extracellular sucrose productivity reached 35.5 mg L−1 h−1 for the Syn2973 strain expressing cscB, which contained the similar amounts of intracellular glycogen with the wild type. Potassium chloride was firstly proved to induce sucrose accumulation as well as sodium chloride in Syn2973. By semi-continuous culturing, 8.7 g L−1 sucrose was produced by the cscB-expressing strain of Syn2973 in 21 days. These results support that Syn2973 is a promising candidate with great potential for production of sugars.


Glycogen Sucrose Salt stress Synechococcus elongatus UTEX 2973 



We thank Dr. Cheng Li, Quan Luo, and Yangkai Duan for valuable discussions.

Compliance with ethical standards


This work was supported by the National Science Fund for Distinguished Young Scholars of China (31525002 to X. Lu), the Excellent Youth Award of the Shandong Natural Science Foundation (JQ201306 to X. Lu), the Shandong Taishan Scholarship (X. Lu), the National Science Foundation of China (31301018 to X. Tan), the State Oceanic Administration (SOA) Global Change and Air-Sea Interaction Program (GASI-03-01-02-05 to X. Tan), and the Youth Innovation Promotion Association (X. Tan).

Conflict of interest

The authors declare that they have no competing interests.

Ethical approval

This article does not contain any studies with human participants or animals.

Supplementary material

253_2016_7510_MOESM1_ESM.pdf (276 kb)
ESM 1 (PDF 275 kb)


