Abstract
Brominated phenols are listed as priority pollutants together with nitrophenol and chlorophenol are the key components of paper pulp wastewater. However, the biodegradation of bromophenol in a mixed substrate system is very scanty. In the present investigation, simultaneous biodegradation kinetics of three substituted phenols 4-bromophenol (4-BP), 4-nitrophenol (4-NP), and 4-chlorophenol (4-CP) were investigated using Arthrobacter chlorophenolicus A6. A 23 full factorial design was applied with varying 4-BP and 4-CP from 75–125 mg/L and 4-NP from 50–100 mg/L. Almost complete degradation of this mixture of substituted phenols was achieved at initial concentration combinations of 125, 125, and 100 mg/L of 4-CP, 4-BP, and 4-NP, respectively, in 68 h. Statistical analysis of the results revealed that, among the three variables, 4-NP had the most prominent influence on the degradation of both 4-CP and 4-BP, while the concentration of 4-CP had a strong negative interaction effect on the biodegradation of 4-NP. Irrespective of the concentration levels of these three substrates, 4-NP was preferentially biodegraded over 4-CP and 4-BP. Furthermore, 4-BP biodegradation rates were found to be higher than those of 4-CP, followed by 4-NP. Besides, the variation of the biomass yield coefficient of the culture was investigated at different initial concentration combinations of these substituted phenols. Although the actinomycetes consumed 4-NP at a faster rate, the biomass yield was very poor. This revealed that the microbial cells were more stressed when grown on 4-NP compared to 4-BP and 4-CP. Overall, this study revealed the potential of A. chlorophenolicus A6 for the degradation of 4-BP in mixed substrate systems.
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References
Acosta CA, Pasquali CEL, Paniagua G, Garcinuño RM, Hernando PF (2018) Evaluation of total phenol pollution in water of San Martin Canal from Santiago del Estero, Argentina. Environ Pollut 236:265–272. https://doi.org/10.1016/j.envpol.2018.01.062
Aktaş Ö (2012) Effect of S0/X0 ratio and acclimation on respirometry of activated sludge in the cometabolic biodegradation of phenolic compounds. Bioresource Technol 111:98–104. https://doi.org/10.1016/j.biortech.2012.02.027
Aranda C, Godoy F, Becerra J, Barra R, Mart´inez M (2003) Aerobic secondary utilization of a non-growth and inhibitorysubstrate 2,4,6-trichlorophenol by Sphingopyxischilensis S37 and Sphingopyxis-like strain S32. Biodegradation 14:265–274
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 198:49–56. https://doi.org/10.1016/j.jhazmat.2011.10.009
Backhaus T (2014) Medicines, shaken and stirred: a critical review on the ecotoxicology of pharmaceutical mixtures. Philos Trans R Soc Lond Ser B-Biol Sci 369(1656):20130585. https://doi.org/10.1098/rstb.2013.0585
Cho K, Lee CH, Ko K, Lee YJ, Kim KN, Kim MK, Chung YH, Kim D, Yeo IK, 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
Cunha I, Moreira S, Santos MM (2015) Review on hazardous and noxious substances (HNS) involved in marine spill incidents—an online database. J Hazard Mater 285:509–516. https://doi.org/10.1016/j.jhazmat.2014.11.005
Darbre P (2019) The history of endocrine-disrupting chemicals. Curr Opin Endocr Metab Res 7:26–33. https://doi.org/10.1016/j.coemr.2019.06.007.
