Heterotrophic microalgae production on food waste and by-products

  • Stephan S. W. EndeEmail author
  • Anja Noke


The present review provides an overview of the latest research on microalgae production techniques based on carbon instead of light as energy source. The independence of light in mixotrophic and heterotrophic cultivation considerably reduces production costs and space compared to autotrophic production. Hence, this production technique may play a key role to meet future increasing food and feed demands. In order to reach this aim, it is, however, necessary to explore the possibilities of utilizing low-cost carbon sources such as molasses from industrial waste streams. This review provides an overview of worldwide potentially available low-cost carbon sources, potential microalgae species and their chemical composition, available pre-treatment methods for media sterilization and enhanced bioavailability, latest literature on growth of heterotrophic microalgae cultured on new, innovative low cost carbon sources, non-sterile culture approaches, and finally, economic considerations including a future outlook.


Heterotrophic microalgae Aquaculture Chlorella Waste stream By-products 



The authors would like to thank all students and technical assistants participating in the virtual biotechnology company “TiGer BioTec” of the International Degree Course Industrial and Environmental Biology ISTAB (B.Sc.) at the University of Applied Sciences Bremen (Germany).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Blimling, Associates (2017). Ingredient digest, vol 2Google Scholar
  2. Bumbak F, Cook S, Zachleder V, Hauser S, Kovar K (2011) Best practices in heterotrophic high-cell-density microalgal processes: achievements, potential and possible limitations. Appl Microbiol Biotechnol 91:31–46CrossRefGoogle Scholar
  3. Cripps SJ, Bergheim A (2000) Solids management and removal for intensive land-based aquaculture production systems. Aquac Eng 22:33–56CrossRefGoogle Scholar
  4. El-Sheekh MM, Bedaiwy MY, Osman ME, Ismail MM (2014) Influence of molasses on growth, biochemical composition and ethanol production of the green algae Chlorella vulgaris and Scenedesmus obliquus. Journal of Agricultural Engineering and Biotechnology 2:20–28CrossRefGoogle Scholar
  5. Endo H, Nakajima K, Chino R, Shirota M (1974) Growth characteristics and cellular components of Chlorella regularis, heterotrophic fast growing strain. Agric Biol Chem 38:9–18CrossRefGoogle Scholar
  6. Enzing C, Sijtsma L, Parisi C, Vigani M, Barbosa M, Ploeg M, Rodrigues Cerezo E (2014) Microalgae-based products for the food and feed sector: an outlook for Europe. European Commission. LuxembourgGoogle Scholar
  7. 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 155:170–176CrossRefGoogle Scholar
  8. FAO (2014) The state of the world fisheries and aquaculture. Food and Agriculture Organization of the United Nations, RomeGoogle Scholar
  9. FAO (2017) The global initiative on food loss and waste reduction. Food and Agriculture Organization of the United Nations, RomeGoogle Scholar
  10. Gami B, Patel JP, Kothari IL (2014) Cultivation of Chlorella protothecoides (ISIBES -101) under autotrophic and heterotrophic conditions for biofuel production. J Algal Biomass Utln 5:20–29Google Scholar
  11. Graziani G, Schiavo S, Nicolai MA, Buono S, Fogliano V, Pinto G, Pollio A (2013) Microalgae as human food: chemical and nutritional characteristics of the thermo-acidophilic microalga Galdieria sulphuraria. Food Funct 4:144–152CrossRefGoogle Scholar
  12. Gross W (1999) Revision of comparative traits for the acido-and thermophilic red algae Cyanidium and Galdieria. In: Seckbach J (ed) Enigmatic microorganisms and life in extreme environments. Vol 1. Springer, Berlin pp 437–446Google Scholar
  13. Gross W, Schnarrenberger C (1995) Heterotrophic growth of two strains of the acido-thermophilic red alga Galdieria sulphuraria. Plant Cell Physiol 36:633–638Google Scholar
