Abstract
The study reports a novel algal system for biofuel production coupled to phenol remediation. High-performance liquid chromatography analysis shows phenol-acclimatized Chlorella pyrenoidosa completely degrades high phenol concentrations of 50–1200 mg/l. The ability of C. pyrenoidosa to efficiently grow on high phenol concentrations was endorsed by its high growth kinetic parameters of Ks (400.54 mg/l) and KI (800.41 mg/l). An enhanced growth rate of 0.072 h−1 was obtained by utilizing optimized physical parameters of biomass concentration (200 mg/l), photoperiodicity (14 h light: 10 h dark) and pH 7. Preadaptation of C. pyrenoidosa to target phenol concentration before actual application for phenol treatment is proposed as a strategy for eliminating lag phase and thus faster growth (0.078 h−1) and degradation (0.561 h−1) rates. Preadaptation further increases µmax (0.22 h−1), Ks (500.54 mg/l) and KI (900.41 mg/l) enhancing efficiency for growth on high phenol concentrations. The practical applicability of C. pyrenoidosa for phenol contaminated wastewater remediation was proved by its ability to completely degrade 10 and 250 mg/l phenol in petroleum refinery wastewater. Phenol stress induced total and neutral lipid production in algal biomass qualifying the spent biomass as a promising source for biodiesel production. Additionally, the residual biomass after lipid extraction served as substrate for bioethanol fermentation adding to efficiency of the process for biofuel applications. These findings suggest an environmentally sustainable process for treatment of phenol pollution and clean energy production which is the need of the hour. The developed process has been covered by an applied patent.
Graphical Abstract
Similar content being viewed by others
References
Abdelwahab O, Amin NK, El Ashtoukhy ES (2009) Electrochemical removal of phenol from oil refinery wastewater. J Hazard Mater 163(711):716
Abuhamed T, Bayraktar E, Mehmetoğlu T, Mehmetoğlu Ü (2004) Kinetics model for growth of Pseudomonas putida F1 during benzene, toluene and phenol biodegradation. Process Biochem 39(8):983–988
Agarry SE, Durojaiye AO, Solomon BO (2008a) Microbial degradation of phenols: a review. Int J Environ Pollut 32:12–28
Agarry SE, Durojaiye AO, Yusuf RO, Aremu MO (2008b) Biodegradation of phenol in refinery wastewater by pure cultures of Pseudomonas aeruginosa NCIB 950 and Pseudomonas fluorescence NCIB 3756. Int J Environ Pollut 32:3–11
Aiba S, Shoda M, Nagatani M (1968) Kinetics of product inhibition in alcohol fermentation. Biotechnol Bioeng 10:845–864
Bai J, Wen J-P, Li H-M, Jiang Y (2007) Kinetic modeling of growth and biodegradation of phenol and m-cresol using Alcaligenes faecalis. Process Biochem 42(4):510–517
Bajaj M, Gallert C, Winter J (2008) Biodegradation of high phenol containing synthetic wastewater by an aerobic fixed bed reactor. Bioresour Technol 99:8376–8381
Banerjee A, Ghoshal AK (2010) Phenol degradation by Bacillus cereus: pathway and kinetic modeling. Bioresour Technol 101:5501–5507
Baranyi J (2010) Modelling and parameter estimation of bacterial growth with distributed lag time. Dissertation, University of Szeged
Bhatnagar A, Bhatnagar M, Chinnasamy S, Das KC (2010) Chlorella minutissima—a promising fuel alga for cultivation in municipal wastewaters. Appl Biochem Biotechnol 161:523–536
Bligh EG, Dyer WJ (1959) A rapid method for total lipid extraction and purification. Can J Biochem Physiol 37:911–917
Chen W, Sommerfeld M, Hu Q (2011) Microwave assisted nile red method for in vivo quantification of neutral lipids in microalgae. Bioresour Technol 102:135–141
