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Frontiers of Environmental Science & Engineering

ISSN 2095-2201

ISSN 2095-221X(Online)

CN 10-1013/X

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2018 Impact Factor: 3.883

Front. Environ. Sci. Eng.    2020, Vol. 14 Issue (6) : 113    https://doi.org/10.1007/s11783-020-1292-3
RESEARCH ARTICLE
Enhanced enzymatic removal of anthracene by the mangrove soil-derived fungus, Aspergillus sydowii BPOI
Paul Olusegun Bankole1(), Kirk Taylor Semple2, Byong-Hun Jeon3, Sanjay Prabhu Govindwar3
1. Department of Pure and Applied Botany, College of Biosciences, Federal University of Agriculture Abeokuta, Ogun State 234039, Nigeria
2. Lancaster Environment Centre, Lancaster University, Lancaster LA1 4YQ, UK
3. Department of Earth Resources and Environmental Engineering, Hanyang University, Seoul 04763, Republic of Korea
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Abstract

A. sydowii strain bpo1 exhibited 99.8% anthracene degradation efficiency.

• Four unique metabolic products were obtained after anthracene degradation.

• Ligninolytic enzymes induction played vital roles in the removal of anthracene.

• Laccase played a crucial role in comparison with other enzymes induced.

The present study investigated the efficiency of Aspergillus sydowii strain bpo1 (GenBank Accession Number: MK373021) in the removal of anthracene (100 mg/L). Optimal degradation efficiency (98.7%) was observed at neutral pH, temperature (30℃), biomass weight (2 g) and salinity (0.2% w/v) within 72 h. The enzyme analyses revealed 131%, 107%, and 89% induction in laccase, lignin peroxidase, and manganese peroxidase respectively during anthracene degradation. Furthermore, the degradation efficiency (99.8%) and enzyme induction were significantly enhanced with the addition of 100 mg/L of citric acid and glucose to the culture. At varying anthracene concentrations (100–500 mg/L), the degradation rate constants (k1) peaked with increasing concentration of anthracene while the half-life (t1/2) decreases with increase in anthracene concentration. Goodness of fit (R2 = 0.976 and 0.982) was observed when the experimental data were subjected to Langmuir and Temkin models respectively which affirmed the monolayer and heterogeneous nature exhibited by A. sydwoii cells during degradation. Four distinct metabolites; anthracene-1,8,9 (2H,8aH,9aH)-trione, 2,4a-dihydronaphthalene-1,5-dione, 1,3,3a,7a-tetrahydro-2-benzofuran-4,7-dione and 2-hydroxybenzoic acid was obtained through Gas Chromatography-Mass spectrometry (GC-MS). A. sydowii exhibited promising potentials in the removal of PAHs.

