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Synechococcus elongatus BDU 130192, an Attractive Cyanobacterium for Feedstock Applications: Response to Culture Conditions

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Abstract

Marine cyanobacteria are attractive organisms as feedstock for bioethanol and biotechnological applications. Previously, a marine cyanobacterial strain Synechococcus elongatus BDU 130192 was identified which can accumulate high polyglucan levels without the need to resort to N-deprivation. In this study, among the three different temperatures (30, 34, and 38 °C) tested, the highest biomass accumulation and total carbohydrate occur at 34 °C. The biomass and total carbohydrate increased with increasing light intensities, while protein, chlorophyll, and carotenoid contents were reduced. The best growth occurred at 1.8% NaCl concentration, even though the strain could grow well until 5.8% NaCl. Among the different concentrations of CO2 tested, the best growth occurred at 5% CO2 in the air. NaNO3 gave the best growth, though the cells were able to grow well on urea and NH4Cl too. Tripling the concentration of either N or P in the medium led to a significant increase in growth rate. The strain does not require the addition of vitamin B12 for growth, and about 90% flocculation could be achieved in an hour with the addition of chitosan. High productivities of 0.5 g/L/day of biomass and 0.23 g/L/day of carbohydrates could be reached in a 3-L photobioreactor (PBR) bubbled with air. This work shows many unique properties of this strain such as high carbohydrate productivity, ability to tolerate high light intensities and high concentrations of salt and CO2, and efficient flocculation. These properties make Synechococcus elongatus BDU 130192 an attractive candidate as a feedstock for bioethanol and biotechnological applications.

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References

  1. Luan G, Lu X (2018) Tailoring cyanobacterial cell factory for improved industrial properties. Biotechnol Adv 36:430–442. https://doi.org/10.1016/j.biotechadv.2018.01.005

    Article  CAS  PubMed  Google Scholar 

  2. Kusakabe T, Tatsuke T, Tsuruno K, Hirokawa Y, Atsumi S, Liao JC, Hanai T (2013) Engineering a synthetic pathway in cyanobacteria for isopropanol production directly from carbon dioxide and light. Metab Eng 20:101–108. https://doi.org/10.1016/j.ymben.2013.09.007

    Article  CAS  PubMed  Google Scholar 

  3. Stanier RY, Deruelles J, Rippka R, Herdman M, Waterbury JB (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. Microbiol 111:1–61. https://doi.org/10.1099/00221287-111-1-1

    Article  Google Scholar 

  4. Stanier RY, Bazine GC (1977) Phototrophic prokaryotes: the cyanobacteria. Annu Rev Microbiol 31:225–274. https://doi.org/10.1146/annurev.mi.31.100177.001301

    Article  CAS  PubMed  Google Scholar 

  5. Dismukes GC, Carrieri D, Bennette N, Ananyev GM, Posewitz MC (2008) Aquatic phototrophs: efficient alternatives to land-based crops for biofuels. Curr Opin Biotechnol 19:235–240. https://doi.org/10.1016/j.copbio.2008.05.007

    Article  CAS  PubMed  Google Scholar 

  6. Pathak J, Rajneesh MPK et al (2018) Cyanobacterial farming for environment friendly sustainable agriculture practices: innovations and perspectives. Front Environ Sci 6. https://doi.org/10.3389/fenvs.2018.00007

  7. Wang H, Yang Y, Chen W, Ding L, Li P, Zhao X, Wang X, Li A, Bao Q (2013) Identification of differentially expressed proteins of Arthrospira (Spirulina) plantensis-YZ under salt-stress conditions by proteomics and qRT-PCR analysis. Proteome Sci 11:6. https://doi.org/10.1186/1477-5956-11-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Figler A, B-Beres V, Dobronoki D et al (2019) Salt tolerance and desalination abilities of nine common green microalgae isolates. Water 11:2527. https://doi.org/10.3390/w11122527

    Article  CAS  Google Scholar 

  9. Hagemann M (2011) Molecular biology of cyanobacterial salt acclimation. FEMS Microbiol Rev 35:87–123. https://doi.org/10.1111/j.1574-6976.2010.00234.x

    Article  CAS  PubMed  Google Scholar 

  10. Skjanes K, Lindblad P, Muller J (2007) BioCO2 – A multidisciplinary, biological approach using solar energy to capture CO2 while producing H2 and high value products. Biomol Eng 24:405–413. https://doi.org/10.1016/j.bioeng.2007.06.002

    Article  CAS  PubMed  Google Scholar 

  11. Fx F, Me W, Y Z et al (2007) Effects of increased temperature and CO2 on photosynthesis, growth, and elemental ratios in marine Synechococcus and Prochlorococcus (Cyanobacteria). J Phycol 43:485–496. https://doi.org/10.1111/j.1529-8817.2007.00355.x

    Article  Google Scholar 

  12. Pessarakli M (2016) Handbook of Photosynthesis. CRC Press

  13. Hasunuma T, Kikuyama F, Matsuda M, Aikawa S, Izumi Y, Kondo A (2013) Dynamic metabolic profiling of cyanobacterial glycogen biosynthesis under conditions of nitrate depletion. J Exp Bot 64:2943–2954. https://doi.org/10.1093/jxb/ert134