  14. Guerrero AB, Aguado PL, Sánchez J, Curt MD (2016) GIS-based assessment of banana residual biomass potential for ethanol production and power generation: a case study. Waste Biomass Valori 7:405–415CrossRefGoogle Scholar
  15. Harel M, Clayton D (2004) Feed formulation for terrestrial and aquatic animals. WO patent application WO/2004/080196 (23/09/2004)Google Scholar
  16. Hayes RJ (2014) Cost of quality (CoQ) - an analysis of the cost of maintaining a state of compliance. International Pharmaceutical Industry 6:74–76Google Scholar
  17. Heritage J, Evans EGV, Killington RA (1997) Introductory microbiology. Cambridge University Press, CambridgeGoogle Scholar
  18. Informa (2018) World molasses feed and ingredient report. Informa PLC. Accessed 15 Nov 2018
  19. Jelen P (2009) Dried whey, whey proteins, lactose and lactose derivative products. In: Tamime AY (ed) Dairy powders and concentrated products. Blackwell, Oxford, pp 255–267CrossRefGoogle Scholar
  20. Kotrbáček V, Doubek J, Doucha J (2015) The chlorococcalean alga Chlorella in animal nutrition: a review. J Appl Phycol 27:2173–2180CrossRefGoogle Scholar
  21. Lau KY, Pleissner D, Lin CSK (2014) Recycling of food waste as nutrients in Chlorella vulgaris cultivation. Bioresour Technol 170:144–151CrossRefGoogle Scholar
  22. Leesing R, Kookkhunthod S (2011) Heterotrophic growth of Chlorella sp. KKU-S2 for lipid production using molasses as a carbon substrate. In: Proceedings of the International Conference on Food Engineering and Biotechnology, 2011. IACSIT Press, Singapore pp 87–91Google Scholar
  23. Liu J, Sun Z, Zhong Y, Gerken H, Huang J, Chen F (2013) Utilization of cane molasses towards cost-saving astaxanthin production by a Chlorella zofingiensis mutant. J Appl Phycol 25:1447–1456CrossRefGoogle Scholar
  24. Miao X, Wu Q (2006) Biodiesel production from heterotrophic microalgal oil. Bioresour Technol 97:841–846CrossRefGoogle Scholar
  25. Mohapatra D, Mishra S, Sutar N (2010) Banana and its by-product utilisation: An overview. J Sci Indust Res 69:323–329Google Scholar
  26. Oesterhelt C, Schnarrenberger C, Gross W (1999) Characterization of a sugar/polyol uptake system in the red alga Galdieria sulphuraria. Eur J Phycol 34:271–277CrossRefGoogle Scholar
  27. Øverland M, Karlsson A, Mydland LT, Romarheim OH, Skrede A (2013) Evaluation of Candida utilis, Kluyveromyces marxianus and Saccharomyces cerevisiae yeasts as protein sources in diets for Atlantic salmon (Salmo salar). Aquaculture 402:1–7CrossRefGoogle Scholar
  28. Panesar PS, Kennedy JF (2012) Biotechnological approaches for the value addition of whey. Crit Rev Biotechnol 32:327–348CrossRefGoogle Scholar
  29. Pérez R (1997) Feeding pigs in the tropics. Ministry of Sugar, Havana, CubaGoogle Scholar
  30. Perez-Garcia O, Escalante FM, de-Bashan LE, Bashan Y (2011) Heterotrophic cultures of microalgae: metabolism and potential products. Water Res 45:11–36CrossRefGoogle Scholar
  31. Pleissner D, Rumpold BA (2018) Utilization of organic residues using heterotrophic microalgae and insects. Waste Manag 72:227–239CrossRefGoogle Scholar
  32. Pleissner D, Venus J (2014) Agricultural residues as feedstocks for lactic acid fermentation. In: Green technologies for the environment, vol 1186. ACS Symposium Series, vol 1186. American Chemical Society, pp 247–263Google Scholar
  33. Pulz O, Gross W (2004) Valuable products from biotechnology of microalgae. Appl Microbiol Biotechnol 65:635–648CrossRefGoogle Scholar
  34. Radmer RJ, Parker BC (1994) Commercial applications of algae: opportunities and constraints. J Appl Phycol 6:93–98CrossRefGoogle Scholar
  35. Rigano C, Fuggi A, Rigano VDM, Aliotta G (1976) Studies on utilization of 2-ketoglutarate, glutamate and other amino acids by the unicellular alga Cyanidium caldarium. Arch Microbiol 107:133–138CrossRefGoogle Scholar
  36. Rigano C, Aliotta G, Rigano VDM, Fuggi A, Vona V (1977) Heterotrophic growth patterns in the unicellular alga Cyanidium caldarium. Arch Microbiol 113:191–196CrossRefGoogle Scholar
