Abstract
The feasibility of alginate-immobilised Chlorella sorokiniana for nitrate and ammonium removal from drinking water in regard to carbon source effects was studied in this paper. Three different natural carbon sources were tested in batch experiments with nitrate as nitrogen source: sucrose, grape juice and acacia honey. The nitrate removal efficiencies achieved at 50 mg/L of initial nitrate concentration under sucrose, grape juice and acacia honey were 93, 99 and 94 %, respectively. At 100 mg/L of nitrate, comparable efficiencies were obtained after approximately 3 days, whilst for acacia honey at 50 mg/L, it took only 2 days of cultivation and 3 days for the other two carbon sources. Grape juice and acacia honey showed better performances than sucrose, which must be linked to their chemical compositions. The study of the impact of biosorbent quantity on nitrate removal efficiency showed that sufficient nitrate removal efficiencies could be achieved with a beads/water ratio of 1:6.7 (v/v) or smaller. In addition, the beads’ ages significantly impacted the nitrate removal. The removal of ammonium was studied in the presence of nitrate with acacia honey as carbon source. At the highest concentrations being tested (ammonium-30 mg/L and nitrate-50 mg/L), ammonium was completely removed in <3 days and nitrate by 81 % in 4 days, whereby the suitable beads/water ratio was 1:5. The priority of ammonium assimilation was noticed when compared to nitrate. According to the results, the alginate-immobilised C. sorokiniana represents a promising tool for the removal of nitrogen from drinking water sources.
Similar content being viewed by others
References
Abdel Hameed MS (2007) Effect of algal density in bead, bead size and bead concentrations on wastewater nutrient removal. Afr J Biotechnol 6(10):1185–1191
Abdel-Raouf N, Al-Homaidan AA, Ibraheem IBM (2012) Microalgae and wastewater treatment. Saudi J Biol Sci 19:257–275. doi:10.1016/j.sjbs.2012.04.005
Awasthi M (2005) Nitrate reductase activity: a solution to nitrate problems tested in free and Immobilized algal cells in presence of heavy metals. Int J Environ Sci Technol 2:201–206. doi:10.1007/bf03325876
Bischoff H, Bold HC (2003) Psychological studies IV. In: Some soil algae from enchanted rock and related algal species, vol 6318. University Texas Publications
Bizaj E (2006) The influence of grape juice composition on the alcoholic fermentation course. Biotechnical Faculty, Department of Food Science and Technology, University of Ljubljana, Ljubljana
Božnar A (2003) Microbiology of honey. V: microbiology of foodstuffs. University of Ljubljana, Biotechnical Faculty, Department of Food Science and Technology, Ljubljana
Christenson L, Sims R (2011) Production and harvesting of microalgae for wastewater treatment, biofuels, and bioproducts. Biotechnol Adv 29:686–702. doi:10.1016/j.biotechadv.2011.05.015
Cruz I, Bashan Y, Hernàndez-Carmona G, de-Bashan LE (2013) Biological deterioration of alginate beads containing immobilized microalgae and bacteria during tertiary wastewater treatment. Appl Microbiol Biotechnol 97:9847–9858. doi:10.1007/s00253-013-4703-6
de-Bashan LE, Bashan Y (2010) Immobilized microalgae for removing pollutants: review of practical aspects. Bioresour Technol 101:1611–1627. doi:10.1016/j.biortech.2009.09.043
de-Bashan LE, Hernandez J-P, Morey T, Bashan Y (2004) Microalgae growth-promoting bacteria as “helpers” for microalgae: a novel approach for removing ammonium and phosphorus from municipal wastewater. Water Res 38:466–474. doi:10.1016/j.watres.2003.09.022
de-Bashan LE, Trejo A, Huss VAR, Hernandez J-P, Bashan Y (2008) Chlorella sorokiniana UTEX 2805, a heat and intense, sunlight-tolerant microalga with potential for removing ammonium from wastewater. Bioresour Technol 99:4980–4989. doi:10.1016/j.biortech.2007.09.065
DIN 38 406-E5-1 (1983) Photometric determination of ammonium nitrogen by sodium dichloroisocyanurate and sodium salicylate. DIN—German Institute for Standardization, Berlin, Germany