Keywords Aspergillus sydowii      Anthracene      Biodegradation      Polycyclic aromatic hydrocarbons     
Corresponding Author(s): Paul Olusegun Bankole   
Issue Date: 13 November 2020
 Cite this article:   
Paul Olusegun Bankole,Kirk Taylor Semple,Byong-Hun Jeon, et al. Enhanced enzymatic removal of anthracene by the mangrove soil-derived fungus, Aspergillus sydowii BPOI[J]. Front. Environ. Sci. Eng., 2020, 14(6): 113.
 URL:  
https://academic.hep.com.cn/fese/EN/10.1007/s11783-020-1292-3
https://academic.hep.com.cn/fese/EN/Y2020/V14/I6/113
Fig.1  Phylogenetic typing through maximum-likelihood method of A. sydowii strain bpo1. The tree was inferred from the analysis of sequence data (ITS genes) with a scale bar of 0.020 indicating the genetic distance
Fig.2  Influence of (a) concentration, (b) temperature, (c) contact time, (d) salinity and (e) pH on degradation efficiencies and biomass. Graphs were plotted as mean±standard error of means
Fig.3  Influence of organic acids and glucose on (a) anthracene degradation efficiency, (b) induction of laccase, (c) induction of lignin peroxidase and (d) induction manganese peroxidase
Fig.4  Proposed metabolic pathway of anthracene degradation by A. sydowii
PAH Fungi Concentration
(mg/L)
Temperature
(℃)
Degradation efficiency
(%)
Time
(days)
Enzymes Reference
Anthracene sydowii 200 30 99.8 3 MnP, LiP, Lac Present study
fumigatus 10 30 60 5 LiP Ye et al., 2011
terreus 50 30 60 7 ND Capotorti et al., 2005
fusca 50 22 94 5 ND Villemain et al., 2006
L. gongylophorus 10 30 71.8 11 Lac Ike et al., 2019
F. palustris 1000 24 31.7 20 MnP, LiP, Lac Arun et al., 2008
D. elegans 1000 24 2.4 20 MnP, LiP, Lac Arun et al., 2008
P. ostreatus 1000 24 19 20 MnP, LiP, Lac Arun et al., 2008
C. versicolor 1000 24 22.4 20 MnP, LiP, Lac Arun et al., 2008
P. sanguineus 1000 24 15.6 20 MnP, LiP, Lac Arun et al., 2008
Tab.1  Comparison of anthracene biodegradation by A. sydowii strain bpo1 with reference to other fungi in similar conditions
1 A B Al-Hawash, X Zhang, F Ma (2019). Removal and biodegradation of different petroleum hydrocarbons using the filamentous fungus Aspergillus sp. RFC-1. MicrobiologyOpen, 8(1): e00619
2 V A Alva, B M Peyton (2003). Phenol and catechol biodegradation by the haloalkaliphile Halomonas campisalis: influence of pH and salinity. Environmental Science & Technology, 37(19): 4397–4402
https://doi.org/10.1021/es0341844
3 R Ambrosoli, L Petruzzelli, J Luis Minati, Ajmone F Marsan(2005). Anaerobic PAH degradation in soil by a mixed bacterial consortium under denitrifying conditions. Chemosphere, 60(9): 1231–1236
https://doi.org/10.1016/j.chemosphere.2005.02.030
4 A Arun, P P Raja, R Arthi, M Ananthi, K S Kumar, M Eyini (2008). Polycyclic aromatic hydrocarbons (PAHs) biodegradation by basidiomycetes fungi, Pseudomonas isolate, and their cocultures: comparative in vivo and in silico approach. Applied Biochemistry and Biotechnology, 151(2–3): 132–142
https://doi.org/10.1007/s12010-008-8160-0
5 C Balachandran, V Duraipandiyan, K Balakrishna, S Ignacimuthu (2012). Petroleum and polycyclic aromatic hydrocarbons (PAHs) degradation and naphthalene metabolism in Streptomyces sp. (ERI-CPDA-1) isolated from oil contaminated soil. Bioresource Technology, 112: 83–90
https://doi.org/10.1016/j.biortech.2012.02.059
6 O Baltrons, M Lopez-Mesas, M Vilaseca, C Gutierrez-Bouzan, F Le Derf, F Portet-Koltalo, C Palet (2018). Influence of a mixture of metals on PAHs biodegradation processes in soils. Science of the Total Environment, 628–629: 150–158
https://doi.org/10.1016/j.scitotenv.2018.02.013
7 P O Bankole, A A Adekunle, S P Govindwar (2018). Enhanced decolorization and biodegradation of Acid Red 88 dye by newly isolated fungus, Achaetomium strumarium. Journal of Environmental Chemical Engineering, 6(2): 1589–1600
https://doi.org/10.1016/j.jece.2018.01.069
8 W G Birolli, D de A Santos, N Alvarenga, A C F S Garcia, L P C Romao, A L M Porto (2018). Biodegradation of anthracene and several PAHs by the marine derived fungus Cladosporium sp. CBMAI 1237. Marine Pollution Bulletin, 129: 525–533
https://doi.org/10.1016/j.marpolbul.2017.10.023
