Advertisement

Waste and Biomass Valorization

, Volume 10, Issue 5, pp 1295–1302 | Cite as

Towards a Sustainable Route for the Production of Squalene Using Cyanobacteria

  • Mariane Bittencourt Fagundes
  • Raquel Guidetti Vendruscolo
  • Mariana Manzoni Maroneze
  • Juliano Smanioto Barin
  • Cristiano Ragagnin de Menezes
  • Leila Queiroz Zepka
  • Eduardo Jacob-Lopes
  • Roger WagnerEmail author
Original Paper

Abstract

Treatment of slaughterhouse wastewater is a huge industrial problem. The use of an algae biorefinery platform could be a sustainable technological alternative that produces value-added compounds instead of dumping the wastewater. For this reason, this research aimed to evaluate squalene production from the microalgae Phormidium autumnale cultivated using agroindustrial wastewater. A derivatization method was performed to determine the squalene and fatty acids content, evaluated by gas chromatography with flame ionization and mass spectrometry detectors. A total of 0.18 g/kg of squalene were found in the biomass, with a high content of unsaturated fatty acids (52%). Sensitivity analysis estimated production of 727–72,750 kg/year in industries with different capacities. In this sense, P. autumnale in agroindustrial wastewater could offer a potential alternative method of squalene production.

Graphical Abstract

Keywords

Bioactive compound Gas chromatography Microalgae Phormidium autumnale Sensitivity analysis 

Notes

Acknowledgements

The present study was carried out with the financial support of the National Council for Scientific and Technological Development (CNPq)- Brazil and funding from FAPERGS - Foundation for Research Support of the State of Rio Grande do Sul, Porto Alegre, RS, Brazil and CAPES improving coordination of Higher Education Personnel for supporting this research.

Compliance with Ethical Standards

Conflict of interest

Mariane Bittencourt Fagundes declares that she has no conflict of interest and all the other authors: Raquel Guidetti Vendruscolo, Mariana Manzone Maroneze, Cristiano Ragagnin Menezes, Leila Queiroz Zepka, Juliano Smanioto Barin, Eduardo Jacob-Lopes and Roger Wagner also declares that they have no conflict of interest.

