BioEnergy Research

, Volume 8, Issue 4, pp 1647–1660 | Cite as

Dairy Wastewaters for Algae Cultivation, Polyhydroxyalkanote Reactor Effluent Versus Anaerobic Digester Effluent

  • Maxine Passero
  • Ben Cragin
  • Erik R. Coats
  • Armando G. McDonald
  • Kevin FerisEmail author


Nutrients in dairy wastewaters can be remediated through assimilation into algal biomass. Anaerobically digested manure creates an effluent (ADE) that is useful for algal cultivation while alternate processing of manure through a polyhydroxyalkanoate reactor generates a distinct effluent (PHAE), not previously characterized for algal cultivation. Each effluent was evaluated for growth rate, biomass production, and nutrient recovery using type algae species Chlorella vulgaris. Growth rates were elevated in 5, 10, and 20 % dilutions of PHAE (0.59, 0.53, 0.42 days−1) compared to equal concentrations of ADE (0.40, 0.36, 0.37 days−1). In addition, the growth phase lasted up to twice as long for PHAE, resulting in a fourfold higher stationary phase algal concentration (cells∙mL−1) compared to ADE. Growth in ADE was limited by specific inhibitory properties: high concentrations of dissolved organic matter, ammonia, and elevated bacterial load. Maximum nutrient removal rates for ADE and PHAE were 0.95 and 3.46 mg·L−1·day−1 for nitrogen and 0.67 and 0.04 mg·L−1·day−1 for phosphorus, respectively. Finally, biomass derived from PHAE was higher in lipids (11.3 % versus 7.2 %) and thus has a greater potential as a feedstock for biofuel compared to ADE.


Algae Biofuel Dairy wastewater Anaerobic digester Polyhydroxyalkanoate 



Anaerobic digester


Anaerobic digester effluent


Colony forming unit




Chemical oxygen demand


Carbon dioxide equivalent


Dissolved organic matter


Energy return on investment


Greenhouse gas










Polyhydroxyalkanoate reactor effluent




Renewable fuel standard


Standard deviation


Total dissolved phosphorus


Total dissolved nitrogen


Total solids


Volatile fatty acid



This research was funded in part by the Idaho National Laboratory (INL) and the Center for Advanced Energy Studies (CAES), 00041394 Task Order 33. Additional funding was provided by the Environmental Protection Agency (EPA), Science to Achieve Results (STAR) graduate fellowship, 2011–2013. FP-91736101, and the United States Department of Agriculture National Institute of Food and Agriculture (USDA-NIFA) award number 2012–68002–19952.


