Abstract
A non-white rot fungus, Penicillium simplicissimum (isolate 10), was investigated for its biodegradation activities towards toxic triphenylmethane (TPM) dyes such as Crystal Violet (CV), Methyl Violet (MV), Malachite Green (MG), and Cotton Blue (CB). High decolorization efficiencies of 98.7, 97.5, 97.1, and 96.1% were observed for CV, MV, MG, and CB, respectively, within 2 h of incubation in the dye solutions (50 mg L−1, pH 5.0, 25 ± 2 °C). UV–visible spectral analysis of dyes conducted before and after treatment with P. simplicissimum indicated the occurrence of biodegradation. This was confirmed when enzymatic analyzes revealed induced production of manganese peroxidase (MnP, EC 1.11.1.13; 23.31 U mL−1), tyrosinase (EC 1.14.18.1; 16.18 U mL−1), and triphenylmethane reductase activities (1.15 U mL−1), particularly in biodegrading MG. For MV and CB, increased activities of tyrosinase (20.35 and 18.74 U mL−1, respectively) were detected, whereas no enzyme activities were detected for CV. Dye biodegradation by P. simplicissimum led to reduced toxicity (particularly for MG) based on phytotoxicity and microbial toxicity assays. It was concluded that P. simplicissimum showed potential in biodegrading and detoxifying TPM dyes via MnP, tyrosinase and triphenylmethane reductase activities, resulting in less harmful treated dye solutions.
Graphical abstract
Article Highlights
-
P. simplicissimum biodegraded TPM dyes via enzymatic activities
-
Rapid and efficient decolourization (96.1–98.7%) were achieved within 2 h
-
MnP, tyrosinase, and triphenylmethane reductase biodegrades TPM dyes
-
Dye biodegradation reduced dye toxicity (particularly for MG)
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abd El Monssef RA, Hassan EA, Ramadan EM (2016) Production of laccase enzyme for their potential application to decolorize fungal pigments on aging paper and parchment. Ann Agric Sci 61:145–154. https://doi.org/10.1016/j.aoas.2015.11.007
Agrawal N, Verma P, Shahi SK (2018) Degradation of polycyclic aromatic hydrocarbons (phenanthrene and pyrene) by the ligninolytic fungi Ganoderma lucidum isolated from the hardwood stump. Bioresour Bioprocess 5:11. https://doi.org/10.1186/s40643-018-0197-5
Ahmad MSA, Hussain M, Ijaz S, Alvi AK (2008) Photosynthetic performance of two mung bean (Vigna radiata) cultivars under lead and copper stress. Int J Agri Biol 10:167–172
Ali HM, Shehata SF, Ramadan KMA (2016) Microbial decolorization and degradation of crystal violet dye by Aspergillus niger. Int J Environ Sci Technol 13:2917–2926. https://doi.org/10.1007/s13762-016-1117-x
Almeida EJ, Corso CR (2014) Comparative study of toxicity of azo dye Procion Red MX-5B following biosorption and biodegradation treatments with the fungi Aspergillus niger and Aspergillus terreus. Chemosphere 112:317–322. https://doi.org/10.1016/j.chemosphere.2014.04.060
Asgher M, Ramzan M, Bilal M (2016) Purification and characterization of manganese peroxidases from native and mutant Trametes versicolor IBL-04. Chin J Catal 37:561–570. https://doi.org/10.1016/S1872-2067(15)61044-0
Ayed L, Chaieb K, Cheref A, Bakhrouf A (2008) Biodegradation of triphenylmethane dye Malachite Green by Sphingomonas paucimobilis. World J Microbiol Biotechnol 25:705–711. https://doi.org/10.1007/s11274-008-9941-x
