Skip to main content
Log in

Heterotrophic and mixotrophic cultivation of microalgae for biodiesel production in agricultural wastewaters and associated challenges—a critical review

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

Many studies have demonstrated that heterotrophic and mixotrophic growth for various microalgae species yields greater biomass and lipid content as compared to photoautotrophic cultivation. This review explores the possibility of leveraging the natural ability of the microorganisms to metabolize carbon heterotrophically and mixotrophically in agricultural wastewaters. This has the potential advantage of improving the overall economics for the production of biodiesel and value-added biomolecules from microalgae, mitigating an existing waste stream and minimizing water requirements. However, there are a number of challenges and gaps in scientific knowledge that suggest a need for ongoing research in the area. In this review, specific focus is dedicated to the metabolic mechanisms, reported performances, and practical challenges that contribute to the uncertainty of employing agricultural wastewaters for heterotrophic and mixotrophic microalgae cultures.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Ahn JH, Do TH, Kim SD, Hwang S (2006) The effect of calcium on the anaerobic digestion treating swine wastewater. Biochem Eng J 30:33–38

    CAS  Google Scholar 

  • Amer L, Adhikari B, Pellegrino J (2011) Technoeconomic analysis of five microalgae-to-biofuels processes of varying complexity. Bioresour Technol 102:9350–9359

    CAS  PubMed  Google Scholar 

  • Anderson RA (ed) (2005) Algae Culturing Techniques. Elsevier Academic Press, NY

    Google Scholar 

  • Appels L, Baeyens J, Degrève J, Dewil R (2008) Principles and potential of the anaerobic digestion of waste-activated sludge. Prog Energ Combust 34:755–781

    CAS  Google Scholar 

  • Arbeli Z, Brenner A, Abeliovich A (2006) Treatment of high-strength dairy wastewater in an anaerobic deep reservoir: analysis of the methanogenic fermentation pathway and the rate-limiting step. Water Res 40:3653–3659

    CAS  PubMed  Google Scholar 

  • Barsanti L, Gualtieri P (2006) Algae: anatomy, biochemistry, and biotechnology. CRC Press, Boca Raton

    Google Scholar 

  • Ben W, Qiang Z, Adams C, Zhang H, Chen L (2008) Simultaneous determination of sulfonamides, tetracyclines and tiamulin in swine wastewater by solid-phase extraction and liquid chromatography-mass spectrometry. J Chromatogr 1202:173–180

    CAS  Google Scholar 

  • Bhatnagar A, Chinnasamy S, Singh M, Das KC (2011) Renewable biomass production by mixotrophic algae in the presence of various carbon sources and wastewaters. Appl Energ 88:3425–3431

    CAS  Google Scholar 

  • Bohutskyi P, Kula T, Kessler BA, Hong Y, Bouwer EJ, Betenbaugh MJ, Allnutt FCT (2014) Mixed trophic state production process for microalgal biomass with high lipid content for generating biodiesel and biogas. Bioenerg Res 1–12

  • Borowitzka MA (1999) Commercial production of microalgae: ponds, tanks, tubes and fermenters. J Biotechnol 70:313–321

    CAS  Google Scholar 

  • Borowitzka MA (2013) High-value products from microalgae—their development and commercialisation. J Appl Phycol 25:743–756

    CAS  Google Scholar 

  • Brennan L, Owende P (2010) Biofuels from microalgae—a review of technologies for production, processing, and extractions of biofuels and co-products. Ren Sust Energ Rev 14:557–577

    CAS  Google Scholar 

  • 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 91:31–46

    CAS  PubMed Central  PubMed  Google Scholar 

  • Burkholder JM, Glibert PM, Skelton HM (2008) Mixotrophy, a major mode of nutrition for harmful algal species in eutrophic waters. Harmful Algae 8:77–93

    CAS  Google Scholar 

  • Campbell PK, Beer T, Batten D (2011) Life cycle assessment of biodiesel production from microalgae in ponds. Bioresour Technol 102:50–56