  1. Aikawa S, Joseph A, Yamada R, Izumi Y, Yamagishi T, Matsuda F, Kawai H, Chang JS, Hasunuma T, Kondo A (2013) Direct conversion of Spirulina to ethanol without pretreatment or enzymatic hydrolysis processes. Energ Environ Sci 6(6):1844–1849. doi: 10.1039/c3ee40305j CrossRefGoogle Scholar
  2. Aikawa S, Nishida A, Ho SH, Chang JS, Hasunuma T, Kondo A (2014) Glycogen production for biofuels by the euryhaline cyanobacteria Synechococcus sp. strain PCC 7002 from an oceanic environment. Biotechnol Biofuels 7:88. doi: 10.1186/1754-6834-7-88 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Allen MM (1984) Cyanobacterial cell inclusions. Ann Rev Microbiol 38(1):1–25. doi: 10.1146/annurev.mi.38.100184.000245 CrossRefGoogle Scholar
  4. Angermayr SA, Rovira AG, Hellingwerf KJ (2015) Metabolic engineering of cyanobacteria for the synthesis of commodity products. Trends Biotechnol 33(6):352–361. doi: 10.1016/j.tibtech.2015.03.009 CrossRefPubMedGoogle Scholar
  5. Balat M, Balat H (2009) Recent trends in global production and utilization of bio-ethanol fuel. Appl Energ 86(11):2273–2282. doi: 10.1016/j.apenergy.2009.03.015 CrossRefGoogle Scholar
  6. Berry S, Esper B, Karandashova I, Teuber M, Elanskaya I, Rogner M, Hagemann M (2003) Potassium uptake in the unicellular cyanobacterium Synechocystis sp. strain PCC 6803 mainly depends on a Ktr-like system encoded by slr1509 (ntpJ). FEBS Lett 548(1–3):53–58. doi: 10.1016/S0014-5793(03)00729-4 CrossRefPubMedGoogle Scholar
  7. Carrieri D, Paddock T, Maness PC, Seibert M, Yu JP (2012) Photo-catalytic conversion of carbon dioxide to organic acids by a recombinant cyanobacterium incapable of glycogen storage. Energ Environ Sci 5(11):9457–9461. doi: 10.1039/c2ee23181f CrossRefGoogle Scholar
  8. Desplats P, Folco E, Salerno GL (2005) Sucrose may play an additional role to that of an osmolyte in Synechocystis sp. PCC 6803 salt-shocked cells. Plant Physiol Biochem 43(2):133–138. doi: 10.1016/j.plaphy.2005.01.008 CrossRefPubMedGoogle Scholar
  9. Du W, Liang F, Duan Y, Tan X, Lu X (2013) Exploring the photosynthetic production capacity of sucrose by cyanobacteria. Metab Eng 19:17–25. doi: 10.1016/j.ymben.2013.05.001 CrossRefPubMedGoogle Scholar
  10. Ducat DC, Avelar-Rivas JA, Way JC, Silver PA (2012) Rerouting carbon flux to enhance photosynthetic productivity. Appl Environ Microbiol 78(8):2660–2668. doi: 10.1128/aem.07901-11 CrossRefPubMedPubMedCentralGoogle Scholar
  11. E4tech, RE-CORD, WUR (2015) From the Sugar Platform to biofuels and biochemicals. Final report for the European Commission:contract No. ENER/C2/423–2012/SI2012.673791.Google Scholar
  12. Elhai J, Wolk CP (1988) Conjugal transfer of DNA to cyanobacteria. Methods Enzymol 167:747–754CrossRefPubMedGoogle Scholar
  13. Graham-Rowe D (2011) Agriculture: beyond food versus fuel. Nature 474(7352):S6–S8. doi: 10.1038/474S06a CrossRefPubMedGoogle Scholar
  14. Grundel M, Scheunemann R, Lockau W, Zilliges Y (2012) Impaired glycogen synthesis causes metabolic overflow reactions and affects stress responses in the cyanobacterium Synechocystis sp. PCC 6803. Microbiology 158(12):3032–3043. doi: 10.1099/mic.0.062950-0 CrossRefPubMedGoogle Scholar
  15. Gupta V, Ratha SK, Sood A, Chaudhary V, Prasanna R (2013) New insights into the biodiversity and applications of cyanobacteria (blue-green algae)—prospects and challenges. Algal Res 2(2):79–97. doi: 10.1016/j.algal.2013.01.006 CrossRefGoogle Scholar
  16. Hagemann M (2011) Molecular biology of cyanobacterial salt acclimation. FEMS Microbiol Rev 35(1):87–123. doi: 10.1111/j.1574-6976.2010.00234.x CrossRefPubMedGoogle Scholar
  17. Hara KY, Araki M, Okai N, Wakai S, Hasunuma T, Kondo A (2014) Development of bio-based fine chemical production through synthetic bioengineering. Microb Cell Factories 13(1):1–19. doi: 10.1186/s12934-014-0173-5 CrossRefGoogle Scholar
  18. Hays SG, Ducat DC (2015) Engineering cyanobacteria as photosynthetic feedstock factories. Photosynthesis Res 123(3):285–295. doi: 10.1007/s11120-014-9980-0 CrossRefGoogle Scholar