Dayana S, Bakthavatsalam AK (2019) A comparative study on growth and degradation behavior of C. pyrenoidosaon synthetic phenol and phenolic wastewater of a coal gasification plant. J Environ Chem Eng 7:103079. https://doi.org/10.1016/j.jece.2019.103079
Dey S, Mukherjee S (2013) Biodegradation kinetics of bi-substrate solution of phenol and resorcinol in an anaerobic batch reactor. KSCE J Civ Eng 17:1587–1595. https://doi.org/10.1007/s12205-013-0196-1
Dionisi D, Etteh CC (2019) Effect of process conditions on the aerobic biodegradation of phenol and paracetamol by open mixed microbial cultures. J Environ Chem Eng 7:103282. https://doi.org/10.1016/j.jece.2019.103282
Duan W, Meng F, Cui H, Lin Y, Wang G, Wu J (2018) Ecotoxicity of phenol and cresols to aquatic organisms: a review. Ecotoxicol Environ Saf 157:441–456. https://doi.org/10.1016/j.ecoenv.2018.03.089
Duan W, Meng F, Lin Y, Wang G (2017) Toxicological effects of phenol on four marine microalgae. Environ Toxicol Pharmacol 52:170–176. https://doi.org/10.1016/j.etap.2017.04.006
Elhalil A, Tounsadi H, Elmoubarki R, Mahjoubi FZ, Farnane M, Sadiq M, Abdennouri M, Qourzal S, Barka N (2016) Factorial experimental design for the optimization of catalytic degradation of malachite green dye in aqueous solution by Fenton process. Water Resour Ind 15:41–48. https://doi.org/10.1016/j.wri.2016.07.002
Eslami A, Hashemi M, Ghanbari F (2018) Degradation of 4-chlorophenol using catalyzed peroxymonosulfate with nano-MnO2/UV irradiation: Toxicity assessment and evaluation for industrial wastewater treatment. J Clean Prod 195:1389–1397. https://doi.org/10.1016/j.jclepro.2018.05.137
Farag S, Soliman NA, Abdel-Fattah YR (2018) Statistical optimization of crude oil biodegradation by a local marine bacterium isolate Pseudomonas sp. Sp 48. Biotechnol Genet Eng Rev 16:409–420. https://doi.org/10.1016/j.jgeb.2018.01.001
Fernández I, Suárez-Ojeda ME, Pérez J, Carrera J (2013) Aerobic biodegradation of a mixture of monosubstituted phenols in asequencing batch reactor. J Hazard Mater 260:563–568. https://doi.org/10.1016/j.jhazmat.2013.05.052
Fu H, Zhang JJ, Xu Y, Chao HJ, Zhou NY (2017) Simultaneous biodegradation of three mononitrophenol isomers by a tailor-made microbial consortium immobilized in sequential batch reactors. Lett Appl Microbiol 64:203–209. https://doi.org/10.1111/lam.12696
Jiang B, Tan L, Ning S, Shi S (2016) A novel integration system of magnetically immobilized cells and a pair of graphite plate-stainless iron mesh electrodes for the bioremediation of coking wastewater. Bioresour Technol 216:684–690. https://doi.org/10.1016/j.biortech.2016.06.009
Jugder BE, Ertan H, Lee M, Manefield M, Marquis CP (2015) Reductive dehalogenases come of age in biological destruction of organohalides. Trends Biotechnol 33:595–610. https://doi.org/10.1016/j.tibtech.2015.07.004
Khan A, Ahmad A, Ahmad KL, Pado CJ, Van VS, Manzoor N (2015) Effect of two monoterpene phenols on antioxidant defense system in Candida albicans. Microb Pathog 80:50–56. https://doi.org/10.1016/j.micpath.2015.02.004
Khanpour-Alikelayeh E, Partovinia A, Talebi A, Hossein Kermanian H (2020) Investigation of Bacillus licheniformis in the biodegradation of Iranian heavy crude oil: a two-stage sequential approach containing factor-screening and optimization. Ecotoxicol Environ Saf 205:111103. https://doi.org/10.1016/j.ecoenv.2020.111103
Khatoon H, Rai JPN (2020) Optimization studies on biodegradation of atrazine by Bacillus badius ABP6 strain using response surface methodology. Biotechnol Rep 26:e00459. https://doi.org/10.1016/j.btre.2020.e00459
Khoramfar S, Jones KD, Ghobadi J, Parisa Taheri P (2020) Effect of surfactants at natural and acidic pH on microbial activity and biodegradation of mixture of benzene and o-xylene. Chemosphere 260:127471. https://doi.org/10.1016/j.chemosphere.2020.127471
Li GY, Xiong JK, Wong PK, An TC (2016) Enhancing tetrabromobisphenol biodegradation in river sediment microcosms and understanding the corresponding microbial community. Environ Pollut 208:796–802. https://doi.org/10.1016/j.envpol.2015.11.001