    CAS  PubMed  Google Scholar 

  • Cañizares-Villanueva RO, Domínguez AR, Cruz MS, Ríos-Leal E (1995) Chemical composition of cyanobacteria grown in diluted, aerated swine wastewater. Bioresour Technol 51:111–116

    Google Scholar 

  • Chang KJL, Rye L, Dunstan GA, Grant T, Koutoulis A, Nichols PD, Blackburn SI (2014) Life cycle assessment: Heterotrophic cultivation of thraustochytrids for biodiesel production. J Appl Phycol. doi:10.1007/s10811-014-0364-9

    Google Scholar 

  • Chen F (1996) High cell density culture of microalgae in heterotrophic growth. Trends Biotech 14:421–426

    CAS  Google Scholar 

  • Chen F, Johns MR (1996) Heterotrophic growth of Chlamydomonas reinhardtii on acetate in chemostat culture. Process Biochem 31:601–604

    CAS  Google Scholar 

  • Chen T, Wang Y (2013) Optimized astaxanthin production in Chlorella zofingiensis under dark condition by response surface methodology. Food Sci Biotechnol 1–8

  • Chen F, Zhang Y (1997) High cell density mixotrophic culture of Spirulina platensis on glucose for phycocyanin production using a fed-batch system. Enzyme Microb Technol 20:221–224

    CAS  Google Scholar 

  • Chen F, Chen H, Gong X (1997) Mixotrophic and heterotrophic growth of Haematococcus lacustris and rheological behaviour of the cell suspensions. Bioresour Technol 62:19–24

    CAS  Google Scholar 

  • Chen C-Y, Yeh K-L, Aisyah R, Lee DJ, Chang JS (2011) Cultivation, photobioreactor design and harvesting of microalgae for biodiesel production: a critical review. Bioresour Technol 102:71–81

    CAS  PubMed  Google Scholar 

  • Chisti Y (2007) Biodiesel from microalgae. Biotehnol Adv 25:294–306

    CAS  Google Scholar 

  • Chisti Y (2013) Constraints to commercialization of algal fuels. J Biotechnol 167:201–214

    CAS  PubMed  Google Scholar 

  • Cole KM, Sheath RG (eds) (1990) Biology of the Red Algae. Cambridge University Press, Cambridge

    Google Scholar 

  • De Bashan LE, Bashan Y (2004) Recent advances in removing phosphorus from wastewater and its future use as fertilizer (1997–2003). Water Res 38:4222–4246

    PubMed  Google Scholar 

  • De Swaaf ME, Sijtsma L, Pronk JT (2003) High-cell-density fed-batch cultivation of the docosahexaenoic acid producing marine alga Crypthecodinium cohnii. Biotechnol Bioeng 81:666–672

    PubMed  Google Scholar 

  • Del Campo J, García-González M, Guerrero M (2007) Outdoor cultivation of microalgae for carotenoid production: current state and perspectives. Appl Microbiol Biot 74:1163–1174

    CAS  Google Scholar 

  • Droop MR (1974) Heterotrophy of Carbon. In: Stewart WDP (ed) Algal Physiology and Biochemistry. Blackwell Scientific, Oxford, pp 530–559

    Google Scholar 

  • Fang X, Wei C, Zhao-Ling C, Fan O (2004) Effects of organic carbon sources on cell growth and eicosapentaenoic acid content of Nannochloropsis sp. J Appl Phycol 16:499–503

    CAS  Google Scholar 

  • Feng Y, Li C, Zhang D (2011) Lipid production of Chlorella vulgaris cultured in artificial wastewater medium. Bioresour Technol 102:101–105

    CAS  PubMed  Google Scholar 

  • Ferguson JL (2002) Characterizing the process of composting mink manure and pelted mink carcasses. Master’s Thesis, Nova Scotia Agricultural College, Truro, Canada

  • Fu R, Wang H, Pei G (2012) A study on lipid production of the mixotrophic microalgae Phaeodactylum tricornutum on various carbon sources. Afr J Microbiol Res 6:1041–1047

