Abstract
Microalgae are promising sustainable and renewable sources of oils that can be used for biodiesel production. In addition, they contain important compounds, such as proteins and pigments, which have large applications in the food and pharmaceutical industries. Combining the production of these valuable products with wastewater treatment renders the cultivation of microalgae very attractive and economically feasible. This review paper presents and discusses the current applications of microalgae cultivation for wastewater treatment, particularly for the removal of phenolic compounds. The effects of cultivation conditions on the rate of contaminants removal and biomass productivity, as well as the chemical composition of microalgae cells are also discussed.
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Abbreviations
- IARC:
-
International Agency for Research on Cancer
- USEPA:
-
United State Environmental Protection Agency
- ATSDR:
-
Agency of Toxic Substances Registry
- UASB:
-
Up-flow anaerobic sludge blanket
- FBR:
-
Fluidized bed reactor
- PBR:
-
Photobioreactor
- PPF:
-
Photosynthetic photons flux
- ALE:
-
Adaptive laboratory evolution
- MIMA:
-
Mixed indigenous microalgae
References
Aaronson S (1974) The biology and ultrastructure of phagotrophy in Ochromonas danica (Chrysophyceae: Chrysomdnadida). Microbiology 83(1):21–29
Abdelwahab O, Amin NK (2013) Adsorption of phenol from aqueous solutions by Luffa cylindrica fibers: kinetics, isotherm and thermodynamic studies. Egypt J Aquatic Res 39(4):215–223. https://doi.org/10.1016/j.ejar.2013.12.011
Abdelwahab O, Amin NK, El-Ashtoukhy ESZ (2009) Electrochemical removal of phenol from oil refinery wastewater. J Hazard Mater 163(2–3):711–716. https://doi.org/10.1016/j.jhazmat.2008.07.016
Agency for Toxic Substances and Disease Registry (ATSDR) (2008) Toxicological profile for phenol. U.S. Department of Health and Human Services, Public Health Service, Atlanta, GA
Al-Khalid T, El-Naas MH (2012) Aerobic biodegradation of phenols: a comprehensive review. Crit Rev Environ Sci Technol 42(16):1631–1690. https://doi.org/10.1080/10643389.2011.569872
Al-Muhtaseb AH, Khraisheh M (2015) Photocatalytic removal of phenol from refinery wastewater: catalytic activity of Cu-doped titanium dioxide. J Water Process Eng 8:82–90. https://doi.org/10.1016/j.jwpe.2015.09.004
Al-Obaidi MA, Kara-Zaïtri C, Mujtaba IM (2018) Simulation and optimisation of a two-stage/two-pass reverse osmosis system for improved removal of chlorophenol from wastewater. J Water Process Eng 22:131–137. https://doi.org/10.1016/j.jwpe.2018.01.012
Altaş L, Büyükgüngör H (2008) Sulfide removal in petroleum refinery wastewater by chemical precipitation. J Hazard Mater 153(1–2):462–469. https://doi.org/10.1016/j.jhazmat.2007.08.076
Al-Zuhair S, El-Naas M (2011) Immobilization of Pseudomonas putida in PVA gel particles for the biodegradation of phenol at high concentrations. Biochem Eng J 56(1–2):46–50. https://doi.org/10.1016/j.bej.2011.05.005
Al-Zuhair S, Nabil M, Abdi Y, Al Sayyed M, Taher H (2016) High concentration phenol removal using freshwater microalgae. Int J Biotechnol Wellness Indu 5(2):39–45
Amini Khoeyi Z, Seyfabadi J, Ramezanpour Z (2012) Effect of light intensity and photoperiod on biomass and fatty acid composition of the microalgae, Chlorella vulgaris. Aquac Int 20(1):41–49. https://doi.org/10.1007/s10499-011-9440-1
Andrulevičiūtė V, Skorupskaitė V, Kasperovičienė J (2011) Cultivation of microalgae Chlorella sp. and Scenedesmus sp. as a potentional biofuel feedstock. Environ Res Eng Manag 57(3):21–27
Arya D, Kumar S, Kumar S (2011) Biodegradation dynamics and cell maintenance for the treatment of resorcinol and p-cresol by filamentous fungus Gliomastix indicus. J Hazard Mater 198(0):49–56. https://doi.org/10.1016/j.jhazmat.2011.10.009
Baggi G (2000) Ecological implications of synergistic and antagonistic interactions among growth and non growth analogs present in mixture. Ann Microbiol 50(2):103–116
Bailey JE, Ollis DF (1986) Biochemical engineering fundamentals, Seconed edn. McGraw-Hill Book Co., Singapore
Balasubramanian A, Venkatesan S (2012) Removal of phenolic compounds from aqueous solutions by emulsion liquid membrane containing ionic liquid [BMIM]+[PF6]− in tributyl phosphate. Desalination 289(0):27–34. https://doi.org/10.1016/j.desal.2011.12.027
Banerjee A, Ghoshal AK (2011) Phenol degradation performance by isolated Bacillus cereus immobilized in alginate. Int Biodeterior Biodegrad 65(7):1052–1060
Barrios-Martinez A, Barbot E, Marrot B, Moulin P, Roche N (2006) Degradation of synthetic phenol-containing wastewaters by MBR. J Membr Sci 281(1–2):288–296. https://doi.org/10.1016/j.memsci.2006.03.048
Basha K, Rajendran A, Thangavelu V (2010) Recent advances in the biodegradation of phenol: a review. Asian J Exp Biol Sci 1 (219–234)
Batista AP, Moura P, Marques PASS, Ortigueira J, Alves L, Gouveia L (2014) Scenedesmus obliquus as feedstock for biohydrogen production by Enterobacter aerogenes and Clostridium butyricum. Fuel 117(Part A):537–543. https://doi.org/10.1016/j.fuel.2013.09.077