Banerjee S, Dubey S, Gautam RK, Chattopadhyaya MC, Sharma YC (2017) Adsorption characteristics of alumina nanoparticles for the removal of hazardous dye, Orange G from aqueous solutions. Arab J Chem. https://doi.org/10.1016/j.arabjc.2016.12.016
Barapatre A, Aadil KR, Jha H (2017) Biodegradation of Malachite Green by the Ligninolytic Fungus Aspergillus flavus. Clean (Weinh) 45:1600045. https://doi.org/10.1002/clen.201600045
Bergsten-Torralba LR, Nishikawa MM, Baptista DF, Magalhães DP, da Silva M (2009) Decolorization of different textile dyes by Penicillium simplicissimum and toxicity evaluation after fungal treatment. Braz J Microbiol 40:808–817. https://doi.org/10.1590/S1517-838220090004000011
Bora P, Holschuh H, da Silva Vasconcelos M (2004) Characterization of polyphenol oxidase of soursop (Annona muricata L.) fruit and a comparative study of its inhibition in enzyme extract and in pulp. Cienc Tecnol Aliment 4:267–273. https://doi.org/10.1080/11358120409487770
Bouras HD, Yeddou AR, Bouras N, Hellel D, Holtz MD, Sabaou N, Chergui A, Nadjemi B (2017) Biosorption of Congo red dye by Aspergillus carbonarius M333 and Penicillium glabrum Pg1: Kinetics, equilibrium and thermodynamic studies. J Taiwan Inst Chem Eng 80:915–923. https://doi.org/10.1016/j.jtice.2017.08.002
Casas N, Parella T, Vicent T, Caminal G, Sarra M (2009) Metabolites from the biodegradation of triphenylmethane dyes by Trametes versicolor or laccase. Chemosphere 75:1344–1349. https://doi.org/10.1016/j.chemosphere.2009.02.029
Chaturvedi V, Verma P (2015) Biodegradation of malachite green by a novel copper-tolerant Ochrobactrum pseudogrignonense strain GGUPV1 isolated from copper mine waste water. Bioresour Bioprocess 2:1. https://doi.org/10.1186/s40643-015-0070-8
Chaudhry MT, Zohaib M, Rauf N, Tahir SS, Parvez S (2014) Biosorption characteristics of Aspergillus fumigatus for the decolorization of triphenylmethane dye acid violet 49. Appl Microbiol Biotechnol 98:3133–3141. https://doi.org/10.1007/s00253-013-5306-y
Chen SH, Ting ASY (2015a) Biodecolorization and biodegradation potential of recalcitrant triphenylmethane dyes by Coriolopsis sp. isolated from compost. J Environ Manage 150:274–280. https://doi.org/10.1016/j.jenvman.2014.09.014
Chen SH, Ting ASY (2015b) Biosorption and biodegradation potential of triphenylmethane dyes by newly discovered Penicillium simplicissimum isolated from indoor wastewater sample. Int Biodeterior Biodegrad 103:1–7. https://doi.org/10.1016/j.ibiod.2015.04.004
El-Batal AI, ElKenawy NM, Yassin AS, Amin MA (2015) Laccase production by Pleurotus ostreatus and its application in synthesis of gold nanoparticles. Biotechnol Rep (Amst) 5:31–39. https://doi.org/10.1016/j.btre.2014.11.001
Franciscon E, Grossman MJ, Paschoal JAR, Reyes FGR, Durrant LR (2012) Decolorization and biodegradation of reactive sulfonated azo dyes by a newly isolated Brevibacterium sp. strain VN-15. SpringerPlus 1:37–37. https://doi.org/10.1186/2193-1801-1-37
Fu XY, Zhao W, Xiong AS, Tian YS, Zhu B, Peng RH, Yao QH (2013) Phytoremediation of triphenylmethane dyes by overexpressing a Citrobacter sp. triphenylmethane reductase in transgenic Arabidopsis. Appl Microbiol Biotechnol 97:1799–1806. https://doi.org/10.1007/s00253-012-4106-0
Jang MS, Lee YM, Kim CH, Lee JH, Kang DW, Kim SJ, Lee YC (2005) Triphenylmethane reductase from Citrobacter sp. strain KCTC 18061P: purification, characterization, gene cloning, and overexpression of a functional protein in Escherichia coli. Appl Environ Microbiol 71:7955–7960. https://doi.org/10.1128/AEM.71.12.7955-7960.2005