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. John RP, Anisha GS, Nampoothiri KM, Pandey A (2011) Micro and macroalgal biomass: a renewable source for bioethanol. Bioresour Technol 102:186–193. https://doi.org/10.1016/j.biortech.2010.06.139

    Article  CAS  PubMed  Google Scholar 

  15. Mollers K, Cannella D, Jorgensen H, Frigaard N-U (2014) Cyanobacterial biomass as carbohydrate and nutrient feedstock for bioethanol production by yeast fermentation. Biotechnol Biofuels 7:64. https://doi.org/10.1186/1754-6834-7-64

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Cordara A, Re A, Pagliano C, van Alphen P, Pirone R, Saracco G, Branco dos Santos F, Hellingwerf K, Vasile N (2018) Analysis of the light intensity dependence of the growth of Synechocystis and of the light distribution in a photobioreactor energized by 635 nm light. PeerJ 6:e5256. https://doi.org/10.7717/peerj.5256

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Selao TT, Włodarczyk A, Nixon PJ, Norling B (2019) Growth and selection of the cyanobacterium Synechococcus sp. PCC 7002 using alternative nitrogen and phosphorus sources. Metab Eng 54:255–263. https://doi.org/10.1016/j.ymben.2019.04.013

    Article  CAS  PubMed  Google Scholar 

  18. Kumar M, Kulshreshtha J, Singh GP (2011) Growth and biopigment accumulation of cyanobacterium Spirulina platensis at different light intensities and temperature. Braz J Microbiol 42:1128–1135. https://doi.org/10.1590/S1517-83822011000300034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Mackey KRM, Paytan A, Caldeira K, Grossman AR, Moran D, McIlvin M, Saito MA (2013) Effect of temperature on photosynthesis and growth in marine Synechococcus spp. Plant Physiol 163:815–829. https://doi.org/10.1104/pp.113.221937

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Renault F, Sancey B, Badot PM, Crini G (2009) Chitosan for coagulation/flocculation processes – an eco-friendly approach. Eur Polym J 45:1337–1348. https://doi.org/10.1016/j.eurpolymj.2008.12.027

    Article  CAS  Google Scholar 

  21. Ducat DC, Way JC, Silver PA (2011) Engineering cyanobacteria to generate high-value products. Trends Biotechnol 29:95–103. https://doi.org/10.1016/j.tibtech.2010.12.003

    Article  CAS  PubMed  Google Scholar 

  22. Rosenberg JN, Oyler GA, Wilkinson L, Betenbaugh MJ (2008) A green light for engineered algae: redirecting metabolism to fuel a biotechnology revolution. Curr Opin Biotechnol 19:430–436. https://doi.org/10.1016/j.copbio.2008.07.008

    Article  CAS  PubMed  Google Scholar 

  23. Pathania R, Ahmad A, Srivastava S (2017) Draft genome sequence of an Indian marine cyanobacterial strain with fast growth and high polyglucan content. Genome Announc 5. https://doi.org/10.1128/genomeA.01334-17

  24. Ahmad A, Pathania R, Srivastava S (2020) Biochemical characteristics and a genome-scale metabolic model of an Indian euryhaline cyanobacterium with high polyglucan content. Metabolites 10:177. https://doi.org/10.3390/metabo10050177

    Article  CAS  PubMed Central  Google Scholar 

  25. De Farias Silva CE, Sforza E, Bertucco A (2017) Effects of pH and carbon source on Synechococcus PCC 7002 cultivation: biomass and carbohydrate production with different strategies for pH control. Appl Biochem Biotechnol 181:682–698. https://doi.org/10.1007/s12010-016-2241-2

    Article  CAS  PubMed  Google Scholar 

  26. Muthuraj M, Kumar V, Palabhanvi B, Das D (2014) Evaluation of indigenous microalgal isolate Chlorella sp. FC2 IITG as a cell factory for biodiesel production and scale up in outdoor conditions. J Ind Microbiol Biotechnol 41:499–511. https://doi.org/10.1007/s10295-013-1397-9

    Article  CAS  PubMed  Google Scholar 

  27. Kim H, Jo BY, Kim HS et al (2017) Effect of different concentrations and ratios of ammonium, nitrate, and phosphate on growth of the blue-green alga (cyanobacterium) Microcystis aeruginosa isolated from the Nakdong River, Korea. ALGAE 32:275–284. https://doi.org/10.4490/algae.2017.32.10.23

    Article  CAS  Google Scholar 

  28. Varshney P, Sohoni S, Wangikar PP, Beardall J (2016) Effect of high CO2 concentrations on the growth and macromolecular composition of a heat- and high-light-tolerant microalga. J Appl Phycol 28:2631–2640. https://doi.org/10.1007/s10811-016-0797-4

    Article  CAS  Google Scholar 

  29. Dutt V, Srivastava S (2018) Novel quantitative insights into carbon sources for synthesis of poly hydroxybutyrate in Synechocystis PCC 6803. Photosynth Res 136:303–314. https://doi.org/10.1007/s11120-017-0464-x