Benyahia F, Abdulkarim M, Embaby A, Rao M (2006) Refinery wastewater treatment: a true technological challenge. In: The Seventh Annual UAE University Research Conference. UAE University
Bhattacharya SS, Karmakar S, Banerjee R (2009) Optimization of laccase mediated biodegradation of 2,4-dichlorophenol using genetic algorithm. Water Res 43(14):3503–3510. https://doi.org/10.1016/j.watres.2009.05.012
Bilad MR, Vandamme D, Foubert I, Muylaert K, Vankelecom IFJ (2012) Harvesting microalgal biomass using submerged microfiltration membranes. Bioresour Technol 111(Supplement C):343–352. https://doi.org/10.1016/j.biortech.2012.02.009
Boussiba S, Vonshak A, Cohen Z, Avissar Y, Richmond A (1987) Lipid and biomass production by the halotolerant microalga Nannochloropsis salina. Biomass 12(1):37–47
Bouterfas R, Belkoura M, Dauta A (2002) Light and temperature effects on the growth rate of three freshwater [2pt] algae isolated from a eutrophic lake. Hydrobiologia 489(1):207–217. https://doi.org/10.1023/a:1023241006464
Brennan L, Owende P (2010) Biofuels from microalgae—a review of technologies for production, processing, and extractions of biofuels and co-products. Renew Sust Energ Rev 14(2):557–577. https://doi.org/10.1016/j.rser.2009.10.009
Brown MR (1991) The amino-acid and sugar composition of 16 species of microalgae used in mariculture. J Exp Mar Biol Ecol 145(1):79–99
Brown MR, Jeffrey SW (1992) Biochemical composition of microalgae from the green algal classes Chlorophyceae and Prasinophyceae. 1. Amino acids, sugars and pigments. J Exp Mar Biol Ecol 161(1):91–113. https://doi.org/10.1016/0022-0981(92)90192-D
Brown MR, Jeffrey SW, Volkman JK, Dunstan GA (1997) Nutritional properties of microalgae for mariculture. Aquaculture 151(1):315–331. https://doi.org/10.1016/S0044-8486(96)01501-3
Canizares-Villanueva R, Dominguez A, Cruz M, Rios-Leal E (1995) Chemical composition of cyanobacteria grown in diluted, aerated swine wastewater. Bioresour Technol 51(2):111–116
Cao J, Li D, Wang J (1996) Studies on biochemical composition of 10 species of common freshwater phytoplankton. Acta Scientiarum Naturalium Universitatis Sunyatseni 36(2):22–27
Cea M, Seaman JC, Jara AA, Mora ML, Diez MC (2005) Describing chlorophenol sorption on variable-charge soil using the triple-layer model. J Colloid Interface Sci 292(1):171–178. https://doi.org/10.1016/j.jcis.2005.05.074
Ceron Garcia M, Camacho FG, Mirón AS, Sevilla JF, Chisti Y, Grima EM (2006) Mixotrophic production of marine microalga Phaeodactylum tricornutum on various carbon sources. J Microbiol Biotechnol 16(5):689
Chakraborty S, Mohanty D, Ghosh S, Das D (2016) Improvement of lipid content of Chlorella minutissima MCC 5 for biodiesel production. J Biosci Bioeng 122(3):294–300. https://doi.org/10.1016/j.jbiosc.2016.01.015
Cheah WY, Ling TC, Show PL, Juan JC, Chang J-S, Lee D-J (2016) Cultivation in wastewaters for energy: a microalgae platform. Appl Energy 179:609–625. https://doi.org/10.1016/j.apenergy.2016.07.015
Chen Y-M, Lin T-F, Huang C, Lin J-C, Hsieh F-M (2007) Degradation of phenol and TCE using suspended and chitosan-bead immobilized Pseudomonas putida. J Hazard Mater 148(3):660–670. https://doi.org/10.1016/j.jhazmat.2007.03.030
Chen C-Y, Yeh K-L, Aisyah R, Lee D-J, Chang J-S (2011) Cultivation, photobioreactor design and harvesting of microalgae for biodiesel production: a critical review. Bioresour Technol 102(1):71–81. https://doi.org/10.1016/j.biortech.2010.06.159
Chen L, Liu T, Zhang W, Chen X, Wang J (2012) Biodiesel production from algae oil high in free fatty acids by two-step catalytic conversion. Bioresour Technol 111(Supplement C):208–214. https://doi.org/10.1016/j.biortech.2012.02.033
Chen C, Wei L, Guo X, Guo S, Yan G (2014) Investigation of heavy oil refinery wastewater treatment by integrated ozone and activated carbon -supported manganese oxides. Fuel Process Technol 124(0):165–173. https://doi.org/10.1016/j.fuproc.2014.02.024
Chenl Y, Celia DGE (1994) Effects of pH on the growth and carbon uptake of marine phytoplankton. Depart Biol Sci Dartmouth Coll Hanover, New Hampshire 3755:83–94
Chinnasamy S, Ramakrishnan B, Bhatnagar A, Das CK (2009) Biomass production potential of a wastewater alga Chlorella vulgaris ARC 1 under elevated levels of CO2 and temperature. Int J Mol Sci 10(2). https://doi.org/10.3390/ijms10020518
Chinnasamy S, Bhatnagar A, Hunt RW, Das KC (2010) Microalgae cultivation in a wastewater dominated by carpet mill effluents for biofuel applications. Bioresour Technol 101(9):3097–3105. https://doi.org/10.1016/j.biortech.2009.12.026
Chisti Y (2007) Biodiesel from microalgae. Biotechnol Adv 25(3):294–306. https://doi.org/10.1016/j.biotechadv.2007.02.001
Chiu S-Y, Kao C-Y, Chen C-H, Kuan T-C, Ong S-C, Lin C-S (2008) Reduction of CO2 by a high-density culture of Chlorella sp. in a semicontinuous photobioreactor. Bioresour Technol 99(9):3389–3396. https://doi.org/10.1016/j.biortech.2007.08.013
Chiu S-Y, Kao C-Y, Tsai M-T, Ong S-C, Chen C-H, Lin C-S (2009) Lipid accumulation and CO2 utilization of Nannochloropsis oculata in response to CO2 aeration. Bioresour Technol 100(2):833–838. https://doi.org/10.1016/j.biortech.2008.06.061
