Skip to main content

Advertisement

SpringerLink
Log in

Organic wastes/by-products as alternative to CO2 for producing mixotrophic microalgae enhancing lipid production

  • Research Paper
  • Published:
Bioprocess and Biosystems Engineering Aims and scope Submit manuscript

Abstract

In this work, white wine lees (WWL), cheese whey (CW), and glycerol (GLY) were used as carbon (C) sources to mixotrophically support the production of the microalga Nannochloropsis salina, replacing CO2 supply. In doing so, the alga was allowed to grow on C sources dosed at 2 g L−1, 3 g L−1, and 4 g L−1 of C, in the presence and absence of CO2 supply. WWL and CW were not able to support the algal growth due to a fungal contamination that was genomically identified, while GLY gave interesting results in particular with 3 g L−1 of C. GLY-C was able to replace CO2-C completely when the latter was omitted, showing an algal biomass production similar to those obtained in autotrophy. If CO2-C was provided jointly with GLY-C, biomass production and lipid contents increased more than 30% and 23%, respectively, compared to autotrophy.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Pulz O, Gross W (2004) Valuable products from biotechnology of microalgae. Appl Microbiol Biotechnol 65:635–648

    Article  CAS  Google Scholar 

  2. Blair MF, Kokabian B, Gude VG (2014) Light and growth medium effect on Chlorella vulgaris biomass production. J Environ Chem Eng 2:665–674

    Article  CAS  Google Scholar 

  3. Acién FG, Fernàndez JM, Magàn JJ, Molina E (2012) Production cost of a real microalgae production plant and strategies to reduce it. Biotechnol Adv 30:1344–1353

    Article  Google Scholar 

  4. Park J, Jin HF, Lim BR, Park KY, Lee K (2010) Ammonia removal from anaerobic digestion effluent of livestock waste using green alga Scenedesmus sp. Bioresour Technol 101:8649–8657

    Article  CAS  Google Scholar 

  5. Ledda C, Romero Villegas GI, Adani F, Acién Fernández FG, Molina Grima E (2015) Utilization of centrate from wastewater treatment for the outdoor production of Nannochloropsis gaditana biomass at pilot-scale. Algal Res 12:17–25

    Article  Google Scholar 

  6. Wan M, Liu P, Xia J, Rosenberg JN, Oyler GA, Betenbaugh MJ, Nie Z, Qiu G (2011) The effect of mixotrophy on microalgal growth, lipid content, and expression levels of three pathway genes in Chlorella sorokiniana. Appl Microbiol Biotechno 91:835–844

    Article  CAS  Google Scholar 

  7. Xiong W, Gao C, Yan D, Wu C, Wu Q (2010) Double CO2 fixation in photosynthesis-fermentation model enhances algal lipid synthesis for biodiesel production. Bioresour Technol 101:2287–2293

    Article  CAS  Google Scholar 

  8. Kang CD, Lee JS, Park TH, Sim SJ (2005) Comparison of heterotrophic and photoautotrophic induction on astaxanthin production by Haematococcus pluvialis. Appl Microbiol Biotechnol 68:237–241

    Article  CAS  Google Scholar 

  9. Hu Q, Sommerfeld M, Jarvis E, Ghirardi M, Posewitz M, Seibert M, Darzins A (2008) Microalgal triacylglycerols as feedstocks for biofuel production: perspectives and advances. Plant J 54:621–639

    Article  CAS  Google Scholar 

  10. Marquez FJ, Sasaki K, Kakizono T, Nishio N, Nagai S (1993) Growth characteristics of Spirulina platensis in mixotrophic and heterotrophic conditions. J Ferment Bioeng 76:408–410

    Article  CAS  Google Scholar 

  11. Vonshak SM, Chen CF (2013) Mixotrophic growth modifies the response of Spirulina (Arthrospira) platensis (Cyanobacteria) cells to light. J Phycol 36:675–679

    Article  Google Scholar 

  12. Yu H, Jia S, Dai Y (2009) Growth characteristics of the cyanobacterium Nostoc flagelliforme in photoautotrophic, mixotrophic and heterotrophic cultivation. J Appl Phyco 21:127–133

    Article  CAS  Google Scholar 

  13. Venkata Mohan S, Rohit MV, Chiranjeevi P, Chandra R, Navaneeth B (2015) Heterotrophic microalgae cultivation to synergize biodiesel production with waste remediation: Progress and perspectives. Bioresour Technol 184:169–178