  1. 1.
    National Research Council (U.S.). Committee on the Sustainable Development of Algal Biofuels., National Research Council (U.S.). Board on Agriculture and Natural Resources., National Research Council (U.S.). Board on Energy and Environmental Systems., National Academies Press (U.S.), Sustainable development of algal biofuels in the United States, National Academies Press, Washington, D.C. 2012Google Scholar
  2. 2.
    Liebrand CB, Ling KC (2009) Research Report 217Google Scholar
  3. 3.
    United States, SCS (2012) Agricultural waste management field handbookGoogle Scholar
  4. 4.
    Pate R, Klise G, Wu B (2011) Resource demand implications for US algae biofuels production scale-up. Appl Energy 88:3377–3388CrossRefGoogle Scholar
  5. 5.
    Craggs R, Heubeck S, Lundquist T, Benemann J (2011) Algal biofuels from wastewater treatment high rate algal ponds. Water Sci Technol 63(4):660–665CrossRefPubMedGoogle Scholar
  6. 6.
    Massingill M, Carlbert J, Schwartz G, Van Olst J, et al (2008) Algae Biomass Summit, Seattle, WAGoogle Scholar
  7. 7.
    U.S. Energy Information Administration, U.S (2013) Department of EnergyGoogle Scholar
  8. 8.
    Innovation Center for U.S (2011) DairyGoogle Scholar
  9. 9.
    Coats ER, Loge FJ, Wolcott MP, Englund K, McDonald AG (2007) Synthesis of polyhydroxyalkanoates in municipal wastewater treatment. Water Environ Res 79:2396–2403CrossRefPubMedGoogle Scholar
  10. 10.
    Liu HY, Hall PV, Darby JL, Coats ER et al (2008) Production of polyhydroxyalkanoate during treatment of tomato cannery wastewater. Water Environ Res 80:367–372CrossRefPubMedGoogle Scholar
  11. 11.
    Wei L, Guho NM, Coats ER, McDonald AG (2014) Characterization of poly(3-hydroxybutyrate-co-3-hydroxyvalerate) biosynthesized by mixed microbial consortia fed fermented dairy manure. J Appl Polymer Sci. 131, n/a-n/aGoogle Scholar
  12. 12.
    Coats ER, Searcy E, Feris K, Shrestha D et al (2013) An integrated two-stage anaerobic digestion and biofuel production process to reduce life cycle GHG emissions from US dairies. Biofuels Bioprod Biorefin 7:459–473CrossRefGoogle Scholar
  13. 13.
    Wang L, Li Y, Chen P, Min M et al (2010) Anaerobic digested dairy manure as a nutrient supplement for cultivation of oil-rich green microalgae Chlorella sp. Bioresour Technol 101:2623–2628CrossRefPubMedGoogle Scholar
  14. 14.
    Bosco F, Chiampo F (2010) Production of polyhydroxyalcanoates (PHAs) using milk whey and dairy wastewater activated sludge: production of bioplastics using dairy residues. J Biosci Bioeng 109:418–421CrossRefPubMedGoogle Scholar
  15. 15.
    Coats ER, Gregg M, Crawford RL (2011) Effect of organic loading and retention time on dairy manure fermentation. Bioresour Technol 102:2572–2577CrossRefPubMedGoogle Scholar
  16. 16.
    Christenson L, Sims R (2011) Production and harvesting of microalgae for wastewater treatment, biofuels, and bioproducts. Biotechnol Adv 29:686–702CrossRefPubMedGoogle Scholar
  17. 17.
    Coats ER, Searcy E, Feris K, Shrestha D, et al (2013) An integrated two-stage anaerobic digestion and biofuel production process to reduce life cycle GHG emissions from US dairies. Biofuels Bioprod BiorefinGoogle Scholar
  18. 18.
    Sooknah RD, Wilkie AC (2004) Nutrient removal by floating aquatic macrophytes cultured in anaerobically digested flushed dairy manure wastewater. Ecol Eng 22:27–42CrossRefGoogle Scholar
  19. 19.
    Kebede-Westhead E, Pizarro C, Mulbry WW (2003) Production and nutrient removal by periphyton growth under different loading rates of anaerobically digested flushed dairy manure. J Phycol 39:1275–1282CrossRefGoogle Scholar
  20. 20.
    University of Texas Culture Collection (2013) University of TexasGoogle Scholar
  21. 21.
    Hipkins M (1986) Photosynthesis energy transduction a practical approach. IRL press, OxfordGoogle Scholar
  22. 22.
    Osman NB, McDonald AG, Laborie M-PG (2012) Analysis of DCM extractable components from hot-pressed hybrid poplar. Holzforschung 68:927–934Google Scholar
  23. 23.
    Chakraborty M, McDonald AG, Nindo C, Chen S (2013) An α-glucan isolated as a co-product of biofuel by hydrothermal liquefaction of Chlorella sorokiniana biomass. Algal Res 2:230–236CrossRefGoogle Scholar
  24. 24.
    Slocombe SP, Ross M, Thomas N, McNeill S, Stanley MS (2013) A rapid and general method for measurement of protein in micro-algal biomass. Bioresour Technol 129:51–57CrossRefPubMedGoogle Scholar
  25. 25.
    Reardon J, Foreman JA, Searcy RL (1966) New reactants for the colorimetric determination of ammonia. Clin Chim Acta Int J Clin Chem 14:203CrossRefGoogle Scholar
  26. 26.
    Largeau C, Casadevall E, Berkaloff C, Dhamelincourt P (1980) Sites of accumulation and composition of hydrocarbons in Botryococcus braunii. Phytochemistry 19:1043–1051CrossRefGoogle Scholar
  27. 27.
    Levine RB, Costanza-Robinson MS, Spatafora GA (2011) Neochloris oleoabundans grown on anaerobically digested dairy manure for concomitant nutrient removal and biodiesel feedstock production. Biomass Bioenergy 35:40–49CrossRefGoogle Scholar
  28. 28.
    Chia MA, Lombardi AT, Melano MdGG (2011) World Aquaculture SocietyGoogle Scholar
  29. 29.
    Converti A, Casazza AA, Ortiz EY, Perego P, Del Borghi M (2009) Effect of temperature and nitrogen concentration on the growth and lipid content of < i > Nannochloropsis oculata</i > and < i > Chlorella vulgaris</i > for biodiesel production. Chem Eng Process Process Intensif 48:1146–1151CrossRefGoogle Scholar