  19. Hernandez-Prieto MA, Semeniuk TA, Futschik ME (2014) Toward a systems-level understanding of gene regulatory, protein interaction, and metabolic networks in cyanobacteria. Front Genet 5:191. doi: 10.3389/fgene.2014.00191 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Hickman JW, Kotovic KM, Miller C, Warrener P, Kaiser B, Jurista T, Budde M, Cross F, Roberts JM, Carleton M (2013) Glycogen synthesis is a required component of the nitrogen stress response in Synechococcus elongatus PCC 7942. Algal Res 2(2):98–106. doi: 10.1016/j.algal.2013.01.008 CrossRefGoogle Scholar
  21. Karandashova IV, Elanskaya IV (2005) Genetic control and mechanisms of salt and hyperosmotic stress resistance in cyanobacteria. Russ J Genet 41(12):1311–1321. doi: 10.1007/s11177-006-0001-z CrossRefGoogle Scholar
  22. Klotz A, Reinhold E, Doello S, Forchhammer K (2015) Nitrogen starvation acclimation in Synechococcus elongatus: redox-control and the role of nitrate reduction as an electron sink. Life 5(1):888. doi: 10.3390/life5010888 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Lau N-S, Matsui M, Abdullah AA-A (2015) Cyanobacteria: photoautotrophic microbial factories for the sustainable synthesis of industrial products. Biomed Res Int 2015:9. doi: 10.1155/2015/754934 Google Scholar
  24. Niederholtmeyer H, Wolfstadter BT, Savage DF, Silver PA, Way JC (2010) Engineering cyanobacteria to synthesize and export hydrophilic products. Appl Environ Microbiol 76(11):3462–3466. doi: 10.1128/AEM.00202-10 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Okuhara H, Matsumura T, Fujita Y, Hase T (1999) Cloning and inactivation of genes encoding ferredoxin- and nadh-dependent glutamate synthases in the cyanobacterium Plectonema boryanum. Imbalances in nitrogen and carbon assimilations caused by deficiency of the ferredoxin-dependent enzyme. Plant Physiol 120(1):33–42CrossRefPubMedPubMedCentralGoogle Scholar
  26. Peralta-Yahya PP, Zhang F, del Cardayre SB, Keasling JD (2012) Microbial engineering for the production of advanced biofuels. Nature 488(7411):320–328. doi: 10.1038/nature11478 CrossRefPubMedGoogle Scholar
  27. Sarkar D, Shimizu K (2015) An overview on biofuel and biochemical production by photosynthetic microorganisms with understanding of the metabolism and by metabolic engineering together with efficient cultivation and downstream processing. Bioresour Bioprocess 2(1):17. doi: 10.1186/s40643-015-0045-9 CrossRefGoogle Scholar
  28. Stanier RY, Kunisawa R, Mandel M, Cohen-Bazire G (1971) Purification and properties of unicellular blue-green algae (order Chroococcales). Bacteriol Rev 35(2):171–205PubMedPubMedCentralGoogle Scholar
  29. Suzuki E, Ohkawa H, Moriya K, Matsubara T, Nagaike Y, Iwasaki I, Fujiwara S, Tsuzuki M, Nakamura Y (2010) Carbohydrate metabolism in mutants of the cyanobacterium Synechococcus elongatus PCC 7942 defective in glycogen synthesis. Appl Environ Microbiol 76(10):3153–3159. doi: 10.1128/aem.00397-08 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Tan X, Du W, Lu X (2015) Photosynthetic and extracellular production of glucosylglycerol by genetically engineered and gel-encapsulated cyanobacteria. Appl Microbiol Biotechnol 99(5):2147–2154. doi: 10.1007/s00253-014-6273-7 CrossRefPubMedGoogle Scholar
  31. Wolk CP, Ernst A, Elhai J (1994) Heterocyst metabolism and development. In: Bryant AD (ed) The molecular biology of cyanobacteria. Springer, Netherlands, pp. 769–823CrossRefGoogle Scholar
  32. Xu Y, Guerra LT, Li Z, Ludwig M, Dismukes GC, Bryant DA (2013) Altered carbohydrate metabolism in glycogen synthase mutants of Synechococcus sp. strain PCC 7002: cell factories for soluble sugars. Metab Eng 16:56–67. doi: 10.1016/j.ymben.2012.12.002 CrossRefPubMedGoogle Scholar
  33. 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 CO(2). Sci Rep 5:8132. doi: 10.1038/srep08132 CrossRefPubMedGoogle Scholar
  34. Zhou J, Li Y (2010) Engineering cyanobacteria for fuels and chemicals production. Protein Cell 1(3):207–210. doi: 10.1007/s13238-010-0043-9 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Ziolkowska JR (2014) Prospective technologies, feedstocks and market innovations for ethanol and biodiesel production in the US. Biotechnol Rep 4:94–98. doi: 10.1016/j.btre.2014.09.001 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Key Laboratory of Biofuels, Shandong Provincial Key Laboratory of Synthetic Biology, Qingdao Institute of Bioenergy and Bioprocess TechnologyChinese Academy of SciencesQingdaoChina
  2. 2.University of Chinese Academy of SciencesBeijingChina

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