Li ZL, Yoshida N, Wang AJ, Nan J, Liang B, Zhang CF, Zhang DD, Suzuki D, Zhou X, Xiao ZX, Katayama A (2015) Anaerobic mineralization of 2,4,6-tribromophenol to CO2 by a synthetic microbial community comprising Clostridiun, Dehalobacter, and Desulfatiglans. Bioresour Technol 176:225–232. https://doi.org/10.1016/j.biortech.2014.10.097
Liang Z, Li G, An T (2017) Purifying, cloning and characterizing a novel dehalogenase from Bacillus sp. GZT to enhance the biodegradation of 2,4,6- tribromophenol in water. Environ Pollut 225:104–111. https://doi.org/10.1016/j.envpol.2017.03.043
Liang Z, Li G, Mai B, An T (2019) Biodegradation of typical BFRs 2,4,6-tribromophenol by an indigenous strain Bacillus sp. GZT isolated from e-waste dismantling area through functional heterologous expression. Sci Total Environ 697:134159. https://doi.org/10.1016/j.scitotenv.2019.134159
Min J, Wang J, Chen W, Hu X (2018) Biodegradation of 2‑chloro‑4‑nitrophenol via a hydroxyquinol pathway by a Gram‑negative bacterium, Cupriavidus sp. strain CNP‑8. AMB Expr 8:43. https://doi.org/10.1186/s13568-018-0574-7
Mohammed-Ridha MJ (2019) Biosorption of PB (II), CR (III), and CD (II) from synthetic wastewater using dried raw waste-activated sludge by response surface methodology. J Eng Sustain Dev 22:80–89. https://doi.org/10.31272/jeasd.2018.2.7
Mohanty SS, Jena HM (2018) Process optimization of butachlor bioremediation by Enterobacter cloacae using plackett burman design and response surface methodology. Proc Saf Environ 119:198–206. https://doi.org/10.1016/j.psep.2018.08.009
Muntathir A, Sagheer A, Onaizi A (2019) Review on phenolic wastewater remediation using homogeneous and heterogeneous enzymatic processes: Current status and potential challenges. Sep Purif Technol 219:186–207. https://doi.org/10.1016/j.seppur.2019.03.028
Nam SN, Cho H, Han J, Her N (2017) Photocatalytic degradation of acesulfameK: optimization using the Box–Behnken design (BBD). Proc Saf Environ 113:10–21. https://doi.org/10.1016/j.psep.2017.09.002
Nordin K, Unell M, Jansson JK (2005) Novel 4-chlorophenol degradation gene cluster and degradation route via hydroxyquinol in Arthrobacter chlorophenolicus A6. Appl Environ Microbiol 71:6538–6544. https://doi.org/10.1128/AEM.71.11.6538-6544.2005
Noszczyńska M, Piotrowska-Seget Z (2018) Bisphenols: application, occurrence, safety, and biodegradation mediated by bacterial communities in wastewater treatment plants and rivers. Chemosphere 201:214–223. https://doi.org/10.1016/j.chemosphere.2018.02.179
Panigrahi N, Barik M, Sahoo NK (2019) Optimization of culture condition of an indigenous culture of Pseudomonas Citronellolis N1 isolated from coke oven wastewater. IJITEE 8(12S):310–315. https://doi.org/10.35940/ijitee.L1082.10812S19
Panigrahy N, Barik M, Sahoo NK (2020a) Kinetics of phenol biodegradation by an indigenous Pseudomonas citronellolis NS1 isolated from coke oven wastewater. J Hazard Toxic Radioact Waste 24:04020019. https://doi.org/10.1061/(ASCE)HZ.2153-5515.0000502
Panigrahy N, Barik M, Sahoo RK, Sahoo NK (2020b) Metabolic profile analysis and kinetics of p-cresol biodegradation by an indigenous Pseudomonas citronellolis NS1 isolated from coke oven wastewater. Int Biodeter Biodegr 147:104837. https://doi.org/10.1016/j.ibiod.2019.104837
Panigrahy N, Pakshirajan K, Sahoo NK (2018) Advances in microbial degradation of substituted phenols with special reference towards Actinomycetes Book title: Bioremediation: Advances in research and applications. Nova, Science Publishers, USA, p 113–151
Peng X, Wang Z, Wei D, Huang Q, Jia X (2017) Biodegradation of tetrabromobisphenol a in the sewage sludge process. J Environ Sci 61:39–48. https://doi.org/10.1016/j.jes.2017.02.023
