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Synechococcus elongatus PCC7942: a cyanobacterium cell factory for producing useful chemicals and fuels under abiotic stress conditions

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Abstract

Sucrose, a compatible osmolyte in cyanobacteria, functions both as an energy reserve and as osmoprotectant. Sugars are the most common substrates used by microorganisms to produce hydrogen (H2) by means of anaerobic dark fermentation. Cells of the unicellular, non-nitrogen fixing, freshwater cyanobacterium Synechococcus elongatus PCC7942 accumulate sucrose under salt stress. In the present work, we used this cyanobacterium and a genetically engineered strain of it (known as PAMCOD) to investigate the optimal conditions for (a) photosynthetic activity, (b) cell proliferation and (c) sucrose accumulation, which are necessary for H2 production via anaerobic dark fermentation of the accumulated sucrose. PAMCOD (Deshnium et al. in Plant Mol Biol 29:897–902, 1995) contains the gene codA that codes for choline oxidase, the enzyme which converts choline to the zwitterion glycine betaine. Glycine betaine is a compatible osmolyte which increases the salt tolerance of Synechococcus elongatus PCC7942. Furthermore, glycine betaine maintains cell proliferation under salt stress and results in increased sucrose accumulation. In the present study, we examine the environmental factors, such as the NaCl concentration, the culture medium pH, and the carbon dioxide content of the air bubbled through it. At optimal conditions, sucrose accumulated in the cyanobacteria cells up to 13.5 mol per mole Chl a. Overall, genetically engineered Synechococcus elongatus PCC7942 produces sucrose in sufficient quantities such that it may be a viable alternative (a) to sucrose synthesis, and (b) to H2 formation via anaerobic dark fermentation.

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References

  • Ainas M, Hasnaoui S, Bouarab R, Abdi N, Drouiche N, Mameri N (2017) Hydrogen production with the cyanobacterium Spirulina platensis. Int J Hydrogen Energy 42:4902–4907

    CAS  Google Scholar 

  • Angermayr SK, Rovira AG, Hellingwerf KJ (2015) Metabolic engineering of cyanobacteria for the synthesis of commodity products. Trends Biotechnol 33:352–361

    CAS  PubMed  Google Scholar 

  • Argun H, Gokfiliz P, Karapinar I (2017) Biohydrogen production potential of different biomass sources. In: Singh A, Rathore D (eds) Biohydrogen production: sustainability of current technology and future perspective. Springer, Berlin, p 12

    Google Scholar 

  • Avigad G (1990) Disaccharides. In: Dey PM, Harborne JB (eds) Methods in plant biochemistry. Academic Press, London

    Google Scholar 

  • Billini M, Stamatakis K, Sophianopoulou V (2008) Two members of a network of putative Na+/H+ antiporters are involved in salt and pH tolerance of the freshwater cyanobacterium Synechococcus elongatus. J Bacteriol 190:6318–6329

    CAS  PubMed  PubMed Central  Google Scholar 

  • Blumwald E, Mehlhorn RJ, Packer L (1983) Ionic osmoregulation during salt adaptation of the cyanobacterium Synechococcus 6311. Plant Physiol 73:377–380

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bothe H (1982) Nitrogen fixation. In: Carr NG, Whitton BA (eds) Botanical monographs, the biology of cyanobacteria. Blackwell Scientific Oxford Publications, Oxford, pp 87–104

    Google Scholar 

  • Bothe H, Boison G, Schmitz O (1999) Hydrogenases in cyanobacteria. In: Peschek GA, Loffelhardt W, Schmetterer G (eds) The phototrophic prokaryotes. Kluwer Academic Plenum publishers, New York, pp 589–594

    Google Scholar 

  • Bryant DA (ed) (1994) The molecular biology of cyanobacteria, advances in photosynthesis. Springer, Berlin

    Google Scholar 

  • Das D (2009) Advances in biohydrogen production processes: an approach towards commercialization. Int J Hydrogen Energy 34:7349–7357