    Article  CAS  Google Scholar 

  14. Ogbonna JC, Yoshizawa H, Tanaka H (2000) Treatment of high strength organic wastewater by a mixed culture of photosynthetic microorganisms. J Appl Phycol 12:277–284

    Article  CAS  Google Scholar 

  15. Yang C, Hua Q, Shimizu K (2000) Energetics and carbon metabolism during growth of microalgal cells under photoautotrophic, mixotrophic and cyclic light-autotrophic/dark-heterotrophic conditions. Biochem Eng J 6:87–102

    Article  CAS  Google Scholar 

  16. Salati S, D’Imporzano G, Menin B, Veronesi D, Scaglia B, Abbruscato P, Mariani P, Adani F (2017) Mixotrophic cultivation of chlorella for local protein production using agro-food by-products. Bioresour Technol 230:82–89

    Article  CAS  Google Scholar 

  17. Guillard RRL (1975) Culture of phytoplankton for feeding marine invertebrates. In: Smith WL, Chanley MH (eds) Culture of marine invertebrate animals. Plenum Press, New York

    Google Scholar 

  18. Guillard RRL, Ryther JH (1962) Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt and Detonula confervacea Cleve. Can J Microbiol 8:229–239

    Article  CAS  Google Scholar 

  19. Dragone G, Mussatto SI, Almeida JB, Teixeira JA (2011) Optimal fermentation conditions for maximizing the ethanol production by Kluyveromyces fragilis from cheese whey powder. Biomass Bioenerg 35:1977–1982. https://doi.org/10.1016/j.biombioe.2011.01.045

    Article  CAS  Google Scholar 

  20. Abreu AP, Fernandes B, Vicente AA, Teixeira J, Dragone G (2012) Mixotrophic cultivation of Chlorella vulgaris using industrial dairy waste as organic carbon source. Bioresour Technol 118:61–66

    Article  CAS  Google Scholar 

  21. Espinosa-Gonzalez I, Parashar A, Bressler DC (2014) Heterotrophic growth and lipid accumulation of Chlorella protothecoides in whey permeate, a dairy by-product stream, for biofuel production. Bioresour Technol 155:170–176

    Article  CAS  Google Scholar 

  22. IRSA, CNR (1994) Analytical methods for Water Analysis (in Italian). Quaderni N. 100 Istituto Poligrafico e Zecca dello Stato, Rome, Italy

  23. Templeton DW, Laurens LML (2015) Nitrogen-to-protein conversion factors revisited for applications of microalgal biomass conversion to food, feed and fuel. Algal Res 11:359–367

    Article  Google Scholar 

  24. DuBois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356

    Article  CAS  Google Scholar 

  25. Palmero D, Iglesias C, de Cara M, Lomas T, Santos M, Tello JC (2009) Isolated from River and Sea Water of Southeastern Spain and pathogenicity on four plant species. Plant Dis 93:377–385

    Article  CAS  Google Scholar 

  26. Gim GH, Ryu J, Kim MJ, Il Kim P, Kim SW (2016) Effects of carbon source and light intensity on the growth and total lipid production of three microalgae under different culture conditions. J Ind Microbiol Biotechnol 43:605–616

    Article  CAS  Google Scholar 

  27. Sforza E, Cipriani R, Morosinotto T, Bertucco A, Giacometti GM (2012) Excess CO2 supply inhibits mixotrophic growth of Chlorella protothecoides and Nannochloropsis salina. Bioresour Technol 104:523–529

    Article  CAS  Google Scholar 

  28. Xu F, Cai ZL, Cong W, Ouyang F (2004) Growth and fatty acid composition of Nannochloropsis sp. grown mixotrophically in fed-batch culture. Biotechnol Lett 26:1319–1322

    Article  CAS  Google Scholar 

  29. Xu F, Hu H, Cong W, Cai Z, Ouyang F (2004) Growth characteristics and eicosapentaenoic acid production by Nannochloropsis sp. in mixotrophic conditions. Biotechnol Lett 26:51–53

    Article  CAS  Google Scholar 

  30. Cheirsilp B, Torpee S (2012) Enhanced growth and lipid production of microalgae under mixotrophic culture condition: effect of light intensity, glucose concentration and fed-batch cultivation. Bioresour Technol 110:510–516

    Article  CAS  Google Scholar 

  31. Das P, Aziz SS, Obbard JP (2011) Two phase microalgae growth in the open system for enhanced lipid productivity. Renew Energy 36:2524–2528