    Article  CAS  PubMed  Google Scholar 

  30. DuBois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:353–356 https://pubs.acs.org/doi/pdf/10.1021/ac60111a017

    Article  Google Scholar 

  31. Watson J, Degnan B, Degnan S, Kromer JO (2014) Determining the biomass composition of a sponge holobiont for flux analysis. In: Kromer JO, Nielsen LK, Blank LM (eds) Metabolic Flux Analysis. Springer New York, New York, NY, pp 107–125

    Google Scholar 

  32. Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, Fujimoto EK, Goeke NM, Olson BJ, Klenk DC (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 150:76–85. https://doi.org/10.1016/0003-2697(85)90442-7

    Article  CAS  PubMed  Google Scholar 

  33. Cataldo DA, Maroon M, Schrader LE, Youngs VL (1975) Rapid colorimetric determination of nitrate in plant tissue by nitration of salicylic acid. Commun Soil Sci Plan 6:71–80. https://doi.org/10.1080/00103627509366547

    Article  CAS  Google Scholar 

  34. Taussky HH, Shorr E (1953) A microcolorimetric method for the determination of inorganic phosphorus. J Biol Chem 202:675–685

    Article  CAS  Google Scholar 

  35. Johnson TJ, Katuwal S, Anderson GA, Gu L, Zhou R, Gibbons WR (2018) Photobioreactor cultivation strategies for microalgae and cyanobacteria. Biotechnol Prog 34:811–827. https://doi.org/10.1002/btpr.2628

    Article  CAS  PubMed  Google Scholar 

  36. Jackson SA, Eaton Rye JJ (2017) Modular growth vessels for the cultivation of the cyanobacterium Synechococcus sp. PCC 7002. N Z J Bot 55:14–24. https://doi.org/10.1080/0028825X.2016.1231123

    Article  Google Scholar 

  37. Aikawa S, Nishida A, Hasunuma T et al (2019) Short-term temporal metabolic behavior in halophilic Cyanobacterium Synechococcus sp. strain PCC 7002 after salt shock. Metabolites 9:297. https://doi.org/10.3390/metabo9120297

    Article  CAS  PubMed Central  Google Scholar 

  38. Pade N, Hagemann M (2014) Salt acclimation of cyanobacteria and their application in biotechnology. Life 5:25–49. https://doi.org/10.3390/life5010025

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Carrieri D, Momot D, Brasg IA, Ananyev G, Lenz O, Bryant DA, Dismukes GC (2010) Boosting autofermentation rates and product yields with sodium stress cycling: application to production of renewable fuels by cyanobacteria. Appl Environ Microbiol 76:6455–6462. https://doi.org/10.1128/AEM.00975-10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Singh P, Kumar D (2020) Biomass and lipid productivities of cyanobacteria- Leptolyngbya foveolarum HNBGU001. Bioenerg Res. https://doi.org/10.1007/s12155-020-10170-3

  41. Bhandari R, Sharma PK (2006) High-light-induced changes on photosynthesis, pigments, sugars, lipids and antioxidant enzymes in freshwater (Nostoc spongiaeforme) and marine (Phormidium corium) cyanobacteria. Photochem Photobiol 82:702–710. https://doi.org/10.1562/2005-09-20-RA-690

    Article  CAS  PubMed  Google Scholar 

  42. Zavrel T, Faizi M, Loureiro C et al (2019) Quantitative insights into the cyanobacterial cell economy. eLife 8:e42508. https://doi.org/10.7554/eLife.42508

    Article  PubMed  PubMed Central  Google Scholar 

  43. Aikawa S, Nishida A, Ho S-H, 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. https://doi.org/10.1186/1754-6834-7-88

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

The authors are thankful to DBT for the funding and ICGEB, New Delhi, for the space and facilities. The authors also thank Dr. Kavish Kumar Jain for his help with the fermenter experiment. RP thanks CSIR (Council of Scientific and Industrial Research) for her Ph.D. fellowship.

Funding

The authors thank the Department of Biotechnology (DBT), Ministry of Science and Technology, India, for funding the research via the DBT-ICGEB Center for Advanced Bioenergy Research grant (No. BT/PB/Centre/03/2011-Phase 2).

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Authors and Affiliations

  1. Systems Biology for Biofuel Group, ICGEB Campus, Aruna Asaf Ali Marg, New Delhi, 110067, India

    Ruchi Pathania & Shireesh Srivastava

  2. DBT-ICGEB Center for Advanced Bioenergy Research, International Centre for Genetic Engineering and Biotechnology (ICGEB), New Delhi, India

    Shireesh Srivastava

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  1. Ruchi Pathania
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Correspondence to Shireesh Srivastava.

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Pathania, R., Srivastava, S. Synechococcus elongatus BDU 130192, an Attractive Cyanobacterium for Feedstock Applications: Response to Culture Conditions. Bioenerg. Res. 14, 954–963 (2021). https://doi.org/10.1007/s12155-020-10207-7

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