Skip to main content
Log in

The Effects of Plant Growth Substances and Mixed Cultures on Growth and Metabolite Production of Green Algae Chlorella sp.: A Review

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Recent interest in the use of microalgae for the production of biofuels and bioproducts has stimulated an interest in methods to enhance the growth rate of microalgae. This review examines past work involving the stimulation of Chlorella sp. growth and metabolite production by plant growth substances as well as by mixed cultures of Chlorella sp. with bacteria. Plant growth substances known to regulate Chlorella sp. growth and metabolite production include auxins, cytokinins, abscisic acid, polyamines, brassinosteroids, jasmonic acid, salicylic acid, and combinations of two or three of the aforementioned substances. Mixed cultures of bacteria are examined, including both natural bacteria–algae consortia and artificially induced symbioses. For natural consortia, commonly occurring bacterial species, including the genera Brevundimonas and Sphingomonas, are discussed. For artificially induced symbioses, the use of the nitrogen-fixing bacterium Azospirillum is examined in detail. In particular, a variety of studies have involved the coimmobilization of Chlorella sp. with Azospirillum sp. in alginate beads, with the goal of using the mixed culture to treat wastewater. In summary, the use of plant growth substances and mixed cultures provides two methods to increase the growth of Chlorella sp., whether for the production of lipids for biofuels, the production of bioproducts, the treatment of wastewater, or a variety of other reasons.

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

  • Andersen RA (ed) (2005) Algal culturing techniques. Elsevier Academic Press, Burlington

    Google Scholar 

  • Bai R, Silaban AG, Gutierrez-Wing MT, Benton MG, Rusch KA (in review) Effects of nitrogen and irradiance on lipid content and composition of a Louisiana native Chlorella vulgaris/Leptolyngbya sp. co-culture

  • Bajguz A (2000) Effect of brassinosteroids on nucleic acids and protein content in cultured cells of Chlorella vulgaris. Plant Physiol Biochem 38:209–215

    Article  CAS  Google Scholar 

  • Bajguz A (2009a) Brassinosteroid enhanced the level of abscisic acid in Chlorella vulgaris subjected to short-term heat stress. J Plant Physiol 166:882–886

    Article  PubMed  CAS  Google Scholar 

  • Bajguz A (2009b) Isolation and characterization of brassinosteroids from algal cultures of Chlorella vulgaris Beijerinck (Trebouxiophyceae). J Plant Physiol 166:1946–1949

    Article  PubMed  CAS  Google Scholar 

  • Bajguz A, Czerpak R (1996) Effect of brassinosteroids on growth and proton extrusion in the alga Chlorella vulgaris Beijerinck (Chlorophyceae). J Plant Growth Regul 15:153–156

    Article  CAS  Google Scholar 

  • Bashan Y, Holguin G, de-Bashan LE (2004) Azospirillum–plant relationships: physiological, molecular, agricultural, and environmental advances (1997–2003). Can J Microbiol 50:521–577

    Article  PubMed  CAS  Google Scholar 

  • Bhola V, Desikan R, Santosh SK, Subburamu K, Sanniyasi E, Bux F (2011) Effects of parameters affecting biomass yield and thermal behaviour of Chlorella vulgaris. J Biosci Bioeng 111:377–382

    Article  PubMed  CAS  Google Scholar 

  • Blanc G, Duncan G, Agarkova I, Borodovsky M, Gurnon J, Kuo A, Lindquist E, Lucas S, Pangilinan J, Polle J, Salamov A, Terry A, Yamada T, Dunigan DD, Grigoriev IV, Claverie J-M, Van Etten JL (2010) The Chlorella variabilis NC64A genome reveals adaptation to photosymbiosis, coevolution with viruses, and cryptic sex. Plant Cell 22:2943–2955

    Article  PubMed  CAS  Google Scholar 

  • Bradley PM (1991) Plant hormones do have a role in controlling growth and development of algae. J Phycol 27:317–321

    Article  CAS  Google Scholar 

  • Burkiewicz K (1987) The influence of gibberellins and cytokinins on the growth of some unicellular Baltic algae. Bot Mar 30:63–69