Cooney M, Young G, Nagle N (2009) Extraction of bio-oils from microalgae. Sep Purif Rev 38:291–325
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 176:1382–1401
Dey S, Mukherjee S (2010) Performance and kinetic evaluation of phenol biodegradation by mixed microbial culture in a batch reactor. Int J Water Resour Environ Eng 3:40–49
Duan Z (2011) Microbial degradation of phenol by activated sludge in batch reactor. Environ Prot Eng 37:53–63
DuBois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356
Edwards VH (2004) The influence of high substrate concentrations on microbial kinetics. Biotechnol Bioeng 12:679–712
El Naas MH, Al-Zuhair S, Alhajja MA (2010) Removal of phenol from petroleum refinery wastewater through absorption on date pit activated carbon. Chem Eng J 162:997–1005
El-Sheekh MM, Ghareib MM, EL-Souod GWA (2012) Biodegradation of phenolic and polycyclic aromatic compounds by some algae and cyanobacteria. J Bioremed Biodegrad 3:133
Farooq W, Lee YC, Ryu BG, Kim BH, Kim HS, Choi YE, Yang JW (2013) Two-stage cultivation of two Chlorella sp. strains by simultaneous treatment of brewery wastewater and maximizing lipid productivity. Bioresour Technol 132:230–238
Feng Y, Li C, Zhang D (2011) Lipid production of Chlorella vulgaris cultured in artificial wastewater medium. Bioresour Technol 102:101–105
Feng GD, Zhang F, Cheng LH, Xu XH, Zhang L, Chen HL (2013) Evaluation of FTIR and nile red methods for microalgal lipid characterization and biomass composition determination. Bioresour Technol 128:107–112
Firozjaee TT, Najafpour GD, Khavarpour M, Bakhshi Z, Pishgar R, Mousavi N (2011) Phenol biodegradation kinetics in an anaerobic batch reactor. Iranica J Energy Env 2:68–73
Friman H, Schechter A, Ioffe Y, Nitzan Y, Cahan R (2013) Current production in a microbial fuel cell using a pure culture of Cupriavidus basilensis growing in acetate or phenol as a carbon source. Microb Biotechnol 6:425–434
Gao QT, Wong YS, Tam NFY (2011) Removal and biodegradation of nonylphenol by different Chlorella sp. Mar Pollut Bull 63:445–451
Gracia MCC, Camacho GF, Miron AS, Sevilla JMF, Chisti Y, Grima EM (2006) Mixotrophic production of marine microalga Phaeodactylum tricornutum on various carbon sources. J Microbiol Biotechnol 16:689–694
Haldane JBS (1965) Enzyme. MIT Press, Cambridge
Hasan SA, Jabeen S (2015) Degradation kinetics and pathway of phenol by Pseudomonas and Bacillus sp. Biotechnol Biotec Equip 29:45–53
Hu H, Gao K (2003) Optimization of growth and fatty acid composition of a unicellular marine picoplankton, Nannochloropsis sp., with enriched carbon sources. Biotechnol Lett 25:421–425
Jiang HL, Tay JH, Tay STL (2002) Aggregation of immobilized activated sludge cells into aerobically grown microbial granules the aerobic biodegradation of phenol. Lett Appl Microbiol 35:439–445
Jiang ST, Guan YJ, Bai SL (2012) Power generation from phenol degradation using a microbial fuel cell. Adv Mater Res 512:1432–1437
Jou CJG, Huang GC (2003) A pilot study for oil refinery wastewater treatment using a fixed-film bioreactor. Adv Environ Res 7:463–469
Kavitha C, Ashokkumar V, Chinnasamy S, Bhaskar S, Rengasamy R (2014) Pretreatment of lipid extracted Botryococcus braunii spent biomass for bioethanol production. Int J Curr Biotechnol 2:11–18
Kelknar V, Kosarnic N (1992) Degradation of phenols by algae. Environ Technol 13:493–501
Kim KH, Choi IS, Kim HM, Wi SG, Bae HJ (2014) Bioethanol production from the nutrient stress-induced microalga Chlorella vulgaris by enzymatic hydrolysis and immobilized yeast fermentation. Bioresour Technol 153:47–54
Kong WB, Yang H, Cao YT, Song HH, Xia SF (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 51:62–69