References

  1. 1.
    Xu, W., Ma, X., Wang, Y.: Production of squalene by microbes: an update. World J. Microbiol. Biotechnol. 32, 195 (2016)CrossRefGoogle Scholar
  2. 2.
    Spanova, M., Daum, G.M.: Squalene–biochemistry, molecular biology, process biotechnology, and applications. Eur. J. Lipid Sci. Technol. 113, 1299–1320 (2011)CrossRefGoogle Scholar
  3. 3.
    Mura, S., Bui, D.T., Couvreur, P., Nicolas, J.: Lipid prodrug nanocarriers in cancer therapy. J. Control. Release. 208, 25–41 (2015)CrossRefGoogle Scholar
  4. 4.
    Xu, R., Fazio, G.C., Matsuda, S.P.: On the origins of triterpenoid skeletal diversity. Phytochemistry. 65(3), 261–291 (2004)CrossRefGoogle Scholar
  5. 5.
    Narayan Bhilwade, H., Tatewaki, N., Nishida, H., Konishi, T.: Squalene as novel food factor. Curr. Pharm. Biotechnol. 11, 875–880 (2010)CrossRefGoogle Scholar
  6. 6.
    Reddy, L.H., Couvreur, P.: Squalene: a natural triterpene for use in disease management and therapy. Adv. Drug Deliver. Rev. 61, 1412–1426 (2009)CrossRefGoogle Scholar
  7. 7.
    Roselló-Soto, E., Koubaa, M., Moubarik, A., Lopes, P.R., Saraiva, A.J., Boussetta, N., Grimi, N., Barba, F.J.: Emerging opportunities for the effective valorization of wastes and by-products generated during olive oil production process: Non-conventional methods for the recovery of high-added value compounds. Trends Food Sci. Tech. 45, 296–310 (2015)CrossRefGoogle Scholar
  8. 8.
    Saito, K., Shirasagoa, Y., Suzukic, T., Aizakid, H., Hanadaa, K., Wakitad, T., Nishijimae, M., Fukasawa, M.: Targeting cellular squalene synthase, an enzyme essential for cholesterol biosynthesis, is a potential antiviral strategy against hepatitis C virus. J. virol. 89, 2220–2232 (2015)CrossRefGoogle Scholar
  9. 9.
    Wolosik, K., Knas, M., Zalewska, A., Niczyporuk, M., Przystupa, A.W.: The importance and perspective of plant-based squalene in cosmetology. J. Cosmet. Sci. 64(1), 59–66 (2013)Google Scholar
  10. 10.
    Ghimire, G.P., Thuan, N.H., Koirala, N., Sohng, J.K.: Advances in biochemistry and microbial production of squalene and its derivatives. J. Microbiol. Biotechnol. 26, 441–451 (2016)CrossRefGoogle Scholar
  11. 11.
    Nakazawa, A., Matsuura, H., Kose, R., Kato, S., Honda, D., Inouye, I., Watanabe, M.M.: Optimization of culture conditions of the thraustochytrid Aurantiochytrium sp. strain 18W-13a for squalene production. Bioresour. Technol. 109(Supplement C), 287–291 (2012).  https://doi.org/10.1016/j.biortech.2011.09.127 CrossRefGoogle Scholar
  12. 12.
    Fan, K.W., Aki, T., Chen, F., Jiang, Y.: Enhanced production of squalene in the Thraustochytrid aurantiochytrium mangrovei by medium optimization and treatment with terbinafine. World J. Microb. Biot. 26, 1303–1309 (2010)CrossRefGoogle Scholar
  13. 13.
    Englund, E., Pattanaik, B., Ubhayasekera, S.J.K., Stensjö, K., Bergquist, J., Lindberg, P.: Production of squalene in Synechocystis sp. PCC 6803. PLoS ONE. 9(3), e90270 (2014).  https://doi.org/10.1371/journal.pone.0090270 CrossRefGoogle Scholar
  14. 14.
    Siedenburg, G., Jendrossek, D.: Squalene-hopene cyclases. Appl. Environ. Microbiol. 77, 3905–3915 (2011)CrossRefGoogle Scholar
  15. 15.
    Dangi, S.K., Dubey, S., Bhargava, S.: Cyanobacterial diversity: a potential source of bioactive compounds. Adv. Biol. Microbiol. 4(2474–7617), 001–003 (2017)Google Scholar
  16. 16.
    Koller, M., Marsalek, L.: Cyanobacterial polyhydroxyalkanoate production: status quo and quo vadis? Curr. Biotechnol. 4(4), 464–480 (2015)CrossRefGoogle Scholar
  17. 17.
    Chew, K.W., Yap, J.Y., Show, P.L., Suan, N.H., Juan, J.C., Ling, T.C., Chang, J.S.: Microalgae biorefinery: high value products perspectives. Bioresour. Technol. 229, 53–62 (2017)CrossRefGoogle Scholar
  18. 18.
    Santos, A.M., Roso, G.R., Menezes, C.R., Queiroz, M.I., Zepka, L.Q., Jacob-Lopes, E.: The bioeconomy of microalgal heterotrophic bioreactors applied to agroindustrial wastewater treatment. Desalt. Water Treat. 64, 12–20 (2017) CrossRefGoogle Scholar
  19. 19.
    Santos, A.M., Depra, M.C., Santos, A.M., Zepka, L.Q., Jacob-Lopes, E.: Aeration energy requirements in microalgal heterotrophic bioreactors applied to agroindustrial wastewater treatment. Curr. Biotechnol. 5, 249–254 (2015)CrossRefGoogle Scholar
  20. 20.