  37. Rodehutscord M, Jacobs S, Pack M, Pfeffer E (1995a) Response of rainbow trout (Oncorhynchus mykiss) growing from 50 to 150 g to supplements of DL-methionine in a semipurified diet containing low or high levels of cystine. J Nutr 125:964–969PubMedGoogle Scholar
  38. Rodehutscord M, Jacobs S, Pack M, Pfeffer E (1995b) Response of rainbow trout (Oncorhynchus mykiss) growing from 50 to 170 g to supplements of either L-arginine or L-threonine in a semipurified diet. J Nutr 125:970–975PubMedGoogle Scholar
  39. Rodehutscord M, Becker A, Pack M, Pfeffer E (1997) Response of rainbow trout (Oncorhynchus mykiss) to supplements of individual essential amino acids in a semipurified diet, including an estimate of the maintenance requirement for essential amino acids. J Nutr 127:10CrossRefGoogle Scholar
  40. Selvaratnam T, Pegallapati AK, Montelya F, Rodriguez G, Nirmalakhandan N, Van Voorhies W, Lammers PJ (2014) Evaluation of a thermo-tolerant acidophilic alga, Galdieria sulphuraria, for nutrient removal from urban wastewaters. Bioresour Technol 156:395–399CrossRefGoogle Scholar
  41. Sharma YC, Singh B, Korstad J (2011) A critical review on recent methods used for economically viable and eco-friendly development of microalgae as a potential feedstock for synthesis of biodiesel. Green Chem 13:2993–3006CrossRefGoogle Scholar
  42. Shelly K, Higgins T, Beardall J, Wood B, McNaughton D, Heraud P (2007) Characterising nutrient-induced fluorescence transients (NIFTs) in nitrogen-stressed Chlorella emersonii (Chlorophyta). Phycologia 46:503–512CrossRefGoogle Scholar
  43. Shen Y, Yuan W, Pei Z, Mao E (2010) Heterotrophic culture of Chlorella protothecoides in various nitrogen sources for lipid production. Appl Biochem Biotechnol 160:1674–1684CrossRefGoogle Scholar
  44. Sheth K (2017) Top banana producing countries in the world. World Atlas. Accessed 25 Apr 2017
  45. USDA (2016) Statistics report 09040, bananas, raw. National Nutrient Database for Standard Reference, USDA Food Composition DatabasesGoogle Scholar
  46. Vidotti DSA, Coelho R, Franco ML, Franco T (2014) Miniaturized culture for heterotrophic microalgae using low cost carbon sources as a tool to isolate fast and economical strains. Chem Eng Trans 38:325–330Google Scholar
  47. Vítová M, Goecke F, Sigler K, Řezanka T (2016) Lipidomic analysis of the extremophilic red alga Galdieria sulphuraria in response to changes in pH. Algal Res 13:218–226CrossRefGoogle Scholar
  48. Wai N (1955) Effects of some antiseptics on the growth of Chlorella. Physiol Plant 8:71–73CrossRefGoogle Scholar
  49. Wen Z-Y, Chen F (2003) Heterotrophic production of eicosapentaenoic acid by microalgae. Biotechnol Adv 21:273–294CrossRefGoogle Scholar
  50. WHO/UNU (2007) Protein and amino acid requirements in human nutrition, WHO Technical Reports Series 935Google Scholar
  51. Winkler B, Tosi H, Webster AJF, Resende FD, Oliveira AAMA, Villela LCV (2011) Dried yeast (Saccharomyces cerevisae) as a protein source for horses. Livest Sci 137:168–177CrossRefGoogle Scholar
  52. Xie T, Sun Y, Du K, Liang B, Cheng R, Zhang Y (2012) Optimization of heterotrophic cultivation of Chlorella sp. for oil production. Bioresour Technol 118:235–242CrossRefGoogle Scholar
  53. Xie T, Xia Y, Zeng Y, Li X, Zhang Y (2017) Nitrate concentration-shift cultivation to enhance protein content of heterotrophic microalga Chlorella vulgaris: over-compensation strategy. Bioresour Technol 233:247–255CrossRefGoogle Scholar
  54. Zepka LQ, Jacob-Lopes E, Goldbeck R, Souza-Soares LA, Queiroz MI (2010) Nutritional evaluation of single-cell protein produced by Aphanothece microscopica Nägeli. Bioresour Technol 101:7107–7111CrossRefGoogle Scholar
  55. Zhao J, Fleet GH (2005) Degradation of RNA during the autolysis of Saccharomyces cerevisiae produces predominantly ribonucleotides. J Ind Microbiol Biotechnol 32:415–423CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Helmholtz Centre for Polar and Marine ResearchAlfred Wegener InstituteBremerhavenGermany
  2. 2.Faculty of Architecture, Construction and EnvironmentUniversity of Applied SciencesBremenGermany

Personalised recommendations