Cho K, Lee C-H, Ko K, Lee Y-J, Kim K-N, Kim M-K, Chung Y-H, Kim D, Yeo I-K, Oda T (2016) Use of phenol-induced oxidative stress acclimation to stimulate cell growth and biodiesel production by the oceanic microalga Dunaliella salina. Algal Res 17:61–66. https://doi.org/10.1016/j.algal.2016.04.023
Chu F-LE, Webb KL (1984) Polyunsaturated fatty acids and neutral lipids in developing larvae of the oyster, Crassostrea virginica. Lipids 19(11):815. https://doi.org/10.1007/BF02534509
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 Process Process Intensif 48(6):1146–1151
Costard GS, Machado RR, Barbarino E, Martino RC, Lourenccedil SO (2012) Chemical composition of five marine microalgae that occur on the Brazilian coast. Int J Fisheries Aquaculture 4(9):191–201
Cristóvão RO, Botelho CM, Martins RJE, Loureiro JM, Boaventura RAR (2014) Primary treatment optimization of a fish canning wastewater from a Portuguese plant. Water Res Industry 6(0):51–63. https://doi.org/10.1016/j.wri.2014.07.002
Damjanović L, Rakić V, Rac V, Stošić D, Auroux A (2010) The investigation of phenol removal from aqueous solutions by zeolites as solid adsorbents. J Hazard Mater 184(1–3):477–484. https://doi.org/10.1016/j.jhazmat.2010.08.059
Das B, Mandal TK, Patra S (2015) A comprehensive study on Chlorella pyrenoidosa for phenol degradation and its potential applicability as biodiesel feedstock and animal feed. Appl Biochem Biotechnol 176(5):1382–1401. https://doi.org/10.1007/s12010-015-1652-9
Das B, Mandal T, Patra S (2016) Biodegradation of phenol by a novel diatom BD1IITG-kinetics and biochemical studies. Int J Environ Sci Technol 13(2):529–542
Dassey AJ, Theegala CS (2013) Harvesting economics and strategies using centrifugation for cost effective separation of microalgae cells for biodiesel applications. Bioresour Technol 128(Supplement C):241–245. https://doi.org/10.1016/j.biortech.2012.10.061
Dayana Priyadharshini S, Bakthavatsalam AK (2016) Optimization of phenol degradation by the microalga Chlorella pyrenoidosa using Plackett–Burman design and response surface methodology. Bioresour Technol 207:150–156. https://doi.org/10.1016/j.biortech.2016.01.138
De Martino A, Iorio M, Prenzler PD, Ryan D, Obied HK, Arienzo M (2013) Adsorption of phenols from olive oil waste waters on layered double hydroxide, hydroxyaluminium–iron-co-precipitate and hydroxyaluminium–iron–montmorillonite complex. Appl Clay Sci 80–81:154–161. https://doi.org/10.1016/j.clay.2013.01.014
De Sena RF, Tambosi JL, Genena AK, Moreira RFPM, Schröder HF, José HJ (2009) Treatment of meat industry wastewater using dissolved air flotation and advanced oxidation processes monitored by GC–MS and LC–MS. Chem Eng J 152(1):151–157. https://doi.org/10.1016/j.cej.2009.04.021
Demirbas A (2007) Importance of biodiesel as transportation fuel. Energy Policy 35(9):4661–4670. https://doi.org/10.1016/j.enpol.2007.04.003
Di Iaconi C (2012) Biological treatment and ozone oxidation: integration or coupling? Bioresour Technol 106(0):63–68. https://doi.org/10.1016/j.biortech.2011.12.007
Diya’uddeen BH, Daud WMAW, Abdul Aziz AR (2011) Treatment technologies for petroleum refinery effluents: a review. Process Saf Environ Prot 89(2):95–105. https://doi.org/10.1016/j.psep.2010.11.003
Dobson RS, Burgess JE (2007) Biological treatment of precious metal refinery wastewater: a review. Miner Eng 20(6):519–532. https://doi.org/10.1016/j.mineng.2006.10.011
Dosta J, Nieto JM, Vila J, Grifoll M, Mata-Álvarez J (2011) Phenol removal from hypersaline wastewaters in a membrane biological reactor (MBR): operation and microbiological characterisation. Bioresour Technol 102(5):4013–4020. https://doi.org/10.1016/j.biortech.2010.11.123
Doucha J, Straka F, Lívanský K (2005) Utilization of flue gas for cultivation of microalgae Chlorella sp. in an outdoor open thin-layer photobioreactor. J Appl Phycol 17(5):403–412. https://doi.org/10.1007/s10811-005-8701-7
El-Naas MH, Al-Muhtaseb SA, Makhlouf S (2009) Biodegradation of phenol by Pseudomonas putida immobilized in polyvinyl alcohol (PVA) gel. J Hazard Mater 164(2–3):720–725. https://doi.org/10.1016/j.jhazmat.2008.08.059
El-Naas MH, Al-Zuhair S, Makhlouf S (2010) Continuous biodegradation of phenol in a spouted bed bioreactor (SBBR). Chem Eng J 160(2):565–570. https://doi.org/10.1016/j.cej.2010.03.068
El-Naas MH, Alhaija MA, Al-Zuhair S (2014) Evaluation of a three-step process for the treatment of petroleum refinery wastewater. J Environ Chem Eng 2(1):56–62. https://doi.org/10.1016/j.jece.2013.11.024
El-Sheekh MM, Hamouda RA, Nizam AA (2013) Biodegradation of crude oil by Scenedesmus obliquus and Chlorella vulgaris growing under heterotrophic conditions. Int Biodeterior Biodegrad 82:67–72. https://doi.org/10.1016/j.ibiod.2012.12.015
Estrada-Arriaga EB, Zepeda-Aviles JA, García-Sánchez L (2016) Post-treatment of real oil refinery effluent with high concentrations of phenols using photo-ferrioxalate and Fenton’s reactions with membrane process step. Chem Eng J 285:508–516. https://doi.org/10.1016/j.cej.2015.10.030