    CAS  Google Scholar 

  • Gao C, Zhai Y, Ding Y, Wu Q (2010) Application of sweet sorghum for biodiesel production by heterotrophic microalga Chlorella protothecoides. Appl Energ 87:756–761

    CAS  Google Scholar 

  • García-Fernández JM, De Marsac NT, Diez J (2004) Streamlined regulation and gene loss as adaptive mechanisms in Prochlorococcus for optimized nitrogen utilization in oligotrophic environments. Microbiol Mol Biol Rev 68:630–638

    PubMed Central  PubMed  Google Scholar 

  • Ghaly AE, Kamal M, Mahmoud NS (2005) Phytoremediation of aquaculture wastewater for water recycling and production of fish feed. Environ Int 31:1–13

    CAS  PubMed  Google Scholar 

  • González C, Marciniak J, Villaverde S et al (2008) Microalgae-based processes for the biodegradation of pretreated piggery wastewaters. Appl Microbiol Biotechnol 80:891–898

    PubMed  Google Scholar 

  • Guillen-Jimenez E, Alvarez-Mateos P, Romero-Guzman F, Pereda-Marin J (2000) Bio-mineralization of organic matter in dairy wastewater, as affected by pH. The evolution of ammonium and phosphates. Water Res 34:1215–1224

    CAS  Google Scholar 

  • Hammouda O, Gaber A, Abdelraouf N (1995) Microalgae and wastewater treatment. Ecotox Env Safety 31:205–210

    CAS  Google Scholar 

  • Hunt PG, Szogi AA, Humenik FJ et al (2002) Constructed wetlands for the treatment of swine wastewater from an anaerobic lagoon. Trans ASAE 45:639–647

    CAS  Google Scholar 

  • Ip PF, Chen F (2005) Production of astaxanthin by the green microalga Chlorella zofingiensis in the dark. Process Biochem 40:733–738

    CAS  Google Scholar 

  • Ip P-F, Wong K-H, Chen F (2004) Enhanced production of astaxanthin by the green microalga Chlorella zofingiensis in mixotrophic culture. Process Biochem 39:1761–1766

    CAS  Google Scholar 

  • Kim MK, Choi K-M, Yin C-R, Lee K-Y, Im W-T, Lim JH, Lee S-T (2004) Odorous swine wastewater treatment by purple non-sulfur bacteria, Rhodopseudomonas palustris, isolated from eutrophicated ponds. Biotechnol Lett 26:819–822

    CAS  PubMed  Google Scholar 

  • Kim MK, Park JW, Park CS, Kim SJ, Jeune KH, Chang MU, Acreman J (2007) Enhanced production of Scenedesmus spp. (green microalgae) using a new medium containing fermented swine wastewater. Bioresour Technol 98:2220–2228

    CAS  PubMed  Google Scholar 

  • Kong Q, Li L, Martinez B, Chen P, Ruan R (2010) Culture of microalgae Chlamydomonas reinhardtii in wastewater for biomass feedstock production. Appl Biochem Biotechnol 160:9–18

    CAS  PubMed  Google Scholar 

  • Lee RE (1980) Phycology, 1st edn. Press, Cambridge University

    Google Scholar 

  • Lee Y-K (2001) Microalgal mass culture systems and methods: their limitation and potential. J Appl Phycol 13:307–315

    Google Scholar 

  • Lee YK, Ding SY, Hoe CH, Low CS (1996) Mixotrophic growth of Chlorella sorokiniana in outdoor enclosed photobioreactor. J Appl Phycol 8:163–169

    Google Scholar 

  • Leyva LA, Bashan Y, Mendoza A, de Bashan LE (2014) Accumulation fatty acids of in Chlorella vulgaris under heterotrophic conditions in relation to activity of acetyl-CoA carboxylase, temperature, and co-immobilization with Azospirillum brasilense. Naturwissenschaften 101:819–830