    CAS  Google Scholar 

  • Davila-Vazquez G, Arriaga S, Alatriste-Mondragón F, de León-Rodríguez A, Rosales-Colunga LM, Razo-Flores E (2008) Fermentative biohydrogen production: trends and perspectives. Rev Environ Sci Biotechnol 7:27–45

    CAS  Google Scholar 

  • Deshnium P, Los DA, Hayashi H, Mustardy L, Murata N (1995) Transformation of Synechococcus with a gene for choline oxidase enhances tolerance to salt stress. Plant Mol Biol 29:897–902

    CAS  PubMed  Google Scholar 

  • Duan Y, Luo Q, Liang F, Lu X (2016) Sucrose secreted by the engineered cyanobacterium and its fermentability. J Ocean Univ China 15:890–896

    CAS  Google Scholar 

  • Ducat DC, Avelar-Rivas JA, Way JC, Silvera PA (2012) Rerouting carbon flux to enhance photosynthetic productivity. Appl Env Microbiol 78:2660–2668

    CAS  Google Scholar 

  • Dutta D, De D, Chaudhuri S, Bhattacharya SK (2005) Hydrogen production by cyanobacteria. Microb Cell Factories 4:36

    Google Scholar 

  • Encarnacao T, Pais AA, Camps MG, Burrows HD (2015) Cyanobacteria and microalgae: a renewable resource of bioactive compounds and other chemicals. Sci Prog 98:145–168

    CAS  PubMed  Google Scholar 

  • Formighieri C, Melis A (2018) Cyanobacterial production of plant essential oils. Planta 248:933–946

    CAS  PubMed  Google Scholar 

  • Frenkel A, Gaffron H, Battley HE (1950) Photosynthesis and photoreduction by the blue green alga, Synechococcus elongatus, Näg. Biol Bull 99:157–162

    CAS  PubMed  Google Scholar 

  • Jeanjean R, Matthijs HCP, Onana B, Havaux M, Joset F (1993) Exposure of the cyanobacterium Synechocystis PCC6803 to salt stress induces concerted changes in respiration and photosynthesis. Plant Cell Physiol 34:1073–1079

    CAS  Google Scholar 

  • Gao X, Sun T, Pei G, Chen L, Zhang W (2016) Cyanobacterial chassis engineering for enhancing production of biofuels and chemicals. Appl Microbiol Biotechnol 100:3401–3413

    CAS  PubMed  Google Scholar 

  • Haystead A, Robinson R, Stewart WDP (1970) Nitrogenase activity in extracts of heterocystous blue-green alga. Arch Microbiol 74:235–243

    CAS  Google Scholar 

  • Howarth DC, Codd GA (1985) The uptake and production of molecular hydrogen by unicellular cyanobacteria. J Gen Microbiol 131:1561–1569

    CAS  Google Scholar 

  • Kitchener RL, Grunden AM (2018) Methods for enhancing cyanobacterial stress tolerance to enable improved production of biofuels and industrially relevant chemicals. Appl Microbiol Biotechnol 102:1617–1628

    CAS  PubMed  Google Scholar 

  • Klähn S, Hagemann M (2011) Compatible solute biosynthesis in cyanobacteria. Environ Microbiol 13:551–562

    PubMed  Google Scholar 

  • Kolman MA, Nishi CN, Perez-Cenci M, Salerno GL (2015) Sucrose in cyanobacteria: from a salt-response molecule to play a key role in nitrogen fixation. Life 5:102–126

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kovacevic V, Wesseler J (2010) Cost-effectiveness analysis of algae energy production in the EU. Energy Policy 38:5749–5757

    Google Scholar 

  • Ladas N, Papageorgiou CG (2000a) The salinity tolerance of freshwater cyanobacterium Synechococcus sp. PCC 7942 is determined by its ability for osmotic adjustment and presence of osmolyte sucrose. Photosynthetica 38:343–348

    CAS  Google Scholar 

  • Ladas NP, Papageorgiou GC (2000b) Cell turgor: a critical factor for the proliferation of cyanobacteria at unfavorable salinity. Photosyn Res 65:155–164