9 B W Bogan, R T Lamar (1996). Polycyclic aromatic hydrocarbon degrading capabilities of Phanerochaete laevis HHB-1625 and its extracellular ligninolytic enzymes. Applied and Environmental Microbiology, 62(5): 1597–1603
https://doi.org/10.1128/AEM.62.5.1597-1603.1996
10 H Cao, C Wang, H Liu, W Jia, H Sun (2020). Enzyme activities during Benzo[a] pyrene degradation by the fungus Lasiodiplodia theobromae isolated from a polluted soil. Scientific Reports, 10(1): 865
https://doi.org/10.1038/s41598-020-57692-6
11 G Capotorti, P Cesti, A Lombardi, G Guglielmetti (2005). Formation of sulfate conjugates metabolites in the degradation of phenanthrene, anthracene, pyrene and benzo[a]pyrene by the ascomycete Aspergillus terreus. Polycyclic Aromatic Compounds, 25(3): 197–213
https://doi.org/10.1080/10406630590950273
12 C E Cerniglia (1997). Fungal metabolism of polycyclic aromatic 1424 hydrocarbons: past, present and future applications in 1425 bioremediation. Journal of Industrial Microbiology and Biotechnology, 19(5–6): 324–333
13 C E Cerniglia, J B Sutherland (2010). Degradation of polycyclic aromatic hydrocarbons by fungi. In: Timmis K, editor. Handbook of Hydrocarbon and Lipid Microbiology. Berlin-Heidelberg: Springer, 2079–2110
https://doi.org/10.1007/978-3-540-77587-4_151
14 P J Collins, M J J Kotterman, J A Field, A D W Dobson (1996). Oxidation of anthracene and benzo[a]pyrene by laccases from Trametes versicolor. Applied and Environmental Microbiology, 62(12): 4563–4567
https://doi.org/10.1128/AEM.62.12.4563-4567.1996
15 J J Doyle (1990). Isolation of plant DNA from fresh tissue. Focus (San Francisco, Calif.), 12: 13–15
16 B Gong, P Wu, B Ruan, Y Zhang, X Lai, L Yu, Y Li, Z Dang (2018). Differential regulation of phenanthrene biodegradation process by kaolinite and quartz and the underlying mechanism. Journal of Hazardous Materials, 349: 51–59
https://doi.org/10.1016/j.jhazmat.2018.01.046
17 T Hadibarata, R A Kristanti (2014). Potential of a white-rot fungus Pleurotus eryngii F032 for degradation and transformation of fluorene. Fungal Biology, 118(2): 222–227
https://doi.org/10.1016/j.funbio.2013.11.013
18 K E Hammel, B Green, W Z Gai (1991). Ring fission of anthracene 1611 by a eukaryote. Proceedings of the National Academy of Sciences of the United States of America, 88(23): 10605–10608
https://doi.org/10.1073/pnas.88.23.10605
19 H M Hwang, X Hu, X Zhao (2007). Enhanced bioremediation of polycyclic aromatic hydrocarbons by environmentally friendly techniques. Journal of Environmental Science and Health, 25: 313–352
20 P T L Ike, W G Birolli, D M dos Santos, A L M Porto, D H F Souza (2019). Biodegradation of anthracene and different PAHs by a yellow laccase from Leucoagaricus gongylophorus. Environmental Science and Pollution Research International, 26(9): 8675–8684
https://doi.org/10.1007/s11356-019-04197-z
21 R J S Jacques, B C Okeke, F M Bento, A S Teixeira, M C R Peralba, F A O Camargo (2008). Microbial consortium bioaugmentation of a polycyclic aromatic hydrocarbons contaminated soil. Bioresource Technology, 99(7): 2637–2643
https://doi.org/10.1016/j.biortech.2007.04.047
22 R J S Jacques, E C Santos, F M Bento, M C R Peralba, P A Selbach, E L S Sa, F A O Camargo (2005). Anthracene biodegradation by Pseudomonas sp. isolated from a petrochemical sludge land farming site. International Biodeterioration & Biodegradation, 56(3): 143–150
https://doi.org/10.1016/j.ibiod.2005.06.005
23 R S Juang, F C Wu, R L Tseng (1996). Adsorption isotherms of phenolic compounds from aqueous solution onto activated carbon fibers. Journal of Chemical & Engineering Data, 41(3): 487–492
https://doi.org/10.1021/je950238g
24 S Kumar, G Stecher, M Li, C Knyaz, K Tamura (2018). MEGA X: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution, 35(6): 1547–1549
https://doi.org/10.1093/molbev/msy096
25 A Majcherczyk, C Johannes, A Hüttermann (1998). Oxidation of polycyclic aromatic hydrocarbons (PAH) by laccase of Trametes versicolor. Enzyme and Microbial Technology, 22(5): 335–341
https://doi.org/10.1016/S0141-0229(97)00199-3
26 R Müller, G Antranikian, S Maloney, R Sharp (1998). Thermophilic degradation of environmental pollutants. In Biotechnology of Extremophiles. Part of Advances in Biochemical Engineering/Biotechnology, 61: 155–169