    Rodrigues, D.B., Menezes, C.R., Mercadante, A.Z., Jacob-Lopes, E., Zepka, L.Q.: Bioactive pigments from microalgae Phormidium autumnale. Food Res. Int. 77(Part 2), 273–279 (2015)CrossRefGoogle Scholar
  21. 21.
    Rodrigues, D.B., Flores, É.M.M., Barin, J.S., Mercadante, A.Z., Jacob-Lopes, E., Zepka, L.Q.: Production of carotenoids from microalgae cultivated using agroindustrial wastes. Food Res. Int. 65(Part B), 144–148 (2014).  https://doi.org/10.1016/j.foodres.2014.06.037 CrossRefGoogle Scholar
  22. 22.
    Freitas, A.C., Rodrigues, D., Rocha-Santos, T.A.P., Gomes, A.M.P., Duarte, A.C.: Marine biotechnology advances towards applications in new functional foods. Biotechnol. Adv. 30, 1506–1515 (2012)CrossRefGoogle Scholar
  23. 23.
    Titz, M., Kettl, K.-H., Shahzad, K., Koller, M., Schnitzer, H., Narodoslawsky, M.: Process optimization for efficient biomediated PHA production from animal-based waste streams. Clean Technol. Environ. Policy. 14(3), 495–503 (2012)CrossRefGoogle Scholar
  24. 24.
    Shahzad, K., Narodoslawsky, M., Sagir, M., Ali, N., Ali, S., Rashid, M.I., Ismail, I.M.I., Koller, M.: Techno-economic feasibility of waste biorefinery: using slaughtering waste streams as starting material for biopolyester production. Waste Manag. (New York, N.Y.). 67, 73–85 (2017).  https://doi.org/10.1016/j.wasman.2017.05.047 CrossRefGoogle Scholar
  25. 25.
    Luque, R., Clark, J.H.: Valorisation of food residues: waste to wealth using green chemical technologies. Sustain. Chem. Process. 1, 1–3 (2013)CrossRefGoogle Scholar
  26. 26.
    Rodrigues, D.B., Menezes, C.R., Mercadante, A.Z., Jacob-Lopes, E., Zepka, L.Q.: Bioactive pigments from microalgae Phormidium autumnale. Food Res Int. 77(Part 2), 273–279 (2015).  https://doi.org/10.1016/j.foodres.2015.04.027 CrossRefGoogle Scholar
  27. 27.
    Rippka, R., Deruelles, J., Waterbury, J.B., Herdman, M., Stanier, R.Y.: Generic assignments, strain histories and properties of pure cultures of cyanobacteria. Microbiology. 111, 1–61 (1979)CrossRefGoogle Scholar
  28. 28.
    Water Pollution Control Federation American water works association.: Standard Methods for the Examination of Water and Wastewater, t.e.E.A., APHA, WPCF. Water Pollution Control Federation American water works association, Washington, DC (2005)Google Scholar
  29. 29.
    Francisco, E.C., Franco, T.T., Wagner, R., Jacob-Lopes, E.: Assessment of different carbohydrates as exogenous carbono source in cultivation of cyanobacteria. Bioproc. Biosyst. Eng. 1, 2–11 (2014)Google Scholar
  30. 30.
    Bligh, E.G., Dyer, W.J.: A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37(8), 911–917 (1959).  https://doi.org/10.1139/o59-099 CrossRefGoogle Scholar
  31. 31.
    Christie, W.W.: A simple procedure for rapid transmethylation of glycerolipids and cholesteryl esters. J. Lipid Res. 23, 1072–1075 (1982)Google Scholar
  32. 32.
    European Commission: Method Validation and Quality Control Procedures for Pesticide Residues Analysis in Food and Feed (2007)Google Scholar
  33. 33.
    Romari, K., Godart, F., Calleja, P.: Production of Docosahexaenoic Acid and/or Eicosapentaenoic Acid and/or Carotenoids in Mixotrophic Mode by Nitzschia. Google Patents (2017)Google Scholar
  34. 34.
    Meixner, K., Kovalcik, A., Sykacek, E., Gruber-Brunhumer, M., Zeilinger, W., Markl, K., Haas, C., Fritz, I., Mundigler, N., Stelzer, F., Neureiter, M., Fuchs, W., Drosg, B.: Cyanobacteria biorefinery—production of poly(3-hydroxybutyrate) with Synechocystis salina and utilisation of residual biomass. J. Biotechnol. 265(Supplement C), 46–53 (2018).  https://doi.org/10.1016/j.jbiotec.2017.10.020 CrossRefGoogle Scholar
  35. 35.
    Sekar, S., Chandramohan, M.: Phycobiliproteins as a commodity: trends in applied research, patents and commercialization. J. Appl. Phycol. 20(2), 113–136 (2008).  https://doi.org/10.1007/s10811-007-9188-1 CrossRefGoogle Scholar
  36. 36.
    Gong, M., Bassi, A.: Carotenoids from microalgae: a review of recent developments. Biotechnol Adv. 34(8), 1396–1412 (2016).  https://doi.org/10.1016/j.biotechadv.2016.10.005 CrossRefGoogle Scholar
  37. 37.
    Kajikawa, M., Kinohira, S., Ando, A., Shimoyama, M., Kato, M., Fukuzawa, H.: Accumulation of Squalene in a microalga Chlamydomonas reinhardtii by genetic modification of squalene synthase and squalene epoxidase genes. PLoS ONE. 10(3), e0120446 (2015).  https://doi.org/10.1371/journal.pone.0120446 CrossRefGoogle Scholar