Gao C, Zhai Y, Ding Y, Wu Q (2010) Application of sweet sorghum for biodiesel production by heterotrophic microalga Chlorella protothecoides. Appl Energy 87:756–761. doi:10.1016/j.apenergy.2009.09.006
Hernandez J-P, de-Bashan LE, Bashan Y (2006) Starvation enhances phosphorus removal from wastewater by the microalga Chlorella spp. co-immobilized with Azospirillum brasilense. Enzym Microb Technol 38:190–198. doi:10.1016/j.enzmictec.2005.06.005
Huang L, Xiang Y, Cai J, Jiang L, Lv Z, Zhang Y, Xu Z (2011) Effects of three main sugars in cane molasses on the production of butyric acid with Clostridium tyrobutyricum. Korean J Chem Eng 28:2312–2315
ISO 6777:1984 (1984) Water quality—determination of nitrite—molecular absorption spectrometric method. International Organization of Standardization, Geneva
ISO 7890–1:1986 (1986) Water quality—determination of nitrate—part 1: 2,6-Dimethylphenol spectrometric method. International Organization of Standardization, Geneva
ISO 8467:1993 (1993) Water quality—determination of permanganate index. International Organization of Standardization, Geneva
Kaonga CC, Chiotha SS, Monjerezi M, Fabiano E, Henry EM (2008) Levels of cadmium, manganese and lead in water and algae; Spirogyra aequinoctialis. Int J Environ Sci Technol 5:471–478. doi:10.1007/bf03326043
Khan M, Yoshida N (2008) Effect of l-glutamic acid on the growth and ammonium removal from ammonium solution and natural wastewater by Chlorella vulgaris NTM06. Bioresour Technol 99:575–582. doi:10.1016/j.biortech.2006.12.031
Kim S, Lee Y, Hwang S-J (2013a) Removal of nitrogen and phosphorus by Chlorella sorokiniana cultured heterotrophically in ammonia and nitrate. Int Biodeterior Biodegrad 85:511–516. doi:10.1016/j.ibiod.2013.05.025
Kim S, Park J-E, Cho Y-B, Hwang S-J (2013b) Growth rate, organic carbon and nutrient removal rates of Chlorella sorokiniana in autotrophic, heterotrophic and mixotrophic conditions. Bioresour Technol 144:8–13. doi:10.1016/j.biortech.2013.06.068
Kumar K, Das D (2012) Growth characteristics of Chlorella sorokiniana in airlift and bubble column photobioreactors. Bioresour Technol 116:307–313. doi:10.1016/j.biortech.2012.03.074
Leesing R, Kookkhunthod S (2011) Heterotrophic growth of Chlorella sp. KKU-S2 for lipid production using molasses as a carbon substrate. In: International conference on food engineering and biotechnology, IPCBEE vol 9, pp 87–91
Li Y et al (2011) Characterization of a microalga Chlorella sp. well adapted to highly concentrated municipal wastewater for nutrient removal and biodiesel production. Bioresour Technol 102:5138–5144. doi:10.1016/j.biortech.2011.01.091
Liu K, Li J, Qiao H, Lin A, Wang G (2012) Immobilization of Chlorella sorokiniana GXNN 01 in alginate for removal of N and P from synthetic wastewater. Bioresour Technol 114:26–32. doi:10.1016/j.biortech.2012.02.003
Lizzul AM, Hellier P, Purton S, Baganz F, Ladommatos N, Campos L (2014) Combined remediation and lipid production using Chlorella sorokiniana grown on wastewater and exhaust gases. Bioresour Technol 151:12–18. doi:10.1016/j.biortech.2013.10.040
Mallick N (2002) Biotechnological potential of immobilized algae for wastewater N, P and metal removal: a review. BioMetals 15(4):377–390
Mane PC, Bhosle AB (2011) Bioremoval of some metals by living algae Spirogyra sp. and Spirullina sp. from aqueous solution. Int J Environ Res 6(2):571–576
Mehta SK, Gaur JP (2001) Removal of Ni and Cu from single and binary metalsolutions by free and immobilized Chlorella vulgaris. Eur J Protistol 37:261–271. doi:10.1078/0932-4739-00813
Moreno-Garrido I (2008) Microalgae immobilization: current techniques and uses. Bioresour Technol 99:3949–3964. doi:10.1016/j.biortech.2007.05.040
Ngangkham M, Kumar Ratha S, Prasanna R, Saxena AK, Dhar DW, Sarika C, Narayana Prasad RB (2012) Biochemical modulation of growth, lipid quality and productivity in mixotrophic cultures of Chlorella sorokiniana. Springer Plus 1:33
Nussinovitch A (ed) (2010) Polymer macro- and micro-gel beads: fundamentals and applications, XXV edn. Springer, Berlin