https://doi.org/10.1007/BFb0102292
27 H Punnapayak, S Prasongsuk, K Messner, K Danmek, P Lotrakul (2009). Polycyclic aromatic hydrocarbons (PAHs) degradation by laccase from a tropical white rot fungus Ganoderma lucidum. African Journal of Biotechnology, 8(21): 5897–5900
https://doi.org/10.5897/AJB09.1073
28 K Ramadass, M Megharaj, K Venkateswarlu, R Naidu (2016). Soil bacterial strains with heavy metal resistance and high potential in degrading diesel oil and n-alkanes. International Journal of Environmental Science and Technology, 13(12): 2863–2874
https://doi.org/10.1007/s13762-016-1113-1
29 M I Rashid, L H Mujawar, T Shahzad, T Almeelbi, I M Ismail, M Oves (2016). Bacteria and fungi can contribute to nutrients bioavailability and aggregate formation in degraded soils. Microbiology Research, 183: 26–41
https://doi.org/10.1016/j.micres.2015.11.007
30 S K Samanta, O V Singh, R K Jain (2002). Polycyclic aromatic hydrocarbons: environmental pollution and bioremediation. Trends in Biotechnology, 20(6): 243–248
https://doi.org/10.1016/S0167-7799(02)01943-1
31 E C Santos, R J S Jacques, F M Bento, M C R Peralba, P A Selbach, E L S Sá, F A O Cameroon (2008). Anthracene biodegradation and surface activity by an iron-stimulated Pseudomonas sp. Bioresource Technology, 99(7): 2644–2649
https://doi.org/10.1016/j.biortech.2007.04.050
32 X M Su, A M Bamba, S Zhang, Y G Zhang, M Z Hashmi, H J Lin, L X Ding (2018). Revealing potential functions of VBNC bacteria in polycyclic aromatic hydrocarbons biodegradation. Letters in Applied Microbiology, 66(4): 277–283
https://doi.org/10.1111/lam.12853
33 K Tamura, M Nei (1993). Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution, 10: 512–526
34 W T E Ting, S Y Yuan, S D Wu, B V Chang (2011). Biodegradation of phenanthrene and pyrene by Ganoderma lucidum. International Biodeterioration & Biodegradation, 65(1): 238–242
https://doi.org/10.1016/j.ibiod.2010.11.007
35 D Villemain, P Guiraud, O Bordjiba, R Steiman (2006). Biotransformation of anthracene and fluoranthene by Absidia fusca Linnemann. Electronic Journal of Biotechnology, 9(2): 107–116
https://doi.org/10.2225/vol9-issue2-fulltext-10
36 C Wang, H Sun, J Li, Y Li, Q Zhang (2009).Enzyme activities during degradation of polycyclic aromatic hydrocarbons by white rot fungus Phanerochaete chrysosporium in soils. Chemosphere, 77: 733–738
37 X Wen, Y Jia, J Li (2009). Degradation of tetracycline and oxytetracycline by crude lignin peroxidase prepared from Phanerochaete chrysosporium white rot fungus. Chemosphere, 75(8): 1003–1007
https://doi.org/10.1016/j.chemosphere.2009.01.052
38 Y Wu, Y Xu, N Zhou (2020). A newly defined dioxygenase system from Mycobacterium vanbaalenii PYR-1 endowed with an enhanced activity of dihydroxylation of high-molecular-weight polyaromatic hydrocarbons. Frontiers of Environmental Science and Engineering, 14(1): 14.
39 J Ye, H Yin, J Qiang, H Peng, H Qin, N Zhang, B He (2011). Biodegradation of anthracene by Aspergillus fumigatus. Journal of Hazardous Materials, 185(1): 174–181
https://doi.org/10.1016/j.jhazmat.2010.09.015
40 S Y Yuan, B V Chang (2007). Anaerobic degradation of five polycyclic aromatic hydrocarbons from river sediment in Taiwan. Journal of Environmental Science and Health, Part B: Pesticides, Food contaminants and Agricultural wastes, 42(1): 63–69
https://doi.org/10.1080/03601230601020860
41 J H Zhang, Q H Xue, H Gao, X Ma, P Wang (2016). Degradation of crude oil by fungal enzyme preparations from Aspergillus spp. For potential use in enhanced oil recovery. Journal of Chemical Technology and Biotechnology (Oxford, Oxfordshire), 91(4): 865–875
https://doi.org/10.1002/jctb.4650
42 X X Zhang, S P Cheng, C J Zhu, S L Sun (2006). Microbial PAH degradationin soil: degradation pathways and contributing factors. Pedosphere, 16(5): 555–565
https://doi.org/10.1016/S1002-0160(06)60088-X
43 Z Zheng, J P Obbard (2002). Removal of surfactant solubilized polycyclic aromatic hydrocarbons by Phanerochaete chrysosporium in a rotating biological contactor reactor. Journal of Biotechnology, 96(3): 241–249
https://doi.org/10.1016/S0168-1656(02)00050-0
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