    Article  CAS  Google Scholar 

  • Cheirsilp B, Suwannarat W, Niyomdecha R (2011) Mixed culture of oleaginous yeast Rhodotorula glutinis and microalga Chlorella vulgaris for lipid production from industrial wastes and its use as biodiesel feedstock. New Biotechnol 28:362–368

    Article  CAS  Google Scholar 

  • 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 Nannochloropsis oculata and Chlorella vulgaris for biodiesel production. Chem Eng Prog 48:1146–1151

    Article  CAS  Google Scholar 

  • Croft MT, Lawrence AD, Raux-Deery E, Warren MJ, Smith AG (2005) Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature 438:90–93

    Article  PubMed  CAS  Google Scholar 

  • Czerpak R, Bajguz A, Bialecka B, Wierzcholowska LE, Wolanska MM (1994) Effect of auxin precursors and chemical analogues on the growth and chemical composition in Chlorella pyrenoidosa Chick. Acta Soc Bot Pol 63:279–286

    Article  CAS  Google Scholar 

  • Czerpak R, Krotke A, Mikal A (1999) Comparison of stimulatory effect of auxins and cytokinins on protein, saccharides, and chlorophylls content in Chlorella pyrenoidosa Chick. Pol Arch Hydrobiol 46:71–82

    CAS  Google Scholar 

  • Czerpak R, Bajguz A, Gromek M, Koztowska G, Nowak I (2002) Activity of salicylic acid on the growth and biochemism of Chlorella vulgaris Beijerinck. Acta Physiol Plant 24:45–52

    Article  CAS  Google Scholar 

  • Czerpak R, Bajguz A, Pietrowska A, Dobrogowska R, Matejczyk M, Weislawski W (2003) Biochemical activity of di- and polyamines in the green alga Chlorella vulgaris Beijerinck (Chlorophyceae). Acta Soc Bot Pol 72:19–24

    Article  CAS  Google Scholar 

  • Czerpak R, Pietrowska A, Szulecka K (2006) Jasmonic acid affects changes in the growth and some components content in alga Chlorella vulgaris. Acta Physiol Plant 28:195–203

    Article  CAS  Google Scholar 

  • de-Bashan LE, Bashan Y, Moreno M, Lebsky VK, Bustillos JJ (2002) Increased pigment and lipid content, lipid variety, and cell and population size of the microalgae Chlorella spp. when co-immobilized in alginate beads with the microalgae-growth-promoting bacterium Azospirillum brasilense. Can J Microbiol 48:514–521

    Article  PubMed  CAS  Google Scholar 

  • de-Bashan LE, Antoun H, Bashan Y (2008) Involvement of indole-3-acetic acid produced by the growth-promoting bacterium Azospirillum spp. in promoting growth of Chlorella vulgaris. J Phycol 44:938–947

    Article  CAS  Google Scholar 

  • de-Bashan LE, Schmid M, Rothballer M, Hartmann A, Bashan Y (2011) Cell–cell interaction in the eukaryote–prokaryote model of the microalgae Chlorella vulgaris and the bacterium Azospirillum brasilense immobilized in polymer beads. J Phycol 47:1350–1359

    Article  Google Scholar 

  • Evans LV, Trewavas AJ (1991) Is algal development controlled by plant growth substances? J Phycol 27:322–326

    Article  CAS  Google Scholar 

  • Gallagher BJ (2011) The economics of producing biodiesel from algae. Renew Energy 36:158–162

    Article  CAS  Google Scholar 

  • George EF, Hall MA, de Klerk GJ (eds) (2008a) Plant growth regulators I: introduction; auxins, their analogues and inhibitors. Plant propagation by tissue culture. Springer, Berlin

    Google Scholar 

  • George EF, Hall MA, de Klerk GJ (eds) (2008b) Plant growth regulators II: cytokinins, their analogues and antagonists. Plant cell propagation by tissue culture. Springer, Berlin