Fabregas J, Herrero C, Cabezas B, Abalde J (1986) Biomass production and biochemical composition in mass cultures of the marine microalga Isochrysis galbana Parke at varying nutrient concentrations. Aquaculture 53(2):101–113. https://doi.org/10.1016/0044-8486(86)90280-2
Fava F, Armenante PM, Kafkewitz D (1995) Aerobic degradation and dechlorination of 2-chlorophenol, 3-chlorophenol and 4-chlorophenol by a Pseudomonas pickettii strain. Lett Appl Microbiol 21:307–312
Fernández I, Suárez-Ojeda ME, Pérez J, Carrera J (2013) Aerobic biodegradation of a mixture of monosubstituted phenols in a sequencing batch reactor. J Hazard Mater 260:563–568. https://doi.org/10.1016/j.jhazmat.2013.05.052
Fontes AG, Angeles Vargas M, Moreno J, Guerrero MG, Losada M (1987) Factors affecting the production of biomass by a nitrogen-fixing blue-green alga in outdoor culture. Biomass 13(1):33–43. https://doi.org/10.1016/0144-4565(87)90070-9
Gatenby CM, Orcutt DM, Kreeger DA, Parker BC, Jones VA, Neves RJ (2003) Biochemical composition of three algal species proposed as food for captive freshwater mussels. J Appl Phycol 15(1):1–11
González G, Herrera G, Garci MT, Peña M (2001) Biodegradation of phenolic industrial wastewater in a fluidized bed bioreactor with immobilized cells of Pseudomonas putida. Bioresour Technol 80(2):137–142. https://doi.org/10.1016/S0960-8524(01)00076-1
Greca MD, Monaco P, Pollio A, Previtera L (1992) Structure-activity relationships of phenylpropanoids as growth inhibitors of the green alga Selenastrum capricornutum. Phytochemistry 31(12):4119–4123. https://doi.org/10.1016/0031-9422(92)80425-E
Hao OJ, Kim MH, Seagren EA, Kim H (2002) Kinetics of phenol and chlorophenol utilization by Acinetobacter species. Chemosphere 46(6):797–807. https://doi.org/10.1016/S0045-6535(01)00182-5
Hirooka T, Akiyama Y, Tsuji N, Nakamura T, Nagase H, Hirata K, Miyamoto K (2003) Removal of hazardous phenols by microalgae under photoautotrophic conditions. J Biosci Bioeng 95(2):200–203. https://doi.org/10.1016/S1389-1723(03)80130-5
Hirooka T, Nagase H, Hirata K, Miyamoto K (2006) Degradation of 2,4-dinitrophenol by a mixed culture of photoautotrophic microorganisms. Biochem Eng J 29(1–2):157–162. https://doi.org/10.1016/j.bej.2005.03.018
Ho K-L, Lin B, Chen Y-Y, Lee D-J (2009) Biodegradation of phenol using Corynebacterium sp. DJ1 aerobic granules. Bioresour Technol 100(21):5051–5055. https://doi.org/10.1016/j.biortech.2009.05.050
Hoh D, Watson S, Kan E (2016) Algal biofilm reactors for integrated wastewater treatment and biofuel production: a review. Chem Eng J 287(Supplement C):466–473. https://doi.org/10.1016/j.cej.2015.11.062
Huong P-T, Lee B-K, Kim J (2016) Improved removal of 2-chlorophenol by a synthesized Cu-nano zeolite. Process Saf Environ Prot 100:272–280. https://doi.org/10.1016/j.psep.2016.02.002
Ji M-K, Kabra AN, Choi J, Hwang J-H, Kim JR, Abou-Shanab RAI, Oh Y-K, Jeon B-H (2014) Biodegradation of bisphenol A by the freshwater microalgae Chlamydomonas mexicana and Chlorella vulgaris. Ecol Eng 73:260–269. https://doi.org/10.1016/j.ecoleng.2014.09.070
Ji M-K, Yun H-S, Park Y-T, Kabra AN, Oh I-H, Choi J (2015) Mixotrophic cultivation of a microalga Scenedesmus obliquus in municipal wastewater supplemented with food wastewater and flue gas CO2 for biomass production. J Environ Manag 159:115–120. https://doi.org/10.1016/j.jenvman.2015.05.037
Jiang Y, Cai X, Wu D, Ren N (2010) Biodegradation of phenol and m-cresol by mutated Candida tropicalis. J Environ Sci 22(4):621–626. https://doi.org/10.1016/S1001-0742(09)60154-6
Jones CR, Cook JR (1978) Culture pH, CO2 tension, and cell division in Euglena gracilis Z. J Cell Physiol 96(2):253–259. https://doi.org/10.1002/jcp.1040960214
Khan KA, Suidan MT, Cross WH (1981) Anaerobic activated carbon filter for the treatment of phenol-bearing wastewater. J Water Pollut Control Fed 53(10):1519–1532
Kitaya Y, Azuma H, Kiyota M (2005) Effects of temperature, CO2/O2 concentrations and light intensity on cellular multiplication of microalgae, Euglena gracilis. Adv Space Res 35(9):1584–1588. https://doi.org/10.1016/j.asr.2005.03.039
Klekner V, Kosaric N (1992a) Degradation of phenolic mixtures by chlorella. Environ Technol 13(5):503–506. https://doi.org/10.1080/09593339209385177
Klekner V, Kosaric N (1992b) Degradation of phenols by algae. Environ Technol 13(5):493–501. https://doi.org/10.1080/09593339209385176
Knuckey RM, Brown MR, Barrett SM, Hallegraeff GM (2002) Isolation of new nanoplanktonic diatom strains and their evaluation as diets for juvenile Pacific oysters (Crassostrea gigas). Aquaculture 211(1–4):253–274. https://doi.org/10.1016/S0044-8486(02)00010-8
Knuckey RM, Brown MR, Robert R, Frampton DMF (2006) Production of microalgal concentrates by flocculation and their assessment as aquaculture feeds. Aquac Eng 35(3):300–313. https://doi.org/10.1016/j.aquaeng.2006.04.001
Kong W-B, Yang H, Cao Y-T, Song H, Hua S-F, Xia C-G (2013) Effect of glycerol and glucose on the enhancement of biomass, lipid and soluble carbohydrate production by Chlorella vulgaris in mixotrophic culture. Food Technol Biotechnol 51(1):62–69