  38. 38.
    Fabris, M., Matthijs, M., Carbonelle, S., Moses, T., Pollier, J., Dasseville, R., Baart, G.J., Vyverman, W., Goossens, A.: Tracking the sterol biosynthesis pathway of the diatom Phaeodactylum tricornutum. New Phytol. 204(3), 521–535 (2014).  https://doi.org/10.1111/nph.12917 CrossRefGoogle Scholar
  39. 39.
    Achitouv, E., Metzger, P., Rager, M.N., Largeau, C.: C31-C34 methylated squalenes from a Bolivian strain of Botryococcus braunii. Phytochemistry. 65(23), 3159–3165 (2004).  https://doi.org/10.1016/j.phytochem.2004.09.015 CrossRefGoogle Scholar
  40. 40.
    Jiang, Y., Fan, K.-W., Tsz-Yeung Wong, R., Chen, F.: Fatty acid composition and squalene content of the marine microalga Schizochytrium mangrovei. J. Agric. Food Chem. 52(5), 1196–1200 (2004).  https://doi.org/10.1021/jf035004c CrossRefGoogle Scholar
  41. 41.
    Bhattacharjee, P., Shukla, V.B., Singhal, R.S., Kulkarni, P.R.: Studies on fermentative production of squalene. World J. Microbiol. Biotechnol. 17(8), 811–816 (2001)CrossRefGoogle Scholar
  42. 42.
    Bhattacharjee, P., Singhal, R.S.: Extraction of squalene from yeast by supercritical carbon dioxide. World J. Microb. Biotechnol. 19, 605–608 (2003)CrossRefGoogle Scholar
  43. 43.
    Remme, J.F., Larssen, W.E., Bruheim, I., Sæbø, P.C., Sæbø, A., Stoknes, I.S.: Lipid content and fatty acid distribution in tissues from Portuguese dogfish, leafscale gulper shark and black dogfish. Comp. Biochem. Physiol. Part B. 143(4), 459–464 (2006).  https://doi.org/10.1016/j.cbpb.2005.12.018 CrossRefGoogle Scholar
  44. 44.
    Papiol, V., Fanelli, E., Cartes, J.E., Rumolo, P., López-Pérez, C.: A multi-tissue approach to assess the effects of lipid extraction on the isotopic composition of deep-sea fauna. J. Exp. Mar. Biol. Ecol. 497(Supplement C), 230–242 (2017).  https://doi.org/10.1016/j.jembe.2017.10.001 CrossRefGoogle Scholar
  45. 45.
    Popa, O., Băbeanu, N.E., Popa, I., Niță, S., Dinu-Pârvu, C.E.: Methods for obtaining and determination of squalene from natural sources. Biomed. Res. Int. (2015).  https://doi.org/10.1155/2015/367202 CrossRefGoogle Scholar
  46. 46.
    Francisco, É.C., Franco, T.T., Maroneze, M.M., Zepka, L.Q., Jacob-Lopes, E.: Produção de biodiesel de terceira geração a partir de microalgas. Ciência Rural. 45, 349–355 (2015)CrossRefGoogle Scholar
  47. 47.
    Roso, G.R., dos Santos, A.M., Queiroz, M.I., Barin, J.S., Zepka, L.Q., Jacob-Lopes, E.: The econometrics of production of bulk oil and lipid extracted algae in an agroindustrial biorefinery. Curr. Biotechnol. 4(4), 547–553 (2015)CrossRefGoogle Scholar
  48. 48.
    Venugopal, V., Kumaran, A.K., Sekhar Chatterjee, N., Kumar, S., Kavilakath, S., Nair, J.R., Mathew, S.: Biochemical characterization of liver oil of Echinorhinus brucus (bramble shark) and its cytotoxic evaluation on neuroblastoma cell lines (SHSY-5Y). Scientifica. (2016).  https://doi.org/10.1155/2016/6294030b CrossRefGoogle Scholar
  49. 49.
    Silas, E.G., Selvaraj, G.S.D.: Descriptions of the adult and embryo of the bramble shark Echinorhinus brucus (Bonnaterre) obtained from the continental slope of índia. J. Mar. Biol. Assoc. India. 14, 395–401 (1972)Google Scholar
  50. 50.
    Nichols, P., Rayner, M.S., Stevens, J.D.: A Pilot Investigation of Northern Australian Shark Liver Oils: Characterization and Value-adding. CSIRO Marine Research, Hobart (2001)Google Scholar
  51. 51.
    Martineau, E., Wood, S.A., Miller, R.M., Jungblut, A.D., Hawes, I., Webster-Brown, J., Packer, M.A.: Characterisation of Antarctic cyanobacteria and comparison with New Zealand strains. Hydrobiologia. 711, 139–154 (2013)CrossRefGoogle Scholar
  52. 52.
    Clarke, M.W., Connolly, P.L., Bracken, J.J.: Catch, discarding, age estimation, growth and maturity of the squalid shark Deania calceus west and north of Ireland. Fish. Res. 56, 139–153 (2002)CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  • Mariane Bittencourt Fagundes
    • 1
  • Raquel Guidetti Vendruscolo
    • 1
  • Mariana Manzoni Maroneze
    • 1
  • Juliano Smanioto Barin
    • 1
  • Cristiano Ragagnin de Menezes
    • 1
  • Leila Queiroz Zepka
    • 1
  • Eduardo Jacob-Lopes
    • 1
  • Roger Wagner
    • 1
    Email author
  1. 1.Department of Food Science and TechnologyFederal University of Santa MariaSanta MariaBrazil

Personalised recommendations