    CAS  PubMed  Google Scholar 

  • Li X, Xu H, Wu Q (2007) Large‐scale biodiesel production from microalga Chlorella protothecoides through heterotrophic cultivation in bioreactors. Biotechnol Bioeng 98:764–771

    CAS  PubMed  Google Scholar 

  • Li Y, Horsman M, Wu N, Lan CQ, Dubois-Calero N (2008) Biofuels from microalgae. Biotechnol Prog 24:815–820

    CAS  PubMed  Google Scholar 

  • Li P, Miao X, Li R, Zhong J (2011) In situ biodiesel production from fast-growing and high oil content Chlorella pyrenoidosa in rice straw hydrolysate. J Biomed Biotechnol 2011:1–8

    Google Scholar 

  • Li Y, Zhou W, Hu B, Min M, Chen P, Ruan RR (2012) Effect of light intensity on algal biomass accumulation and biodiesel production for mixotrophic strains Chlorella kessleri and Chlorella protothecoide cultivated in highly concentrated municipal wastewater. Biotechnol Bioeng 109:2222–2229

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Lin Y-F, Jing S-R, Lee D-Y, Wang T-W (2002) Nutrient removal from aquaculture wastewater using a constructed wetlands system. Aquaculture 209:169–184

    CAS  Google Scholar 

  • Lowrey J, Yildiz I (2011) Seawater/wastewater production of microalgae-based biofuels in closed loop tubular photobioreactors. Master Thesis California Polytechnic State University, San Luis Obispo, USA, 141 pp

    Google Scholar 

  • Lowrey J, Yildiz I (2014) Investigation of heterotrophic cultivation potential of Chlorella vulgaris and Tetraselmis chuii in controlled environment wastewater growth media from dairy, poultry and aquaculture industries. Acta Horticult 1037:1109–1114

    Google Scholar 

  • Marquez FJ (1995) Enhancement of biomass and pigment production during growth of Spirulina platensis in mixotrophic culture. J Chem Technol Biot 62:159–164

    CAS  Google Scholar 

  • Mata TM, Martins AA, Caetano NS (2010) Microalgae for biodiesel production and other applications: a review. Renew Sust Energ Rev 14:217–232

    CAS  Google Scholar 

  • McGinn PJ, Dickinson KE, Bhatti S, Frigon JC, Guiot SR, O’Leary SJ (2011) Integration of microalgae cultivation with industrial waste remediation for biofuel and bioenergy production: opportunities and limitations. Photosynth Res 109:231–247

    CAS  PubMed  Google Scholar 

  • McGinn PJ, Dickinson KE, Park KC, Whitney CG, MacQuarrie SP, Black FJ, Frigon J-C, Guiot SR, O’Leary SJB (2012) Assessment of the bioenergy and bioremediation potentials of the microalga Scenedesmus sp. AMDD cultivated in municipal wastewater effluent in batch and continuous mode. Algal Res 1:155–165

    Google Scholar 

  • Mendes A, Reis A, Vasconcelos R, Guerra P, Lopes da Silva T (2009) Crypthecodinium cohnii with emphasis on DHA production: a review. J Appl Phycol 21:199–214

    Google Scholar 

  • Miao X, Wu Q (2006) Biodiesel production from heterotrophic microalgal oil. Bioresour Technol 97:841–846

    CAS  PubMed  Google Scholar 

  • Morris I (1974) Nitrogen assimilation and protein synthesis. In: Stewart WDP (ed) Algal Physiology and Biochemistry. Blackwell Scientific Publs, Oxford, pp 583–609

    Google Scholar 

  • Mulbry W, Kondrad S, Buyer J, Luthria DL (2009) Optimization of an oil extraction process for algae from the treatment of manure effluent. J Am Oil Chem Soc 86:909–915

    CAS  Google Scholar 

  • Obaja D, Macé S, Costa J, Sans C, Mata-Alvarez J (2003) Nitrification, denitrification and biological phosphorus removal in piggery wastewater using a sequencing batch reactor. Bioresour Technol 87:103–111