Jasińska A, Różalska S, Bernat P, Paraszkiewicz K, Długoński J (2012) Malachite green decolorization by non-basidiomycete filamentous fungi of Penicillium pinophilum and Myrothecium roridum. Int Biodeterior Biodegrad 73:33–40. https://doi.org/10.1016/j.ibiod.2012.06.025
Jayanthy V, Geetha R, Rajendran R, Prabhavathi P, Karthik Sundaram S, Dinesh Kumar S, Santhanam P (2014) Phytoremediation of dye contaminated soil by Leucaena leucocephala (subabul) seed and growth assessment of Vigna radiata in the remediated soil. Saudi J Biol Sci 21:324–333. https://doi.org/10.1016/j.sjbs.2013.12.001
Jegan J, Vijayaraghavan J, Bhagavathi Pushpa T, Sardhar Basha SJ (2016) Application of seaweeds for the removal of cationic dye from aqueous solution. Desalin Water Treat 57:25812–25821. https://doi.org/10.1080/19443994.2016.1151835
Jin S, Zhang G, Zhang P, Fan S, Li F (2015) High-pressure homogenization pretreatment of four different lignocellulosic biomass for enhancing enzymatic digestibility. Bioresour Technol 181:270–274. https://doi.org/10.1016/j.biortech.2015.01.069
Kalyani DC, Telke AA, Surwase SN, Jadhav SB, Lee JK, Jadhav JP (2012) Effectual decolorization and detoxification of triphenylmethane dye malachite green (MG) by Pseudomonas aeruginosa NCIM 2074 and its enzyme system. Clean Technol Environ Policy 14:989–1001. https://doi.org/10.1007/s10098-012-0473-6
Kim MH, Kim Y, Park HJ, Lee JS, Kwak SN, Jung WH, Lee SG, Kim D, Lee YC, Oh TK (2008) Structural insight into bioremediation of triphenylmethane dyes by Citrobacter sp. triphenylmethane reductase. J Biol Chem 283:31981–31990. https://doi.org/10.1074/jbc.M804092200
Kumar CG, Mongolla P, Basha A, Joseph J, Sarma VU, Kamal A (2011) Decolorization and biotransformation of triphenylmethane dye, methyl violet, by Aspergillus sp. isolated from Ladakh, India. J Microbiol Biotechnol 21:267–273. https://doi.org/10.4014/jmb.1011.11010
Lima DR, Klein L, Dotto GL (2017) Application of ultrasound modified corn straw as adsorbent for malachite green removal from synthetic and real effluents. Environ Sci Pollut Res Int 24:21484–21495. https://doi.org/10.1007/s11356-017-9802-y
Mani S, Bharagava RN (2016) Exposure to Crystal Violet, its toxic, genotoxic and carcinogenic effects on environment and its degradation and detoxification for environmental safety. In: Voogt WP (ed) Reviews of environmental contamination and toxicology. Springer, Switzerland, pp 71–104
Matpang P, Sriuttha M, Piwpuan N (2017) Effects of malachite green on growth and tissue accumulation in pak choy (Brassica chinensis Tsen & Lee). ANRES 51:96–102. https://doi.org/10.1016/j.anres.2016.10.008
Moturi B, Singara Charya MA (2009) Decolourisation of Crystal Violet and Malachite Green by fungi. Sci World J 4:28–33
Pandey AK, Sarada DVL, Kumar A (2016) Microbial decolorization and degradation of Reactive Red 198 azo dye by a newly isolated alkaligenes species. Proc Natl Acad Sci India B Biol Sci 86:805–815. https://doi.org/10.1007/s40011-015-0497-x
Radha KV, Regupathi I, Arunagiri A, Murugesan T (2005) Decolorization studies of synthetic dyes using Phanerochaete chrysosporium and their kinetics. Process Biochem 40:3337–3345. https://doi.org/10.1016/j.procbio.2005.03.033