Rocha ACS, Reis-Henriques MA, Galhano V, Ferreira M, Guimarães L (2016) Toxicity of seven priority hazardous and noxious substances (HNSs) to marine organisms: current status, knowledge gaps and recommendations for future research. Sci Total Environ 542:728–749. https://doi.org/10.1016/j.scitotenv.2015.10.049
Ruan Y, Dou Y, Chen J, Warren A, Li J, Lin X (2018) Evaluation of phenol-induced ecotoxicity in two model ciliate species: population growth dynamics and antioxidant enzyme activity. Ecotoxicol Environ Saf 166:176–185. https://doi.org/10.1016/j.ecoenv.2018.09.091
Saeed A, Altarawneh M, Dlugogorski BZ (2016) Photodecomposition of bromophenols. Chemosphere 150:749–758. https://doi.org/10.1016/j.chemosphere.2015.11.096
Sahoo NK, Pakshirajan K, Ghosh PK (2010) Enhancing the biodegradation of 4-chlorophenol by Arthrobacter chlorophenolicus A6 via medium development. Int Biodet Biodeg 64:474–480. https://doi.org/10.1016/j.ibiod.2010.05.008
Sahoo NK, Pakshirajan K, Ghosh PK (2011a) Batch biodegradation of para-nitrophenol using Arthrobacter chlorophenolicus A6. Appl Biochem Biotechnol 165:1587–1596. https://doi.org/10.1007/s12010-011-9379-8
Sahoo NK, Pakshirajan K, Ghosh PK (2011b) Biodegradation of 4-chlorophenol by Arthrobacter chlorophenolicus A6: effect of culture conditions and degradation kinetics. Biodegradation 22:275–286. https://doi.org/10.1007/s10532-010-9396-2
Sahoo NK, Pakshirajan K, Ghosh PK (2014a) Biodegradation of 4-bromophenol by Arthrobacter chlorophenolicus A6 in batch shake flasks and a continuously operated packed bed reactor. Biodegradation 25:265–276. https://doi.org/10.1007/s10532-013-9658-x
Sahoo NK, Pakshirajan K, Ghosh PK (2014b) Evaluation of 4-bromophenol biodegradation in mixed pollutants system by Arthrobacter chlorophenolicus A6 in an up-flow packed bed reactor. Biodegradation 25:705–718. https://doi.org/10.1007/s10532-014-9693-2
Sahoo SK, Bhattacharya S, Sahoo NK (2020) Photocatalytic degradation of biological recalcitrant pollutants: a green chemistry approach. Biointerface Res Appl Chem 10:5048–5060. https://doi.org/10.33263/BRIAC102.048060
Sayed AEDH, Mohamed NH, Ismail MA, Abdel-Mageed WM, Shoreit AAM (2016) Antioxidant and antiapoptotic activities of Calotropisprocera latex on catfish (Clarias gariepinus) exposed to toxic 4-nonylphenol. Ecotoxicol Environ Saf 128:189–194. https://doi.org/10.1016/j.ecoenv.2016.02.023
Sharma A, Dutta RK (2018) Se-doped CuO NPs/H2O2/UV as a highly efficient and sustainable photo-Fenton catalytic system for enhanced degradation of 4-bromophenol. J Clean Product 185:464–475. https://doi.org/10.1016/j.jclepro.2018.03.049
Sharma NK, Philip L (2014) Effect of cyanide on phenolics and aromatic hydrocarbons biodegradation under anaerobic and anoxic conditions. Chem Eng J 256:255–267. https://doi.org/10.1016/j.cej.2014.06.070
Shi J, Han Y, Xu C, Han H (2018) Biological coupling process for treatment of toxic and refractory compounds in coal gasification wastewater. Rev Environ Sci Biotechnol 17:765–790. https://doi.org/10.1007/s11157-018-9481-2
Shi S, Qu Y, Zhou H, Ma Q, Ma F (2015) Characterization of a novel cometabolic degradation carbazole pathway by a phenol-cultivated Arthrobacter sp. W1. Bioresour Technol 193:281–287. https://doi.org/10.1016/j.biortech.2015.06.106
Spataro F, Ademollo N, Pescatore T, Rauseo J, Patrolecco L (2019) Antibiotic residues and endocrine disrupting compounds in municipal wastewater treatment plants in Rome, Italy. Microchem J 148:634–642. https://doi.org/10.1016/j.microc.2019.05.053
Surkatti R, El-Naas MH (2017) Competitive interference during the biodegradation of cresols. Int. J. Environ. Sci. Technol. 15:301–308
Tian H, Xu X, Qu J, Li H, Hu Y, Huang L, He W, Li B (2020) Biodegradation of phenolic compounds in high saline wastewater by biofilms adhering on aerated membranes. J Hazard Mater 392:122463. https://doi.org/10.1016/j.jhazmat.2020.122463
Unell A, Nordin K, Jernberg C, Stenstrom J, Jansson JK (2008) Degradation of mixtures of phenolic compounds by Arthrobacter chlorophenolicus A6. Biodegradation 19:495–505. https://doi.org/10.1007/s10532-007-9154-2