Kumar A, Kumar S, Kumar S (2005) Biodegradation kinetics of phenol and catechol using Pseudomonas putida MTCC 1194. Biochem Eng J 22(2):151–159
Kwon KH, Yeom SH (2009) Optimal microbial adaptation routes for the rapid degradation of high concentration of phenol. Bioprocess Biosyst Eng 32:435–442
Laurens LML, Quinn M, Wychen S, Templeton DW, Wolfrum EJ (2012) Accurate and reliable quantification of total microalgal fuel potential as fatty acid methyl esters by in situ transesterification. Anal Bioanal Chem 403:167–178
Lee OK, Oh YK, Lee EY (2015) Bioethanol production from carbohydrate enriched residual biomass obtained after lipid extraction of Chlorella sp. KR-1. Bioresour Technol 196:22–27
Li Y, Li J, Wang C, Wang P (2010) Growth kinetics and phenol biodegradation of psychrotrophic Pseudomonas putida LY1. Bioresour Technol 101:6740–6744
Lika K, Papadakis IA (2009) Modelling biodegradation of phenolic compounds by microalgae. J Sea Res 62:135–146
Lincoln EP, Carmichael WW (1981) Preliminary tests of toxicity of Synechocystis sp. grown on wastewater medium. In: Carmichael WW (ed) The water environment. Springer, New York, pp 223–230
Lv JM, Cheng LH, Xu XH, Zhang L, Chen HL (2010) Enhanced lipid production of Chlorella vulgaris by adjustment of cultivation conditions. Bioresour Technol 101:6797–6804
Magri AD, Magri AL, Balestrieri F, Sacchini A, Marini D (1997) Spectrophotometric micromethod for the determination of ethanol in commercial beverages. Frensenius J Anal Chem 357:985–988
Mahapatra DM, Chanakya HN, Ramachandra TV (2014) Bioremediation and lipid synthesis through mixotrophic algal consortia in municipal wastewater. Bioresour Technol 168:142–150
Maranon E, Vazquez I, Rodriguez J, Castrillon L, Fernandez Y (2008) Coke wastewater treatment by a three-step activated sludge system. Water Air Soil Pollut 192:155–164
Mathur AK, Majumder CB (2010) Kinetics modelling of the biodegradation of benzene, toluene and phenol as single substrate and mixed substrate by using Pseudomonas putida. Chem Biochem Eng 24:101–109
Monteiro ÁAMG, Boaventura RAR, Rodrigues AE (2000) Phenol biodegradation by Pseudomonas putida DSM 548 in a batch reactor. Biochem Eng J 6(1):45–49
Mort SL, Dean-Ross D (1994) Biodegradation of phenolic compounds by sulfate reducing bacteria from contaminated sediments. Microb Ecol 28:67–77
Mosier N, Wyman C, Dale B, Elander R, Lee YY, Holtzapple M, Ladisch M (2005) Features of promising technologies for pretreatment of lignocellulosic biomass. Bioreour Technol 96:673–686
Ojumu TV, Bello OO, Sonibare JA, Solomon BO (2005) Evaluation of microbial systems for bioremediation of petroleum refinery effluents in Nigeria. Afr J Biotechnol 4:31–35
Papazi A, Assimakopoulos K, Kotzabasis K (2012) Bioenergetic strategy for biodegradation of p-cresol by the unicellular green alga Scenedesmus obliquus. PLoS ONE. doi:10.1371/journal.pone.0051852
Patil SS, Jena HM (2015) Statistical optimization of phenol degradation by Bacillus pumilus OS1 using Plackett–Burman design and response surface methodology. Arab J Sci Eng 40:2141–2151
Pinto G, Pollio A, Previtera L, Stanzione M, Temussi F (2003) Removal of low molecular weight phenols from olive oil mill wastewater using microalgae. Biotechnol Lett 25:1657–1659
Pishgar R, Najafpour GD, Mousavi N, Bakhshi Z, Khorrami M (2012) Phenol biodegradation kinetics in the presence of supplimentary substrate. Int J Eng 25(3(B)):181–192
Pistorius AMA, DeGrip WJ, Egorova-Zachernyuk TA (2009) Monitoring of biomass composition from microbiological sources by means of FT-IR spectroscopy. Biotechnol Bioeng 103(1):123–129