Olguín EJ, Sánchez-Galván G, González-Portela RE, López-Vela M (2008) Constructed wetland mesocosms for the treatment of diluted sugarcane molasses stillage from ethanol production using Pontederia sagittata. Water Res 42:3659–3666. doi:10.1016/j.watres.2008.05.015
Perez-Garcia O, Bashan Y, Puente ME (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. doi:10.1111/j.1529-8817.2010.00934.x
Perez-Garcia O, Escalante FME, de-Bashan LE, Bashan Y (2011b) Heterotrophic cultures of microalgae: metabolism and potential products. Water Res 45:11–36. doi:10.1016/j.watres.2010.08.037
Prathima Devi M, Swamy YV, Venkata Mohan S (2013) Nutritional mode influences lipid accumulation in microalgae with the function of carbon sequestration and nutrient supplementation. Bioresour Technol 142:278–286. doi:10.1016/j.biortech.2013.05.001
Qiao H, Wang G, Zhang X (2009) Isolation and characterization of Chlorella sorokiniana GXNN01 (Chlorophyta) with the properties of heterotrophic and microaerobic growth. J Phycol 45:1153–1162
Rashid N, Lee K, Han J, Gross M (2013) Hydrogen production by immobilized Chlorella vulgaris: optimizing pH, carbon source and light. Bioprocess Biosyst Eng 36:867–872. doi:10.1007/s00449-012-0819-9
Rasoul-Amini S et al (2014) Removal of nitrogen and phosphorus from wastewater using microalgae free cells in bath culture system. Biocatal Agric Biotechnol 3:126–131. doi:10.1016/j.bcab.2013.09.003
Riaño B, Hernández D, García-González MC (2012) Microalgal-based systems for wastewater treatment: effect of applied organic and nutrient loading rate on biomass composition. Ecol Eng 49:112–117. doi:10.1016/j.ecoleng.2012.08.021
Ruiz-Marin A, Mendoza-Espinosa LG, Stephenson T (2010) Growth and nutrient removal in free and immobilized green algae in batch and semi-continuous cultures treating real wastewater. Bioresour Technol 101:58–64. doi:10.1016/j.biortech.2009.02.076
Shi X-M, Zhang X-W, Chen F (2000) Heterotrophic production of biomass and lutein by Chlorella protothecoides on various nitrogen sources. Enzym Microb Technol 27:312–318. doi:10.1016/S0141-0229(00)00208-8
Singh G, Thomas PB (2012) Nutrient removal from membrane bioreactor permeate using microalgae and in a microalgae membrane photoreactor. Bioresour Technol 117:80–85. doi:10.1016/j.biortech.2012.03.125
Su Y, Mennerich A, Urban B (2012) Comparison of nutrient removal capacity and biomass settleability of four high-potential microalgal species. Bioresour Technol 124:157–162. doi:10.1016/j.biortech.2012.08.037
Sun N, Wang Y, Li Y-T, Huang J-C, Chen F (2008) Sugar-based growth, astaxanthin accumulation and carotenogenic transcription of heterotrophic Chlorella zofingiensis (Chlorophyta). Process Biochem 43:1288–1292. doi:10.1016/j.procbio.2008.07.014
Tam NFY, Wong YS (2000) Effect of immobilized microalgal bead concentrations on wastewater nutrient removal. Environ Pollut 107:145–151. doi:10.1016/S0269-7491(99)00118-9
Tanner W (2000) The Chlorella hexose/H(+)-symporters. Int Rev Cytol 200:101–141
Urrutia I, Serra JL, Llama MJ (1995) Nitrate removal from water by Scenedesmus obliquus immobilized in polymeric foams. Enzym Microb Technol 17:200–205. doi:10.1016/0141-0229(94)00008-F
Vidotti ADS, Coelho RS, Franco LM, Franco TT (2014) Miniaturized culture for heterotrophic microalgae using low cost carbon sources as a tool to isolate fast and economical strains. Chem Eng Trans 38:325–330
Zheng Y, Li T, Yu X, Bates PD, Dong T, Chen S (2013) High-density fed-batch culture of a thermotolerant microalga Chlorella sorokiniana for biofuel production. Appl Energy 108:281–287. doi:10.1016/j.apenergy.2013.02.059
Acknowledgments
The authors would like to acknowledge the Slovenian Research Agency for the financial support (Project No. 1000-11-310131).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Petrovič, A., Simonič, M. The effect of carbon source on nitrate and ammonium removal from drinking water by immobilised Chlorella sorokiniana . Int. J. Environ. Sci. Technol. 12, 3175–3188 (2015). https://doi.org/10.1007/s13762-014-0747-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13762-014-0747-0