Lai B, Zhang Y, Chen Z, Yang P, Zhou Y, Wang J (2014) Removal of p-nitrophenol (PNP) in aqueous solution by the micron-scale iron–copper (Fe/Cu) bimetallic particles. Appl Catal B Environ 144(Supplement C):816–830. https://doi.org/10.1016/j.apcatb.2013.08.020
Levén L, Nyberg K, Korkea-aho L, Schnürer A (2006) Phenols in anaerobic digestion processes and inhibition of ammonia oxidising bacteria (AOB) in soil. Sci Total Environ 364(1):229–238. https://doi.org/10.1016/j.scitotenv.2005.06.003
Li Y, Chen Y-F, Chen P, Min M, Zhou W, Martinez B, Zhu J, Ruan R (2011) Characterization of a microalga Chlorella sp. well adapted to highly concentrated municipal wastewater for nutrient removal and biodiesel production. Bioresour Technol 102(8):5138–5144. https://doi.org/10.1016/j.biortech.2011.01.091
Li C, Li Y, Cheng X, Feng L, Xi C, Zhang Y (2013) Immobilization of Rhodococcus rhodochrous BX2 (an acetonitrile-degrading bacterium) with biofilm-forming bacteria for wastewater treatment. Bioresour Technol 131(0):390–396. https://doi.org/10.1016/j.biortech.2012.12.140
Li D, Wang L, Zhao Q, Wei W, Sun Y (2015) Improving high carbon dioxide tolerance and carbon dioxide fixation capability of Chlorella sp. by adaptive laboratory evolution. Bioresour Technol 185:269–275. https://doi.org/10.1016/j.biortech.2015.03.011
Li Y, Tabassum S, Zhang Z (2016) An advanced anaerobic biofilter with effluent recirculation for phenol removal and methane production in treatment of coal gasification wastewater. J Environ Sci 47:23–33. https://doi.org/10.1016/j.jes.2016.03.012
Lika K, Papadakis IA (2009) Modeling the biodegradation of phenolic compounds by microalgae. J Sea Res 62(2–3):135–146. https://doi.org/10.1016/j.seares.2009.02.005
Lima SAC, Castro PML, Morais R (2003) Biodegradation of p-nitrophenol by microalgae. J Appl Phycol 15(2):137–142. https://doi.org/10.1023/A:1023877420364
Liu H, Yu QJ, Wang G, Ye F, Cong Y (2011a) Biodegradation of phenol at high concentration by a novel yeast Trichosporon montevideense PHE1. Process Biochem 46(8):1678–1681. https://doi.org/10.1016/j.procbio.2011.04.008
Liu J, Chen F, Huang J (2011b) Microalgae as feedstocks for biodiesel production. INTECH Open Access Publisher,
Lovell CR, Eriksen NT, Lewitus AJ, Chen YP (2002) Resistance of the marine diatom Thalassiosira sp. to toxicity of phenolic compounds. Mar Ecol Prog Ser 229:11–18
Lu Y, Yan L, Wang Y, Zhou S, Fu J, Zhang J (2009) Biodegradation of phenolic compounds from coking wastewater by immobilized white rot fungus Phanerochaete chrysosporium. J Hazard Mater 165(1–3):1091–1097. https://doi.org/10.1016/j.jhazmat.2008.10.091
Lu BL, Qi L, Li MX (2013) Effects of temperature on the growth and product accumulation of Chlorella sp. In: Advanced Materials Research. Trans Tech Publ, pp 428–432
Majumder PS, Gupta SK (2009) Effect of influent pH and alkalinity on the removal of chlorophenols in sequential anaerobic–aerobic reactors. Bioresour Technol 100(5):1881–1883. https://doi.org/10.1016/j.biortech.2008.10.002
Mamma D, Kalogeris E, Papadopoulos N, Hatzinikolaou DG, Christrakopoulos P, Kekos D (2004) Biodegradation of phenol by acclimatized Pseudomonas putida cells using glucose as an added growth substrate. J Environ Sci Health A 39(8):2093–2104. https://doi.org/10.1081/ESE-120039377
Mata TM, Martins AA, Caetano NS (2010) Microalgae for biodiesel production and other applications: a review. Renew Sust Energ Rev 14(1):217–232. https://doi.org/10.1016/j.rser.2009.07.020
Michałowicz J, Duda W (2007) Phenols—sources and toxicity. Pol J Environ Stud 16(3):347–362
Mohamad S, Fares A, Judd S, Bhosale R, Kumar A, Gosh U, Khreisheh M (2017) Advanced wastewater treatment using microalgae: effect of temperature on removal of nutrients and organic carbon. IOP Conf Series: Earth and Environmental Science 67:012032. https://doi.org/10.1088/1755-1315/67/1/012032
Molina Grima E, Belarbi EH, Acién Fernández FG, Robles Medina A, Chisti Y (2003) Recovery of microalgal biomass and metabolites: process options and economics. Biotechnol Adv 20(7):491–515. https://doi.org/10.1016/S0734-9750(02)00050-2
Naoki S, Norio M, Yoshiro M, Nobuo U (1979) Effect of growth temperature on lipid and fatty acid compositions in the blue-green algae, Anabaena variabilis and Anacystis nidulans. Biochimica et Biophysica Acta (BBA) - Lipids and Lipid Metabolism 572(1):19–28. https://doi.org/10.1016/0005-2760(79)90196-6
Nelson DL, Cox M (2000) Lehninger principles of biochemistry, Third edn. Macmillan Worth Publishers, New York
Ngarmkam W, Sirisathitkul C, Phalakornkule C (2011) Magnetic composite prepared from palm shell-based carbon and application for recovery of residual oil from POME. J Environ Manag 92(3):472–479. https://doi.org/10.1016/j.jenvman.2010.08.031
Ogbonda KH, Aminigo RE, Abu GO (2007) Influence of temperature and pH on biomass production and protein biosynthesis in a putative Spirulina sp. Bioresour Technol 98(11):2207–2211
Ozyonar F, Karagozoglu B (2015) Treatment of pretreated coke wastewater by electrocoagulation and electrochemical peroxidation processes. Sep Purif Technol 150:268–277. https://doi.org/10.1016/j.seppur.2015.07.011