    Google Scholar 

  • George EF, Hall MA, de Klerk GJ (eds) (2008c) Plant growth regulators III: gibberellins, ethylene, abscisic acid, their analogues and inhibitors; miscellaneous compounds. Plant cell propagation by tissue culture. Springer, Berlin

    Google Scholar 

  • Gonzalez LE, Bashan Y (2000) Increased growth of the microalga Chlorella vulgaris when coimmobilized and cocultured in alginate beads with the plant-growth-promoting bacterium Azospirillum brasilense. Appl Environ Microbiol 66:1527–1531

    Article  PubMed  CAS  Google Scholar 

  • Gonzalez-Bashan LE, Lebsky VK, Hernandez JP, Bustillos JJ, Bashan Y (2000) Changes in the metabolism of the microalgae Chlorella vulgaris when coimmobilized in alginate with the nitrogen-fixing Phyllobacterium myrsinacearum. Can J Microbiol 46:653–659

    PubMed  CAS  Google Scholar 

  • Greenwell HC, Laurens LML, Shields RJ, Lovitt RW, Flynn KJ (2009) Placing microalgae on the biofuels priority list: a review of the technological challenges. J R Soc Interface 7:703–726

    Article  PubMed  Google Scholar 

  • Harwood JL, Guschina IA (2009) The versatility of algae and their lipid metabolism. Biochimie 91:679–684

    Article  PubMed  CAS  Google Scholar 

  • Hernandez J, de-Bashan L, Rodriguez D, Rodriguez Y, Bashan Y (2009) Growth promotion of the freshwater microalga Chlorella vulgaris by the nitrogen-fixing, plant growth-promoting bacterium Bacillus pumilus from arid zone soils. Eur J Soil Biol 45:88–93

    Article  CAS  Google Scholar 

  • Hsieh CH, Wu WT (2009) Cultivation of microalgae for oil production with a cultivation strategy of urea limitation. Bioresour Technol 100:3921–3926

    Article  PubMed  CAS  Google Scholar 

  • Huang G, Chen F, Wei D, Zhang X, Chen G (2010) Biodiesel production by microalgal biotechnology. Appl Energy 87:38–46

    Article  CAS  Google Scholar 

  • Hunt RW, Chinnasamy S, Bhatnagar A, Das KC (2010) Effect of biochemical stimulants on biomass productivity and metabolite content of the microalga, Chlorella sorokiniana. Appl Biochem Biotechnol 162:2400–2414

    Article  PubMed  CAS  Google Scholar 

  • Hunt RW, Chinnasamy S, Das KC (2011) The effect of naphthalene-acetic acid on biomass productivity and chlorophyll content of green algae, coccolithophore, diatom, and cyanobacterium cultures. Appl Biochem Biotechnol 164:1350–1365

    Article  PubMed  CAS  Google Scholar 

  • Illman AM, Scragg AH, Shales SW (2000) Increase in Chlorella strains calorific values when grown in low nitrogen medium. Enzyme Microb Technol 27:631–635

    Article  PubMed  CAS  Google Scholar 

  • Imase M, Watanabe K, Ioyagi H, Tanaka H (2008) Construction of an artificial symbiotic community using a Chlorella–symbiont association as a model. FEMS Microbiol Ecol 63:273–282

    Article  PubMed  CAS  Google Scholar 

  • Kang CD, Sim SJ (2007) Direct extraction of astaxanthin from Haematococcus culture using vegetable oils. Biotechnol Lett 30:441–444

    Article  PubMed  Google Scholar 

  • Khozin-Goldberg I, Cohen Z (2011) Unraveling algal lipid metabolism: recent advances in gene identification. Biochimie 93:91–100

    Article  PubMed  CAS  Google Scholar 

  • Lakaniemi AM, Intihar VM, Tuovinen OH, Puhakka JA (2011) Growth of Chlorella vulgaris and associated bacteria in photobioreactors. Microb Biotechnol 5:69–78

    Article  PubMed  Google Scholar 

  • Lebsky VK, Gonzalez-Bashan LE, Bashan Y (2001) Ultrastructure of interaction in alginate beads between the microalga Chlorella vulgaris with its natural associative bacterium Phyllobacterium myrsinacearum and with the plant growth-promoting bacterium Azospirillum brasilense. Can J Microbiol 47:1–8