Varadarajan R, Hari Sankar HS, Jose J, Philip B (2014) Sublethal effects of phenolic compounds on biochemical, histological and ionoregulatory parameters in a tropical teleost fish Oreochromis mossambicus (Peters). Int J Sci Res Publ 4(3):1–12
Varadarajan R, Philip B (2016) Antioxidant responses and lipid peroxidation in Mozambique tilapia (Oreochromis mossambicus) exposed to phenol and m-cresol. Indian J Fish 63(2):86–92. https://doi.org/10.21077/ijf.2016.63.2.20575-11
Wang R, Diao P, Chen Q, Wu H, Xu N, Duan S (2017) Identification of novel pathways for biodegradation of bisphenol A by the green alga Desmodesmus sp. WR1, combined with mechanistic analysis at the transcriptome level. Chem Eng J 321:424–431. https://doi.org/10.1016/j.cej.2017.03.121
Xiao M, Ma H, Sun M, Yin X, Feng Q, Song H, Gai H (2019a) Characterization of cometabolic degradation of p-cresol with phenol as a growth substrate by Chlorella Vulgaris. Bioresour Technol 281:296–302. https://doi.org/10.1016/j.biortech.2019.02.079
Xiao M, Yin X, Gai H, Ma H, Qi Y, Li K, Hua X, Sun M, Song H (2019b) Effect ofhydroxypropyl-β-cyclodextrin on the cometabolism of phenol and phenanthrene by a novel Chryseobacterium sp. Bioresour Technol 273:56–62. https://doi.org/10.1016/j.biortech.2018.10.087
Xie L, Gomes T, Knut Solhaug KA, Song Y, Tollefsen KE (2018) Linking mode of action of the model respiratory and photosynthesis uncoupler 3,5-dichlorophenol to adverse outcomes in Lemna minor. Aquatic Toxicol 197:98–108. https://doi.org/10.1016/j.aquatox.2018.02.005
Xiong J, Li G, An T (2015) Development of methodology for the determination of carbon isotope ratios using gas chromatography/combustion/isotope ratio mass spectrometry and applications in the biodegradation of phenolic brominated flame retardants and their degradation products. Rapid Commun Mass Sp 29(1):54–60. https://doi.org/10.1002/rcm.7072
Xu D, Song X, Qi W, Wang H, Bian Z (2017) Degradation mechanism, kinetics, and toxicity investigation of 4-bromophenol by electrochemical reduction and oxidation with Pd–Fe/graphene catalytic cathodes. Chem Eng J 333:477–485. https://doi.org/10.1016/j.cej.2017.09.173
Zhou Y, Nemati M (2018) Treatment of waters contaminated by phenol and cresols in circulating packed bed bioreactors biodegradation and toxicity evaluations. Water Air Soil Pollut 229:288. https://doi.org/10.1007/s11270-018-3949-0
Zou S, Zhang B, Yan N, Zhang C, Xu H, Zhang Y, Rittmann BE (2018) Competition for molecular oxygen and electron donor between phenol and quinoline during their simultaneous biodegradation. Proc Biochem 70:136–143. https://doi.org/10.1016/j.procbio.2018.04.015
Zou WS, Ji YJ, Wang XF, Zhao QC, Zhang J, Shao Q, Liu J, Wang F, Wang YQ (2016) Insecticide as a precursor to prepare highly bright carbon dots for patterns printing and bioimaging: a new pathway for making poison profitable. Chem Eng J 294:323–332. https://doi.org/10.1016/j.cej.2016.03.004
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MMS: conduct experiments and collected data, analysed sample and data, writing the draft manuscript and editing. SR formal analysis, visualization, review and editing. AD: conceptualization, supervision, review and editing. NKS: conceptualization, supervision, writing, review, and editing, funding acquisition, project administration, funding resources.
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This study was funded by the financial support received from the Department of Biotechnology Government of India, New Delhi (SAN No. 102/IFD/SAN/3610-3612/2016-2017), for carrying out this research work.
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Sahoo, M.M., Sahoo, N.K., Daverey, A. et al. Co-metabolic biodegradation of 4-bromophenol in a mixture of pollutants system by Arthrobacter chlorophenolicus A6. Ecotoxicology 31, 602–614 (2022). https://doi.org/10.1007/s10646-021-02508-0
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DOI: https://doi.org/10.1007/s10646-021-02508-0