    CAS  PubMed  Google Scholar 

  • Ogawa T, Aiba S (1981) Bioenergetic analysis of mixotrophic growth in Chlorella vulgaris and Scenedesmus acutus. Biotechnol Bioeng 23:1121–1132

    CAS  Google Scholar 

  • Ogbonna JC, Tanaka H (1998) Cyclic autotrophic/heterotrophic cultivation of photosynthetic cells: a method of achieving continuous cell growth under light/dark cycles. Bioresour Technol 65:65–72

    CAS  Google Scholar 

  • Ogbonna JC, Tanaka H (2000) Light requirement and photosynthetic cell cultivation—development of processes for efficient light utilization in photobioreactors. J Appl Phycol 12:207–218

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • Okubo Y, Futamata H, Hiraishi A (2006) Characterization of phototrophic purple nonsulfur bacteria forming colored microbial mats in a swine wastewater ditch. Appl Environ Microbiol 72:6225–6233

    CAS  PubMed Central  PubMed  Google Scholar 

  • Olguín EJ (2003) Phycoremediation: key issues for cost-effective nutrient removal processes. Biotechnol Adv 22:81–91

    PubMed  Google Scholar 

  • Passell H, Dhaliwal H, Reno M, Wu B, Ben Amotz A, Ivry E, Gay M, Czartoski T, Laurin L, Ayer N (2013) Algae biodiesel life cycle assessment using current commercial data. J Environ Manag 129:103–111

    CAS  Google Scholar 

  • Pate R, Klise G, Wu B (2011) Resource demand implications for US algae biofuels production scale-up. Appl Energ 88:3377–3388

    CAS  Google Scholar 

  • Paul JW, Beauchamp EG (1989) Effect of carbon constituents in manure on denitrification in soil. Can J Soil Sci 69:49–61

    Google Scholar 

  • Perez-Garcia O, De-Bashan LE, Hernandez J-P, Bashan Y (2010) Efficiency of growth and nutrient uptake from wastewater by heterotrophic, autotrophic, and mixotrophic cultivation of Chlorella vulgaris immobilized with Azospirillum brasilense. J Phycol 46:800–812

    CAS  Google Scholar 

  • Perez-Garcia O, Bashan Y, Esther Puente M (2011a) Organic carbon supplementation of sterilized municipal wastewater is essential for heterotrophic growth and removing ammonium by the microalga Chlorella vulgaris. J Phycol 47:190–199

    Google Scholar 

  • Perez-Garcia O, Escalante FME, de Bashan LE, Bashan Y (2011b) Heterotrophic cultures of microalgae: metabolism and potential products. Water Res 45:11–36

    CAS  PubMed  Google Scholar 

  • Prathima Devi M, Venkata Subhash G, Venkata Mohan S (2012) Heterotrophic cultivation of mixed microalgae for lipid accumulation and wastewater treatment during sequential growth and starvation phases: effect of nutrient supplementation. Renew Energ 43:276–283

    CAS  Google Scholar 

  • Queiroz MI, Hornes MO, da Silva G, Manetti A, Zepka LQ, Jacob-Lopes E (2013) Fish processing wastewater as a platform of the microalgal biorefineries. Biosyst Eng 115:195–202

    Google Scholar 

  • Ratledge C, Kanagachandran K, Anderson AJ, Grantham D, Stephenson J (2001) Production of docosahexaenoic acid by Crypthecodinium cohnii grown in a pH-auxostat culture with acetic acid as principal carbon source. Lipids 36:1241–1246

    CAS  PubMed  Google Scholar 

  • Rawat I, Ranjith Kumar R, Mutanda T, Bux F (2011) Dual role of microalgae: phycoremediation of domestic wastewater and biomass production for sustainable biofuels production. Appl Energ 88:3411–3424

    CAS  Google Scholar 

  • Redfield AC (1934) On the proportions of organic derivatives in sea water and their relation to the composition of plankton. In: Daniel RJ (ed) James Johnstone Memorial Volume. Liverpool University Press, Liverpool, pp 176–192