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Litchfield CD, Colwell RR, Prescott JM (1969) Numerical taxonomy of heterotrophic bacteria growing in association with continuous-culture Chlorella sorokiniana. Appl Microbiol 18:1044–1049

    PubMed  CAS  Google Scholar 

  • Liu ZY, Wang GC, Zhou BC (2008) Effect of iron on growth and lipid accumulation in Chlorella vulgaris. Bioresour Technol 99:4717–4722

    Article  PubMed  CAS  Google Scholar 

  • Machida T, Murase H, Kato E, Honjoh K-i, Matsumoto K, Miyamoto T, Iio M (2008) Isolation of cDNAs for hardening-induced genes from Chlorella vulgaris by suppression subtractive hybridization. Plant Sci 195:238–246

    Article  Google Scholar 

  • Mauseth JD (1998) Botany: an introduction to plant biology. Jones and Bartlett, Sudbury

    Google Scholar 

  • Merchant SS, Kropat J, Liu B, Shaw J, Warakanont J (2011) TAG, You’re it! Chlamydomonas as a reference organism for understanding algal triacylglycerol accumulation. Curr Opin Biotechnol 23:352–363

    Article  PubMed  Google Scholar 

  • Multu YB, Isik O, Uslu L, Koc K, Durmaz Y (2011) The effects of nitrogen and phosphorus deficiencies and nitrite addition on the lipid content of Chlorella vulgaris (Chlorophyceae). Afr J Biotechnol 10:453–456

    Google Scholar 

  • Park Y, Je KW, Lee K, Jung SE, Choi TJ (2008) Growth promotion of Chlorella ellipsoidea by co-inoculation with Brevundimonas sp. isolated from the microalga. Hydrobiologia 598:219–228

    Article  CAS  Google Scholar 

  • Perez-Garcia O, De-Bashan LE, Hernandez JP, 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

    Article  CAS  Google Scholar 

  • Piotrowska A, Czerpak R (2009) Cellular response of light/dark-grown green alga Chlorella vulgaris Beijerinck (Chlorophyceae) to exogenous adenine- and phenylurea-type cytokinins. Acta Physiol Plant 31:573–585

    Article  CAS  Google Scholar 

  • Piotrowska A, Czerpak R, Pietryczuk A, Olesiewicz A, Wedołowska M (2008) The effect of indomethacin on the growth and metabolism of green alga Chlorella vulgaris Beijerinck. Plant Growth Regul 55:125–136

    Article  CAS  Google Scholar 

  • Pratt R (1938) Influence of auxins on the growth of Chlorella vulgaris. Am J Bot 25:498–501

    Article  CAS  Google Scholar 

  • Rismani-Yazdi H, Haznedaroglu BZ, Peccia J (2011) Transcriptome sequencing and annotation of the microalgae Dunaliella tertiolecta: pathway description and gene discovery for production of next-generation biofuels. BMC Genomics 12:148

    Article  PubMed  CAS  Google Scholar 

  • Rusch KA, Gutierrez-Wing MT (unpublished data) A protocol for native mixed algae-cyanobacteria selection for biofuels and bioproducts feedstock

  • Singh J, Gu S (2010) Commercialization potential of microalgae for biofuels production. Renew Sustain Energ Rev 14:2596–2610

    Article  CAS  Google Scholar 

  • Subashchandrabose SR, Ramakrishnan B, Megharaj M, Venkateswarlu K, Naidu R (2011) Consortia of cyanobacteria/microalgae and bacteria: biotechnological potential. Biotechnol Adv 29:896–907

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Tam NFY, Wong YS (1990) The comparison of growth and nutrient removal efficiency of Chlorella pyrenoidosa in settled and activated sewages. Environ Pollut 65:93–108

    Article  PubMed  CAS  Google Scholar 

  • Tarakhovskaya ER, Maslov YI, Shishova MF (2007) Phytohormones in algae. Russ J Plant Physiol 52:163–170