Padilla-Sánchez JA, Plaza-Bolaños P, Romero-González R, Barco-Bonilla N, Martínez-Vidal JL, Garrido-Frenich A (2011) Simultaneous analysis of chlorophenols, alkylphenols, nitrophenols and cresols in wastewater effluents, using solid phase extraction and further determination by gas chromatography–tandem mass spectrometry. Talanta 85(5):2397–2404. https://doi.org/10.1016/j.talanta.2011.07.081
Pakshirajan K, Chugh D, Saravanan P (2008) Feasibility of m-cresol degradation using an indigenous mixed microbial culture with glucose as co-substrate. Clean Techn Environ Policy 10(3):303–308. https://doi.org/10.1007/s10098-007-0120-9
Papazi A, Kotzabasis K (2007) Bioenergetic strategy of microalgae for the biodegradation of phenolic compounds—exogenously supplied energy and carbon sources adjust the level of biodegradation. J Biotechnol 129(4):706–716. https://doi.org/10.1016/j.jbiotec.2007.02.021
Papazi A, Kotzabasis K (2008) Inductive and resonance effects of substituents adjust the microalgal biodegradation of toxical phenolic compounds. J Biotechnol 135(4):366–373. https://doi.org/10.1016/j.jbiotec.2008.05.009
Papazi A, Assimakopoulos K, Kotzabasis K (2012) Bioenergetic strategy for the biodegradation of p-cresol by the unicellular green alga Scenedesmus obliquus. PLoS One 7(12):e51852. https://doi.org/10.1371/journal.pone.0051852
Pazarlioğlu NK, Telefoncu A (2005) Biodegradation of phenol by Pseudomonas putida immobilized on activated pumice particles. Process Biochem 40(5):1807–1814. https://doi.org/10.1016/j.procbio.2004.06.043
Pinto G, Pollio A, Previtera L, Temussi F (2002) Biodegradation of phenols by microalgae. Biotechnol Lett 24(24):2047–2051. https://doi.org/10.1023/a:1021367304315
Pittman JK, Dean AP, Osundeko O (2011) The potential of sustainable algal biofuel production using wastewater resources. Bioresour Technol 102(1):17–25. https://doi.org/10.1016/j.biortech.2010.06.035
Product process and service directory (2001) Met Finish 99, Supplement 1 (0):884–914. https://doi.org/10.1016/S0026-0576(01)85341-1
Puyol D, Mohedano AF, Rodriguez JJ, Sanz JL (2011) Effect of 2,4,6-trichlorophenol on the microbial activity of adapted anaerobic granular sludge bioaugmented with Desulfitobacterium strains. New Biotechnol 29(1):79–89. https://doi.org/10.1016/j.nbt.2011.06.011
Rahim Pouran S, Abdul Aziz AR, Wan Daud WMA (2015) Review on the main advances in photo-Fenton oxidation system for recalcitrant wastewaters. J Ind Eng Chem 21:53–69. https://doi.org/10.1016/j.jiec.2014.05.005
Ramanan R, Kannan K, Deshkar A, Yadav R, Chakrabarti T (2010) Enhanced algal CO2 sequestration through calcite deposition by Chlorella sp. and Spirulina platensis in a mini-raceway pond. Bioresour Technol 101(8):2616–2622. https://doi.org/10.1016/j.biortech.2009.10.061
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 Energy 88(10):3411–3424. https://doi.org/10.1016/j.apenergy.2010.11.025
Razo-Flores E, Donlon B, Lettinga G, Field JA (1997) Biotransformation and biodegradation of N-substituted aromatics in methanogenic granular sludge. FEMS Microbiol Rev 20(3–4):525–538. https://doi.org/10.1111/j.1574-6976.1997.tb00335.x
Reis MTA, Freitas OMF, Agarwal S, Ferreira LM, Ismael MRC, Machado R, Carvalho JMR (2011) Removal of phenols from aqueous solutions by emulsion liquid membranes. J Hazard Mater 192(3):986–994. https://doi.org/10.1016/j.jhazmat.2011.05.092
Ren H-Y, Liu B-F, Ma C, Zhao L, Ren N-Q (2013) A new lipid-rich microalga Scenedesmus sp. strain R-16 isolated using Nile red staining: effects of carbon and nitrogen sources and initial pH on the biomass and lipid production. Biotechnology for Biofuels 6(1):143. https://doi.org/10.1186/1754-6834-6-143
Renaud SM, Thinh L-V, Parry DL (1999) The gross chemical composition and fatty acid composition of 18 species of tropical Australian microalgae for possible use in mariculture. Aquaculture 170(2):147–159. https://doi.org/10.1016/S0044-8486(98)00399-8
Richmond A, Cheng-Wu Z, Zarmi Y (2003) Efficient use of strong light for high photosynthetic productivity: interrelationships between the optical path, the optimal population density and cell-growth inhibition. Biomol Eng 20(4):229–236. https://doi.org/10.1016/S1389-0344(03)00060-1
Safi C, Zebib B, Merah O, Pontalier P-Y, Vaca-Garcia C (2014) Morphology, composition, production, processing and applications of Chlorella vulgaris: a review. Renew Sust Energ Rev 35:265–278. https://doi.org/10.1016/j.rser.2014.04.007
Salmerón-Alcocer A, Ruiz-Ordaz N, Juárez-Ramírez C, Galíndez-Mayer J (2007) Continuous biodegradation of single and mixed chlorophenols by a mixed microbial culture constituted by Burkholderia sp., Microbacterium phyllosphaerae, and Candida tropicalis. Biochem Eng J 37(2):201–211. https://doi.org/10.1016/j.bej.2007.04.015
Sandnes JM, Källqvist T, Wenner D, Gislerød HR (2005) Combined influence of light and temperature on growth rates of Nannochloropsis oceanica: linking cellular responses to large-scale biomass production. J Appl Phycol 17(6):515–525. https://doi.org/10.1007/s10811-005-9002-x