    Article  CAS  Google Scholar 

  32. Hu H, Gao K (2003) Optimization of growth and fatty acid composition of a unicellular marine picoplankton Nannochloropsis sp., with enriched carbon sources. Biotechnol Lett 25:421–425

    Article  CAS  Google Scholar 

  33. Park KC, Whitney C, McNichol JC, Dickinson KE, MacQuarrie S, Skrupski BP, Zou J, Wilson KE, O’Leary SJB, McGinn PJ (2012) Mixotrophic and photoautotrophic cultivation of 14 microalgae isolates from Saskatchewan, Canada: potential applications for wastewater remediation for biofuel production. J Appl Phycol 24:339–348

    Article  CAS  Google Scholar 

  34. Wan M, Liu P, Xia J, Rosenberg JN, Oyler GA, Betenbaugh MJ, Nie Z (2011) The effect of mixotrophy on microalgal growth, lipid content, and expression levels of three pathway genes in Chlorella sorokiniana. Appl Microbiol Biotechnol 91:835–844

    Article  CAS  Google Scholar 

  35. Cerón García MC, Sánchez Mirón A, Fernández Sevilla JM, Molina Grima E, García Camacho F (2005) Mixotrophic growth of the microalga Phaeodactylum tricornutum: influence of different nitrogen and organic carbon sources on productivity and biomass composition. Process Biochem 40:297–305

    Article  CAS  Google Scholar 

  36. Heredia-Arroyo T, Wei R, Ruan W, Hu B (2011) Mixotrophic cultivation of Chlorella vulgaris and its potential application for the oil accumulation from non-sugar materials. Biomass Bioenerg 35:2245–2253

    Article  CAS  Google Scholar 

  37. Ip PF, Wong KH, Chen F (2004) Enhanced production of astaxanthin by the green microalga Chlorella zofingiensis in mixotrophic culture. Process Biochem 39:1761–1766

    Article  CAS  Google Scholar 

  38. Liang Y, Sarkany N, Cui Y (2009) Biomass and lipid productivities of Chlorella vulgaris under autotrophic, heterotrophic and mixotrophic growth conditions. Biotechnol Lett 31:1043–1049

    Article  CAS  Google Scholar 

  39. Andruleviciute V, Makareviciene V, Skorupskaite V, Gumbyte M (2014) Biomass and oil content of Chlorella sp., Haematococcus sp., Nannochloris sp. and Scenedesmus sp. under mixotrophic growth conditions in the presence of technical glycerol. J Appl Phycol 26:83–90

    Article  CAS  Google Scholar 

  40. Li Z, Sun M, Li Q, Li A, Zhang C (2012) Profiling of carotenoids in six microalgae (Eustigmatophyceae) and assessment of their carotene productions in bubble column photobioreactor. Biotechnol Lett 34:2049–2053. https://doi.org/10.1007/s10529-012-0996-2

    Article  PubMed  CAS  Google Scholar 

  41. Minhas AK, Hodgson P, Barrow CJ, Adholeya A (2016) A review on the assessment of stress conditions for simultaneous production of microalgal lipids and carotenoids. Front Microbiol 7:1–19

    Article  Google Scholar 

  42. Blifernez O (2012) Molecular mechanisms behind the adjustment of phototrophic light-harvesting and mixotrophic utilization of cellulosic carbon sources in Chlamydomonas reinhardti. P.h.D Thesis pp 91

Download references

Acknowledgements

The Cariplo Foundation, Italy, financially supported this research in relation to the DANCE (2014-0587) project.

Author information

Authors and Affiliations

  1. Gruppo Ricicla-DiSAA, Università Degli Studi Di Milano, Via Celoria 2, 20133, Milan, Italy

    Davide Veronesi, Giuliana D’Imporzano, Silvia Salati & Fabrizio Adani

  2. CNR, Milan, Italy

    Barbara Menin

Authors
  1. Davide Veronesi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Giuliana D’Imporzano
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Barbara Menin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Silvia Salati
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Fabrizio Adani
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Fabrizio Adani.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Veronesi, D., D’Imporzano, G., Menin, B. et al. Organic wastes/by-products as alternative to CO2 for producing mixotrophic microalgae enhancing lipid production. Bioprocess Biosyst Eng 43, 1911–1919 (2020). https://doi.org/10.1007/s00449-020-02381-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00449-020-02381-x

Keywords

Search

Navigation