    CAS  Google Scholar 

  • Li Y, Horsman M, Wu N, Lan CQ, Dubois-Calero N (2008) Biofuels from microalgae. Biotechnol Prog 24:815–882

    CAS  PubMed  Google Scholar 

  • Mamedov MD, Hayashi H, Wada H, Mohanty PS, Papageorgiou GC, Murata N (1991) Glycine betaine enhances and stabilizes the evolution of oxygen and the synthesis of ATP by cyanobacterial thylakoid membranes. FEBS Lett 294:271–274

    CAS  PubMed  Google Scholar 

  • Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31:426–428

    CAS  Google Scholar 

  • Mohanty PS, Hayashi H, Papageorgiou GC, Murata N (1993) Stabilization of the Mn-cluster of the oxygen-evolving complex by glycine betaine. Biochim Biophys Acta 1144:92–96

    CAS  Google Scholar 

  • Moran P (1982) Formulae for determination of chlorophyllous pigments extracted with N,N-dimethyl-formamide. Plant Physiol 69:1376–1381

    CAS  PubMed  PubMed Central  Google Scholar 

  • Murata N, Mohanty PS, Hayashi H, Papageorgiou GC (1992) Glycine betaine stabilizes the association of extrinsic proteins with the photosynthetic oxygen evolving complex. FEBS Lett 296:187–189

    CAS  PubMed  Google Scholar 

  • Najafpour M, Moghaddam AN, Shen J-R (2013) Water Oxidation and water oxidizing complex in cyanobacteria. In: Srivastava AK, Rai AN, Neilan BA (eds) Stress biology of cyanobacteria: molecular mechanisms to cellular responses. CRC Press, Boca Raton, pp 41–60

    Google Scholar 

  • Niederholtmeyer H, Wolfstädter BT, Savage DF, Silver PA, Way JC (2010) Engineering cyanobacteria to synthesize and export hydrophilic products. Appl Environ Microbiol 76:3462–3466

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nomura Μ, Ishitani Μ, Takabe Τ, Rai AK, Takabe T (1995) Synechococcus sp. PCC7942 transformed with Escherichia coli bet genes produces glycine betaine choline and acquires resistance to salt stress. Plant Physiol 107:703–708

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ort DR, Merchant SS, Alric J, Barkang A, Blankenship RE, Bockj R, Croce R, Hanson MR, Hibberd JM, Long SP, Moore TA, Moroney J, Niyogi KK, Parry MAJ, Peralta-Yahya PP, Prince RC, Redding KE, Martin H, Spalding MH, van Wijky KJ, Vermaas WFJ, von Caemmerer S, Weber APM, Yeates TO, Yuan JS, Zhu X-G (2015) Redesigning photosynthesis to sustainably meet global food and bioenergy demand. Proc Natl Acad Sci 112:8529–8536

    CAS  PubMed  Google Scholar 

  • Papageorgiou GC, Alygizaki Zorba A, Ladas N, Murata N (1998) A method to probe the cytoplasmic osmolality and osmotic water and solute fluxes across the cell membrane of cyanobacteria with chlorophyll a fluorescence: experiments with Synechococcus sp. PCC7942. Physiol Plant 103:215–224

    CAS  Google Scholar 

  • Peschek GA (1979a) Aerobic hydrogenase activity in Anacystis nidulans: the oxyhydrogen re-action. Biochim Biophys Acta 548:203–215

    CAS  PubMed  Google Scholar 

  • Peschek GA (1979b) Anaerobic hydrogenase activity in Anacystis nidulans: H2-dependent photoreduction and related reactions. Biochim Biophys Acta 548:187–202

    CAS  PubMed  Google Scholar 

  • Peschek GA (1979c) Evidence for two functionally distinct hydrogenases in Anacystis nidulans. Arch Microbiol 123:81–92

    CAS  Google Scholar 

  • Qiao C, Duan Y, Zhang M, Hagemann M, Luo Q, Lu X (2018) Effects of reduced and enhanced glycogen pools of salt-induced sucrose production in a sucrose-secreting strain of Synechococcus elongatus PCC 7942. Appl Environ Microbiol 84:1–11