Sahoo NK, Ghosh PK, Pakshirajan K (2011a) Kinetics of 4-bromophenol degradation using calcium alginate immobilized Arthrobacter chlorophenolicus A6. Int J Earth Sci Eng 4:663–668
Sahoo NK, Pakshirajan K, Ghosh PK (2011b) Batch Biodegradation of para-nitrophenol using Arthrobacter chlorophenolicus A6. Appl Biochem Biotechnol 165:1587–1596
Saravanan P, Pakshirajan K, Saha P (2008) Growth kinetics of an indigenous mixed microbial constrotium during phenol degradation in a batch reactor. Bioresour Technol 99:205–209
Scragg AH (2006) The effect of phenol on the growth of Chlorella vulgaris and Chlorella VT-1. Enzyme Microb Technol 39(4):796–799
Semple KT, Cain RB (1996) Biodegradation of phenol by algae Ochromonas danica. Appl Environ Microbiol 62:1265–1273
Senthivelan T, Kanagaraj J, Panda RC, Mandal AB (2014) Biodegradation of phenol by mixed microbial culture: an ecofriendly approach for pollution reduction. Clean Technol Environ Policy 16:113–126
Sharma KK, Schuhmann H, Schenk PM (2012) High lipid induction in microalgae for biodiesel production. Energies 5:1532–1553
Tisler T, Zagorc-Koncan J (1997) Comparative assessment of toxicity of phenol, formaldehyde and industrial wastewater to aquatic organisms. Water Air Soil Pollut 97:315–322
Vijayagopal V, Viruthagiri T (2005) Batch kinetic studies in phenol biodegradation and comparison. Indian J Biotechnol 4:565–567
Wang L, Li Y, Yu P, Xie Z, Luo Y, Lin Y (2010) Biodegradation of phenol at high concentration by a novel fungal strain Paecilomyces variotii JH6. J Hazard Mater 183(1–3):366–371
Webb JL (1963) Enzyme and metabolic inhibitors. Academic, New York
Woertz I, Feffer A, Lundquist T, Nelson Y (2009) Algae grown on diary and municipal wastewater for simultaneous nutrient removal and lipid production for biofuel feedstock. J Environ Eng 135:1115–1122
Wolski EA, Durruty I, Haure PM, Gonzalez JF (2012) Penicillium chrysogenum: phenol degradation abilities and kinetic model. Water Air Soil Pollut 223:2323–2332
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
Yang JS, Rasa E, Tantayotai P, Scow KM, Yuan HL, Hristova KR (2011) Mathematical model of Chlorella minutissima UTEX2341 growth and lipid production under photoheterotrophic fermentation conditions. Bioresour Technol 102:3077–3082
Yano T, Nakahara T, Kamiyama S, Yamada K (1966) Kinetic studies on microbial activities in concentrated solutions I effect of excess sugars on oxygen uptake rate of a cell free respiratory system. Agric Biol Chem 30:42–48
Ye F, Shen D (2004) Acclimation of anaerobic sludge degrading chlorophenols and the biodegradation kinetics during acclimation period. Chemosphere 54:1573–1580
Zhao X, Wang Y, Ye Z, Borthwick AGL, Ni J (2006) Oil field wastewater treatment in biological aerated filter by immobilized microorganisms. Process Biochem 41:1475–1483
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 23:22–30
Acknowledgements
Bhaskar Das acknowledge Indian Institute of Technology, Guwahati, for providing research fellowship to pursue doctoral studies at the Centre for the Environment, Indian Institute of Technology, Guwahati. The present work is not financially supported by any funding agency.
Author information
Authors and Affiliations
Corresponding author
Additional information
Editorial responsibiility: G. Ravindran.
Rights and permissions
About this article
Cite this article
Das, B., Selvaraj, G. & Patra, S. An environmentally sustainable process for remediation of phenol polluted wastewater and simultaneous clean energy generation as by-product. Int. J. Environ. Sci. Technol. 16, 147–170 (2019). https://doi.org/10.1007/s13762-017-1599-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13762-017-1599-1