    Google Scholar 

  • Roessler PG (1988) Changes in the activities of various lipid and carbohydrate biosynthetic enzymes in the diatom Cyclotella cryptica in response to silicon deficiency. Arch Biochem Biophys 267:521–528

    CAS  PubMed  Google Scholar 

  • Salminen EA, Rintala JA (2002) Semi-continuous anaerobic digestion of solid poultry slaughterhouse waste: effect of hydraulic retention time and loading. Water Res 36:3175–3182

    CAS  PubMed  Google Scholar 

  • Sánchez S, Martínez ME, Espejo MT, Pacheco R, Espinola F, Hodaifa G (2001) Mixotrophic culture of Chlorella pyrenoidosa with olive-mill wastewater as the nutrient medium. J Appl Phycol 13:443–449

    Google Scholar 

  • Severin BF (1980) Disinfection of municipal wastewater effluents with ultraviolet light. J Water Pollut Contr Fedn 52:2007–2018

    CAS  Google Scholar 

  • Sijtsma L, Anderson AJ, Ratledge C (2005) Alternative carbon sources for heterotrophic production of docosahexaenoic acid by the marine alga Crypthecodinium cohnii. In: Ratledge C, Cohen Z (eds) Single Cell Oils. AOCS Press, Champaign, pp 107–123

    Google Scholar 

  • Singh A, Nigam PS, Murphy JD (2011) Mechanism and challenges in commercialisation of algal biofuels. Bioresour Technol 102:26–34

    CAS  PubMed  Google Scholar 

  • Sloth JK, Wiebe MG, Eriksen NT (2006) Accumulation of phycocyanin in heterotrophic and mixotrophic cultures of the acidophilic red alga Galdieria sulphuraria. Enzyme Microb Tech 38:168–175

    CAS  Google Scholar 

  • Sooknah RD, Wilkie AC (2004) Nutrient removal by floating aquatic macrophytes cultured in anaerobically digested flushed dairy manure wastewater. Ecol Eng 22:27–42

    Google Scholar 

  • Sun A, Davis R, Starbuck M, Ben-Amotz A, Pate R, Pienkos P (2011) Comparative cost analysis of algal oil production for biofuels. Energy 36:5169–5179

    Google Scholar 

  • Syrett PJ, Morris I (1963) The inhibition of nitrate assimilation by ammonium in Chlorella. Biochim Biophys Acta 67:566–575

    CAS  Google Scholar 

  • Tabernero A, Martín del Valle EM, Galán MA (2012) Evaluating the industrial potential of biodiesel from a microalgae heterotrophic culture: scale-up and economics. Biochem Eng J 63:104–115

    CAS  Google Scholar 

  • Tam NF, Wong Y (2000) Effect of immobilized microalgal bead concentrations on wastewater nutrient removal. Environ Pollut 107:145–151

    CAS  PubMed  Google Scholar 

  • Tanoi T, Kawachi M, Watanabe MM (2010) Effects of carbon source on growth and morphology of Botryococcus braunii. J Appl Phycol 23:25–33

    Google Scholar 

  • Tett P, Droop MR, Heaney SI (1985) The Redfield Ratio and phytoplankton growth rate. J Mar Biol Assoc UK 65:487–504

    Google Scholar 

  • Tripathi U, Sarada R, Ravishankar GA (2002) Effect of culture conditions on growth of green alga—Haematococcus pluvialis and astaxanthin production. Acta Physiol Plant 24:323–329

    CAS  Google Scholar 

  • 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 Biotechnol 91:835–844

    CAS  PubMed  Google Scholar 

  • Wang L, Min M, Li Y, Chen Y, Liu Y, Wang Y, Ruan R (2009) Cultivation of green algae Chlorella sp. in different wastewaters from municipal wastewater treatment plant. Appl Biochem Biotechnol 162:1174–1186