    CAS  Google Scholar 

  • Reed RH, Borowitzka LJ, Mackay MA, Chudek JA, Foster R, Warr SRC, Moore DJ, Stewart WDP (1986) Organic solute accumulation in osmotically stressed cyanobacteria. FEMS Microbiol Rev 39:51–56

    CAS  Google Scholar 

  • Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RT (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61

    Google Scholar 

  • Saper G, Kallmann D, Conzuelo F, Zhao F, Tóth NT, Liveanu V, Meir S, Szymanski S, Aharoni A, Schuhmann W, Rothschild A, Schuster G, Adir N (2018) Live cyanobacteria produce photocurrent and hydrogen using both the respiratory and photosynthetic systems. Nat Commun 9:2168

    PubMed  PubMed Central  Google Scholar 

  • Schmitz O, Boison G, Hilscher R, Hundeshagen B, Zimmer W, Lottspeich F, Bothe H (1995) Molecular biological analysis of a bidirectional hydrogenase from cyanobacteria. Eur J Biochem 233:266–276

    CAS  PubMed  Google Scholar 

  • Shevela D, Pishchalinikov E, Govindjee LA (2013) Oxygenic photosynthesis in cyanobacteria. In: Srivastava AK, Rai AN, Neilan BA (eds) Stress biology of cyanobacteria: molecular mechanisms to cellular responses. CRC Press, Boca Raton, pp 3–40

    Google Scholar 

  • 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 76:3153–3159

    CAS  PubMed  PubMed Central  Google Scholar 

  • Stamatakis C, Papageorgiou GC (1993) Stabilization of photosystem II particles isolated from thermophilic cyanobacterium Phormidium laminosum with glycinebetaine and glycerol. Biochim Biophys Acta (Bioenergetics) 1183:333–338

    CAS  Google Scholar 

  • Stewart DP (1980) Some aspects of structure and function in N2-fixing cyanobacteria. Ann Rev Microbiol 34:497–536

    CAS  Google Scholar 

  • Stirbet A, Lazar D, Papageorgiou G (2019) Chlorophyll a fluorescence in cyanobacteria: Relation to photosynthesis. In: Mishra AN, Tiwari DN, Rai AN (eds) Cyanobacteria: from basic science to applications, Chapter 5. Elsevier Publishers Academic, Dordrecht, pp 79–130

    Google Scholar 

  • Tiwari A, Pandey A (2012) Cyanobacterial hydrogen production – a step towards clean environment. Int J Hydrogen Energy 37:139–150

    CAS  Google Scholar 

  • Vermaas W (2013) Solar-powered production of biofuels and other petroleum substitutes by cyanobacteria: stoichiometries of reducing equivalents and chemical energy, and energy conversion efficiency. In: Photosynthesis research for food, fuel and the future. Advanced topics in science and technology in China. Springer, Berlin

  • Waterbury JB, Watson SW, Guillard RRL, Brand LE (1979) Widespread occurrence of a unicellular, marine, planktonic, cyanobacterium. Nature 277:293–294

    Google Scholar 

  • Zhu X-G, Long SP, Ort DR (2008) What is the maximum efficiency with which photosynthesis can convert solar energy into biomass? Curr Opin Biotechnol 19:153–159

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We acknowledge support of this work by the project “Target Identification and Development of Novel Approaches for Health and Environmental Applications” (MIS 5002514) which is implemented under the Action for the Strategic Development on the Research and Technological Sectors, funded by the Operational Programme "Competitiveness, Entrepreneurship and Innovation" (NSRF 2014–2020) and co-financed by Greece and the European Union (European Regional Development Fund).

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Correspondence to Kostas Stamatakis.

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Dedicated to Prof. Norio Murata, a leading scientist in photosynthesis research

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Vayenos, D., Romanos, G.E., Papageorgiou, G.C. et al. Synechococcus elongatus PCC7942: a cyanobacterium cell factory for producing useful chemicals and fuels under abiotic stress conditions. Photosynth Res 146, 235–245 (2020). https://doi.org/10.1007/s11120-020-00747-6

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