Sanjeev Kumar S, Kumar MS, Siddavattam D, Karegoudar TB (2012) Generation of continuous packed bed reactor with PVA–alginate blend immobilized Ochrobactrum sp. DGVK1 cells for effective removal of N,N-dimethylformamide from industrial effluents. J Hazard Mater 199–200(Supplement C):58–63. https://doi.org/10.1016/j.jhazmat.2011.10.053
Semple KT (1997) Biodegradation of phenols by a eukaryotic alga. Res Microbiol 148(4):365–367. https://doi.org/10.1016/S0923-2508(97)81592-6
Semple KT (1998) Heterotrophic growth on phenolic mixtures by Ochromonas danica. Res Microbiol 149(1):65–72. https://doi.org/10.1016/S0923-2508(97)83625-X
Semple KT, Cain RB (1996) Biodegradation of phenols by the alga Ochromonas danica. Appl Environ Microbiol 62(4):1265–1273
She Z, Gao M, Jin C, Chen Y, Yu J (2005) Toxicity and biodegradation of 2,4-dinitrophenol and 3-nitrophenol in anaerobic systems. Process Biochem 40(9):3017–3024. https://doi.org/10.1016/j.procbio.2005.02.007
Sim TS, Goh A, Becker EW (1988) Comparison of centrifugation, dissolved air flotation and drum filtration techniques for harvesting sewage-grown algae. Biomass 16(1):51–62. https://doi.org/10.1016/0144-4565(88)90015-7
Singh RK, Kumar S, Kumar S, Kumar A (2008) Biodegradation kinetic studies for the removal of p-cresol from wastewater using Gliomastix indicus MTCC 3869. Biochem Eng J 40(2):293–303. https://doi.org/10.1016/j.bej.2007.12.015
Soeder CJ, Hegewald E, Fiolitakis E, Grobbelaar JU (1985) Temperature dependence of population growth in a green microalga: thermodynamic characteristics of growth intensity and the influence of cell concentration. Zeitschrift für Naturforschung C, vol 40. doi:https://doi.org/10.1515/znc-1985-3-416
Surkatti R, El-Naas MH (2014) Biological treatment of wastewater contaminated with p-cresol using Pseudomonas putida immobilized in polyvinyl alcohol (PVA) gel. J Water Process Eng 1(0):84–90. https://doi.org/10.1016/j.jwpe.2014.03.008
Surkatti R, El-Naas MH (2017) Competitive interference during the biodegradation of cresols. Int J Environ Sci Technol doi:https://doi.org/10.1007/s13762-017-1383-2
Tang D, Han W, Li P, Miao X, Zhong J (2011) CO2 biofixation and fatty acid composition of Scenedesmus obliquus and Chlorella pyrenoidosa in response to different CO2 levels. Bioresour Technol 102(3):3071–3076. https://doi.org/10.1016/j.biortech.2010.10.047
Taraldsvik M, Myklestad S (2000) The effect of pH on growth rate, biochemical composition and extracellular carbohydrate production of the marine diatom Skeletonema costatum. Eur J Phycol 35(2):189–194. https://doi.org/10.1080/09670260010001735781
Terlizzi DE, Karlander EP (1980) Growth of a coccoid nanoplankter (Eustigmatophyceae) from the Chesapeake BAy as influenced by light, temperature, salinity and nitrogen source in factorial combination 1. J Phycol 16(3):364–368. https://doi.org/10.1111/j.1529-8817.1980.tb03046.x
Thakurta SG, Aakula M, Chakrabarty J, Dutta S (2018) Bioremediation of phenol from synthetic and real waste water using Leptolyngbya sp.—a comparison and assessment of lipid production. 3 Biotech 8:206. https://doi.org/10.1007/s13205-018-1229-8
Torzillo G, Pushparaj B, Masojidek J, Vonshak A (2003) Biological constraints in algal biotechnology. Biotechnol Bioprocess Eng 8(6):338–348. https://doi.org/10.1007/BF02949277
Tsai S-Y, Juang R-S (2006) Biodegradation of phenol and sodium salicylate mixtures by suspended Pseudomonas putida CCRC 14365. J Hazard Mater 138(1):125–132. https://doi.org/10.1016/j.jhazmat.2006.05.044
Tsekova K, Todorova D, Ganeva S (2010) Removal of heavy metals from industrial wastewater by free and immobilized cells of Aspergillus niger. Int Biodeterior Biodegrad 64(6):447–451. https://doi.org/10.1016/j.ibiod.2010.05.003
Uduman N, Qi Y, Danquah MK, Forde GM, Hoadley A (2010) Dewatering of microalgal cultures: a major bottleneck to algae-based fuels. J Renew Sustain Energy 2(1):012701. https://doi.org/10.1063/1.3294480
Vandamme D, Foubert I, Muylaert K (2013) Flocculation as a low-cost method for harvesting microalgae for bulk biomass production. Trends Biotechnol 31(4):233–239. https://doi.org/10.1016/j.tibtech.2012.12.005
Vargas M, Rodriguez H, Moreno J, Olivares H, Del Campo J, Rivas J, Guerrero M (1998) Biochemical composition and fatty acid content of filamentous nitrogen-fixing cyanobacteria. J Phycol 34(5):812–817
Vázquez I, Rodríguez-Iglesias J, Marañón E, Castrillón L, Álvarez M (2007) Removal of residual phenols from coke wastewater by adsorption. J Hazard Mater 147(1–2):395–400. https://doi.org/10.1016/j.jhazmat.2007.01.019
Védrine C, Leclerc J-C, Durrieu C, Tran-Minh C (2003) Optical whole-cell biosensor using Chlorella vulgaris designed for monitoring herbicides. Biosens Bioelectron 18(4):457–463
Viggiani A, Olivieri G, Siani L, Di Donato A, Marzocchella A, Salatino P, Barbieri P, Galli E (2006) An airlift biofilm reactor for the biodegradation of phenol by Pseudomonas stutzeri OX1. J Biotechnol 123(4):464–477
Visviki I, Santikul D (2000) The pH tolerance of Chlamydomonas applanata (Volvocales, Chlorophyta). Arch Environ Contam Toxicol 38(2):147–151