    Article  Google Scholar 

  • Tate JJ, Gutierrez-Wing MT, Rusch KA, Benton MG (2012) Gene expression analysis of a Louisiana native Chlorella vulgaris (Chlorophyta)/Leptolyngbya sp. (cyanobacteria) co-culture using suppression subtractive hybridization. Eng Life Sci. doi:10.1002/elsc.201200063

  • Thurmond W (2009) Algae 2020: advanced biofuel markets and commercialization outlook, 1st edn. Emerging Markets online, Houston

  • Tsavkelova EA, Klimova SY, Cherdyntseva TA, Netrusov AI (2006) Microbial producers of plant growth stimulators and their practical use: a review. Appl Biochem Microbiol 42:117–126

    Article  CAS  Google Scholar 

  • Ueda J, Miyamoto K, Aoki M, Hirata T, Sato T, Momotani Y (1991) Identification of jasmonic acid in Chlorella and Spirulina. Bull Univ Osaka Prefect Ser B 43:103–108

    CAS  Google Scholar 

  • Ulrich WR, Kunz G (1984) Effect of abscisic acid on nitrogen uptake, respiration and photosynthesis in green algae. Plant Sci Lett 37:9–14

    Article  Google Scholar 

  • US DOE (Department of Energy) (2010) National Algal Biofuels Technology Roadmap. Available at http://www1.eere.energy.gov/biomass/pdfs/algal_biofuels_roadmap.pdf. Accessed 1 Sept 2011

  • Vance BD (1987) Phytohormone effects on cell division in Chlorella pyrenoidosa Chick (TX-7-11-05) (Chlorellaceae). J Plant Growth Regul 5:169–173

    Article  CAS  Google Scholar 

  • Vu HT, Otsuka S, Ueda H, Senoo K (2010) Cocultivated bacteria can increase or decrease the culture lifetime of Chlorella vulgaris. J Gen Appl Microbiol 56:413–418

    Article  CAS  Google Scholar 

  • Watanabe K, Takihana N, Aoyagi H, Hanada S, Watanabe Y, Ohmura N, Saiki H, Tanaka H (2005) Symbiotic association in Chlorella culture. FEMS Microbiol Ecol 51:187–196

    Article  PubMed  CAS  Google Scholar 

  • Watanabe K, Imase M, Sasaki K, Ohmura N, Saiki H, Tanaka H (2006) Composition of the sheath produced by the green alga Chlorella sorokiniana. Lett Appl Microbiol 42:538–543

    Article  PubMed  CAS  Google Scholar 

  • Watanabe K, Imase M, Aoyagi H, Ohmura N, Saiki H, Tanaka H (2008) Development of a novel artificial medium based on utilization of algal photosynthetic metabolites by symbiotic heterotrophs. J Appl Microbiol 105:741–751

    Article  PubMed  CAS  Google Scholar 

  • Widjaja A, Chien CC, Ju YH (2009) Study of increasing lipid production from fresh water microalgae Chlorella vulgaris. J Taiwan Inst Chem Eng 40:13–20

    Article  CAS  Google Scholar 

  • Yin HC (1937) Effect of auxin on Chlorella vulgaris. Proc Natl Acad Sci USA 23:174–176

    Article  PubMed  CAS  Google Scholar 

  • Zabochnicka-Swiatek M (2010) Algae–feedstock of the future. Arch Combust 30:225–236

    CAS  Google Scholar 

Download references

Acknowledgments

The authors gratefully acknowledge funding for MGB from the National Science Foundation through CBET 1032599.

Conflict of interest

The authors have no conflicts of interest to disclose.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Michael G. Benton.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tate, J.J., Gutierrez-Wing, M.T., Rusch, K.A. et al. The Effects of Plant Growth Substances and Mixed Cultures on Growth and Metabolite Production of Green Algae Chlorella sp.: A Review. J Plant Growth Regul 32, 417–428 (2013). https://doi.org/10.1007/s00344-012-9302-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-012-9302-8

Keywords

Navigation