  30. 30.
    Biller P, Ross A (2011) Potential yields and properties of oil from the hydrothermal liquefaction of microalgae with different biochemical content. Bioresour Technol 102:215–225CrossRefPubMedGoogle Scholar
  31. 31.
    Behrens PW, Bingham SE, Hoeksema SD, Cohoon DL, Cox JC (1989) J Appl Phycol, pp. 123–130Google Scholar
  32. 32.
    Dragone G, Fernandes BD, Abreu AP, Vicente AA, Teixeira JA (2011) Nutrient limitation as a strategy for increasing starch accumulation in microalgae. Appl Energy 88:3331–3335CrossRefGoogle Scholar
  33. 33.
    Ross AB, Biller P, Kubacki ML, Li H et al (2010) Hydrothermal processing of microalgae using alkali and organic acids. Fuel 89:2234–2243CrossRefGoogle Scholar
  34. 34.
    Pehlivanoglu E, Sedlak DL (2004) Bioavailability of wastewater-derived organic nitrogen to the alga Selenastrum Capricornutum. Water Res 38:3189–3196CrossRefPubMedGoogle Scholar
  35. 35.
    Francko DA, Heath RT (1982) UV-sensitive complex phosphorus: association with dissolved humic material and iron in a bog lake. Limnol Oceanogr 27:564–569CrossRefGoogle Scholar
  36. 36.
    Jensen HS, Andersen FO (1992) Importance of temperature, nitrate, and pH for phosphate release from aerobic sediments of four shallow, eutrophic lakes. Limnol Oceanogr 37:577–589CrossRefGoogle Scholar
  37. 37.
    Pittman JK, Dean AP, Osundeko O (2011) The potential of sustainable algal biofuel production using wastewater resources. Bioresour Technol 102:17–25CrossRefPubMedGoogle Scholar
  38. 38.
    Bolier G, Donze M (1989) On the accuracy and interpretation of growth curves of planktonic algae. Hydrobiologia 188:175–179CrossRefGoogle Scholar
  39. 39.
    Liu X, Duan S, Li A, Xu N et al (2009) Effects of organic carbon sources on growth, photosynthesis, and respiration of Phaeodactylum tricornutum. J Appl Physiol 21:239–246Google Scholar
  40. 40.
    Liang Y, Sarkany N, Cui Y (2009) Biomass and lipid productivities of Chlorella vulgaris under autotrophic, heterotrophic and mixotrophic growth conditions. Biotechnol Lett 31:1043–1049CrossRefPubMedGoogle Scholar
  41. 41.
    Sonzogni WC, Chapra SC, Armstrong DE, Logan TJ (1982) Bioavailability of phosphorus inputs to lakes. J Environ Qual 11:555–563CrossRefGoogle Scholar
  42. 42.
    Källqvist T, Svenson A (2003) Assessment of ammonia toxicity in tests with the microalga, Nephroselmis pyriformis, Chlorophyta. Water Res 37:477–484CrossRefPubMedGoogle Scholar
  43. 43.
    Abeliovich A, Azov Y (1976) Toxicity of ammonia to algae in sewage oxidation ponds. Appl Environ Microbiol 31:801–806PubMedCentralPubMedGoogle Scholar
  44. 44.
    Uludag-Demirer S, Demirer GN, Chen S (2005) Ammonia removal from anaerobically digested dairy manure by struvite precipitation. Process Biochem 40:3667–3674CrossRefGoogle Scholar
  45. 45.
    Jansson M (1988) Phosphate uptake and utilization by bacteria and algae, Phosphorus in Freshwater Ecosystems, Springer, pp. 177–189Google Scholar
  46. 46.
    Currie DJ, Kalff J (1984) A comparison of the abilities of freshwater algae and bacteria to acquire and retain phosphorus. Limnol Oceanogr 29:298–310CrossRefGoogle Scholar
  47. 47.
    Currie DJ, Kalff J (1984) Can bacteria outcompete phytoplankton for phosphorus? A chemostat test. Microb Ecol 10:205–216CrossRefPubMedGoogle Scholar
  48. 48.
    Currie DJ, Kalff J (1984) The relative importance of bacterioplankton and phytoplankton in phosphorus uptake in freshwater. Limnol Oceanogr 29:311–321CrossRefGoogle Scholar
  49. 49.
    Davies-Colley R, Craggs R, Park J, Nagels J (2005) Optical characteristics of waste stabilization ponds: recommendations for monitoring. Water Sci Technol 51:153–161PubMedGoogle Scholar
  50. 50.
    Bährs H, Steinberg CEW (2012) Impact of two different humic substances on selected coccal green algae and cyanobacteria—changes in growth and photosynthetic performance. Environ Sci Pollut Res 19:335–346CrossRefGoogle Scholar
  51. 51.
    Yun YS, Park JM (2001) Attenuation of monochromatic and polychromatic lights in Chlorella vulgaris suspensions. Appl Microbiol Biotechnol 55:765–770CrossRefPubMedGoogle Scholar
  52. 52.
    Engler CR, Jordan ER, McFarland MJ, Lacewell RD (2003) Economics and environmental impact of biogas production as a manure management strategy. Department of Agricultural Engineering, Texas A&M UniversityGoogle Scholar
  53. 53.
    Wilkie AC, Mulbry WW (2002) Recovery of dairy manure nutrients by benthic freshwater algae. Bioresour Technol 84:81–91CrossRefPubMedGoogle Scholar
  54. 54.
    Mulbry W, Westhead EK, Pizarro C, Sikora L (2005) Recycling of manure nutrients: use of algal biomass from dairy manure treatment as a slow release fertilizer. Bioresour Technol 96:451–458CrossRefPubMedGoogle Scholar
  55. 55.
    Sialve B, Bernet N, Bernard O (2009) Anaerobic digestion of microalgae as a necessary step to make microalgal biodiesel sustainable. Biotechnol Adv 27:409–416CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Maxine Passero
    • 1
  • Ben Cragin
    • 1
  • Erik R. Coats
    • 2
  • Armando G. McDonald
    • 3
  • Kevin Feris
    • 1
    Email author
  1. 1.Department of Biological SciencesBoise State UniversityBoiseUSA
  2. 2.Department of Civil EngineeringUniversity of IdahoMoscowUSA
  3. 3.Department of Forest, Rangeland and Fire SciencesUniversity of IdahoMoscowUSA

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