Vonshak A, Abeliovich A, Boussiba S, Arad S, Richmond A (1982) Production of spirulina biomass: effects of environmental factors and population density. Biomass 2(3):175–185. https://doi.org/10.1016/0144-4565(82)90028-2
Wahidin S, Idris A, Shaleh SRM (2013) The influence of light intensity and photoperiod on the growth and lipid content of microalgae Nannochloropsis sp. Bioresour Technol 129(Supplement C):7–11. https://doi.org/10.1016/j.biortech.2012.11.032
Wang Y, Tian Y, Han B, H-b Z, Bi J-n, B-l C (2007) Biodegradation of phenol by free and immobilized Acinetobacter sp. strain PD12. J Environ Sci 19(2):222–225. https://doi.org/10.1016/S1001-0742(07)60036-9
Wang B, Li Y, Wu N, Lan CQ (2008) CO2 bio-mitigation using microalgae. Appl Microbiol Biotechnol 79(5):707–718. https://doi.org/10.1007/s00253-008-1518-y
Wang L, Li Y, Chen P, Min M, Chen Y, Zhu J, Ruan RR (2010a) Anaerobic digested dairy manure as a nutrient supplement for cultivation of oil-rich green microalgae Chlorella sp. Bioresour Technol 101(8):2623–2628. https://doi.org/10.1016/j.biortech.2009.10.062
Wang L, Li Y, Yu P, Xie Z, Luo Y, Lin Y (2010b) Biodegradation of phenol at high concentration by a novel fungal strain Paecilomyces variotii JH6. J Hazard Mater 183(1–3):366–371. https://doi.org/10.1016/j.jhazmat.2010.07.033
Wang L, Min M, Li Y, Chen P, Chen Y, Liu Y, Wang Y, Ruan R (2010c) Cultivation of green algae Chlorella sp. in different wastewaters from municipal wastewater treatment plant. Appl Biochem Biotechnol 162(4):1174–1186
Wang L, Xue C, Wang L, Zhao Q, Wei W, Sun Y (2016) Strain improvement of Chlorella sp. for phenol biodegradation by adaptive laboratory evolution. Bioresour Technol 205:264–268. https://doi.org/10.1016/j.biortech.2016.01.022
Wei Z, Liang F, Liu Y, Luo W, Wang J, Yao W, Zhu Y (2017) Photoelectrocatalytic degradation of phenol-containing wastewater by TiO2/g-C3N4 hybrid heterostructure thin film. Appl Catal B Environ 201:600–606. https://doi.org/10.1016/j.apcatb.2016.09.003
Whyte JN (1987) Biochemical composition and energy content of six species of phytoplankton used in mariculture of bivalves. Aquaculture 60(3–4):231–241
Winkler J, Reyes LH, Kao KC (2013) Adaptive laboratory evolution for strain engineering. Methods Mol Biol (Clifton, NJ) 985:211–222. https://doi.org/10.1007/978-1-62703-299-5_11
Xie D, Li C, Tang R, Lv Z, Ren Y, Wei C, Feng C (2014) Ion-exchange membrane bioelectrochemical reactor for removal of nitrate in the biological effluent from a coking wastewater treatment plant. Electrochem Commun 46(0):99–102. https://doi.org/10.1016/j.elecom.2014.06.020
Xin L, Hong-Ying H, Yu-Ping Z (2011) Growth and lipid accumulation properties of a freshwater microalga Scenedesmus sp. under different cultivation temperature. Bioresour Technol 102(3):3098–3102
Yan J, Jianping W, Hongmei L, Suliang Y, Zongding H (2005) The biodegradation of phenol at high initial concentration by the yeast Candida tropicalis. Biochem Eng J 24(3):243–247. https://doi.org/10.1016/j.bej.2005.02.016
Yan J, Jianping W, Jing B, Daoquan W, Zongding H (2006) Phenol biodegradation by the yeast Candida tropicalis in the presence of m-cresol. Biochem Eng J 29(3):227–234. https://doi.org/10.1016/j.bej.2005.12.002
Yang J, Rasa E, Tantayotai P, Scow KM, Yuan H, Hristova KR (2011) Mathematical model of Chlorella minutissima UTEX2341 growth and lipid production under photoheterotrophic fermentation conditions. Bioresour Technol 102(3):3077–3082. https://doi.org/10.1016/j.biortech.2010.10.049
Yao H, Ren Y, Deng X, Wei C (2011) Dual substrates biodegradation kinetics of m-cresol and pyridine by Lysinibacillus cresolivorans. J Hazard Mater 186(2–3):1136–1140. https://doi.org/10.1016/j.jhazmat.2010.11.118
Zhang L-S, Wu W-Z, Wang J-I (2007) Immobilization of activated sludge using improved polyvinyl alcohol (PVA) gel. J Environ Sci 19(11):1293–1297. https://doi.org/10.1016/s1001-0742(07)60211-3
Zhou G-M, Fang HHP (1997) Co-degradation of phenol and m-cresol in a UASB reactor. Bioresour Technol 61(1):47–52. https://doi.org/10.1016/S0960-8524(97)84698-6
Zhou J, Yu X, Ding C, Wang Z, Zhou Q, Pao H, Cai W (2011) Optimization of phenol degradation by Candida tropicalis Z-04 using Plackett-Burman design and response surface methodology. J Environ Sci 23(1):22–30. https://doi.org/10.1016/S1001-0742(10)60369-5
Zhu L, Yuefeng D, Jianping Z, Ji C (2011) Adsorption of phenol from water by N-butylimidazolium functionalized strongly basic anion exchange resin. J Colloid Interface Sci 364(2):462–468. https://doi.org/10.1016/j.jcis.2011.08.068
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This work was supported by the Emirates Center for Energy and Environment Research [grant number 31R070].
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Surkatti, R., Al-Zuhair, S. Microalgae cultivation for phenolic compounds removal. Environ Sci Pollut Res 25, 33936–33956 (2018). https://doi.org/10.1007/s11356-018-3450-8
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DOI: https://doi.org/10.1007/s11356-018-3450-8