    PubMed  Google Scholar 

  • Wang L, Li Y, Chen P, Min M, Chen Y, Zhu J, Ruan RR (2010) Anaerobic digested dairy manure as a nutrient supplement for cultivation of oil-rich green microalgae Chlorella sp. Bioresour Technol 101:2623–2628

  • Wang H, Xiong H, Hui Z, Zeng X (2012) Mixotrophic cultivation of Chlorella pyrenoidosa with diluted primary piggery wastewater to produce lipids. Bioresour Technol 104:215–220

    CAS  PubMed  Google Scholar 

  • Wang J, Yang H, Wang F (2014) Mixotrophic cultivation of microalgae for biodiesel production: status and prospects. Appl Biochem Biotechnol 172:3307–3329

    CAS  PubMed  Google Scholar 

  • Wei A, Zhang X, Wei D, Chen G, Wu Q, Yang ST (2009) Effects of cassava starch hydrolysate on cell growth and lipid accumulation of the heterotrophic microalgae Chlorella protothecoides. J Ind Microbiol Biotechnol 36:1383–1389

    CAS  PubMed  Google Scholar 

  • Weyer KM, Bush DR, Darzins A, Willson BD (2010) Theoretical maximum algal oil production. Bioenerg Res 3:204–213

    Google Scholar 

  • Wigmosta MS, Coleman AM, Skaggs RJ, Huesemann MH, Lane LJ (2011) National microalgae biofuel production potential and resource demand. Water Resour Res 47: W00H04.

  • Wilkie AC, Mulbry WW (2002) Recovery of dairy manure nutrients by benthic freshwater algae. Bioresour Technol 84:81–91

    CAS  PubMed  Google Scholar 

  • Williams PJB L, Laurens LML (2010) Microalgae as biodiesel & biomass feedstocks: Review & analysis of the biochemistry, energetics & economics. Energ Environ Sci 3:554–590

    Google Scholar 

  • Xu H, Miao X, Wu Q (2006) High quality biodiesel production from a microalga Chlorella protothecoides by heterotrophic growth in fermenters. J Biotechnol 126:499–507

    CAS  PubMed  Google Scholar 

  • Yamane Y, Utsunomiya T, Watanabe M, Sasaki K (2001) Biomass production in mixotrophic culture of Euglena gracilis under acidic condition and its growth energetics. Biotechnol Lett 23:1223–1228

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Yang C, Ding Z, Zhang K (2008) Growth of Chlorella pyrenoidosa in wastewater from cassava ethanol fermentation. World J Microbiol Biotechnol 24:2919–2925

    CAS  Google Scholar 

  • Yetilmezsoy K, Sakar S (2008) Improvement of COD and color removal from UASB treated poultry manure wastewater using Fenton’s oxidation. J Hazard Mater 151:547–558

    CAS  PubMed  Google Scholar 

  • Yetilmezsoy K, Sapci-Zengin Z (2009) Recovery of ammonium nitrogen from the effluent of UASB treating poultry manure wastewater by MAP precipitation as a slow release fertilizer. J Hazard Mater 166:260–269

    CAS  PubMed  Google Scholar 

  • Zhang H, Wang W, Li Y, Yang W, Shen G (2011) Mixotrophic cultivation of Botryococcus braunii. Biomass Bioenergy 35:1710–1715

    CAS  Google Scholar 

  • Zhou W, Min M, Li Y, Hu B, Ma X, Cheng Y, Liu Y, Chen P, Ruan R (2012) A hetero-photoautotrophic two-stage cultivation process to improve wastewater nutrient removal and enhance algal lipid accumulation. Bioresour Technol 110:448–455

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Joshua Lowrey.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lowrey, J., Brooks, M.S. & McGinn, P.J. Heterotrophic and mixotrophic cultivation of microalgae for biodiesel production in agricultural wastewaters and associated challenges—a critical review. J Appl Phycol 27, 1485–1498 (2015). https://doi.org/10.1007/s10811-014-0459-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-014-0459-3

Keywords

Navigation