Rodrigues CS, Madeira LM, Boaventura RA (2013) Treatment of textile dye wastewaters using ferrous sulphate in a chemical coagulation/flocculation process. Environ Technol 34:719–729. https://doi.org/10.1080/09593330.2012.715679
Shanmugam S, Ulaganathan P, Sivasubramanian S, Esakkimuthu S, Krishnaswamy S, Subramaniam S (2017) Trichoderma asperellum laccase mediated crystal violet degradation–Optimization of experimental conditions and characterization. J Environ Chem Eng 5:222–231. https://doi.org/10.1016/j.jece.2016.11.044
Shedbalkar U, Jadhav JP (2011) Detoxification of malachite green and textile industrial effluent by Penicillium ochrochloron. Biotechnol Bioprocess Eng 16:196–204. https://doi.org/10.1007/s12257-010-0069-0
Shedbalkar U, Dhanve R, Jadhav J (2008) Biodegradation of triphenylmethane dye cotton blue by Penicillium ochrochloron MTCC 517. J Hazard Mater 157:472–479. https://doi.org/10.1016/j.jhazmat.2008.01.023
Stancu MM, Grifoll M (2011) Multidrug resistance in hydrocarbon-tolerant Gram-positive and Gram-negative bacteria. J Gen Appl Microbiol 57:1–18
Szewczyk R, Kusmierska A, Bernat P (2018) Ametryn removal by Metarhizium brunneum: Biodegradation pathway proposal and metabolic background revealed. Chemosphere 190:174–183. https://doi.org/10.1016/j.chemosphere.2017.10.011
Ting ASY, Lim SJ, Tan WS (2011) Diversity and metal tolerance of filamentous fungi from analytical wastewater in laboratory. International Congress of the Malaysian Society for Microbiology. Penang, Malaysia, pp 110–113
Vergili I, Kaya Y, Sen U, Gönder ZB, Aydiner C (2012) Techno-economic analysis of textile dye bath wastewater treatment by integrated membrane processes under the zero liquid discharge approach. Resour Conserv Recycl 58:25–35. https://doi.org/10.1016/j.resconrec.2011.10.005
Vyavahare GD, Gurav RG, Jadhav PP, Patil RR, Aware CB, Jadhav JP (2018) Response surface methodology optimization for sorption of malachite green dye on sugarcane bagasse biochar and evaluating the residual dye for phyto and cytogenotoxicity. Chemosphere 194:306–315. https://doi.org/10.1016/j.chemosphere.2017.11.180
Wang M-X, Zhang Q-L, Yao S-J (2015) A novel biosorbent formed of marine-derived Penicillium janthinellum mycelial pellets for removing dyes from dye-containing wastewater. Chem Eng J 259:837–844. https://doi.org/10.1016/j.cej.2014.08.003
Wu Y, Xiao X, Xu C, Cao D, Du D (2013) Decolorization and detoxification of a sulfonated triphenylmethane dye aniline blue by Shewanella oneidensis MR-1 under anaerobic conditions. Appl Microbiol Biotechnol 97:7439–7446. https://doi.org/10.1007/s00253-012-4476-3
Yang X, Zheng J, Lu Y, Jia R (2016) Degradation and detoxification of the triphenylmethane dye malachite green catalyzed by crude manganese peroxidase from Irpex lacteus F17. Environ Sci Pollut Res 23:9585–9597. https://doi.org/10.1007/s11356-016-6164-9
Acknowledgements
This work was supported by the Malaysian Ministry of Higher Education [FRGS/2/2013/STWN01/MUSM/02/2]; and Monash University Malaysia.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
Chen, S.H., Cheow, Y.L., Ng, S.L. et al. Biodegradation of Triphenylmethane Dyes by Non-white Rot Fungus Penicillium simplicissimum: Enzymatic and Toxicity Studies. Int J Environ Res 13, 273–282 (2019). https://doi.org/10.1007/s41742-019-00171-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s41742-019-00171-2