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Degradation of polycyclic aromatic hydrocarbons (phenanthrene and pyrene) by the ligninolytic fungi Ganoderma lucidum isolated from the hardwood stump
© The Author(s) 2018
Received: 30 December 2017
Accepted: 1 March 2018
Published: 7 March 2018
Due to progress in science and technology, several harmful polycyclic aromatic hydrocarbons are synthesized and released into the environment. In the present investigation, a phenanthrene- and pyrene-degrading white rot fungi Ganoderma lucidum strain CCG1 was isolated from the Janjgir Champa district of Chhattisgarh, India, and then the degradation of phenanthrene and pyrene was estimated by high-performance liquid chromatography.
Polycyclic aromatic hydrocarbons (PAHs) are a type of xenobiotic compounds that are released into the environment due to incomplete combustion of organic materials such as oil, petroleum gas, wood, municipal and urban waste (Juhasz and Naidu 2000; Ijoma and Tekere 2017; Kadri et al. 2017). PAHs are made up of three or more fused benzene rings, arranged in the linear, cluster or angular arrangements (Di Toro et al. 2000). PAHs are thermodynamically stable due to their strong negative resonance energy. PAHs are highly bioaccumulative compound in soil and sediments because of their high hydrophobicity and low volatility (Singh 2006). The exposure to PAHs causes acute symptoms such as eye irritation, vomiting, and nausea. High concentration of PAHs can also cause kidney and liver damage, skin inflammation, suppress immune reactions, an embryotoxic effect during pregnancy and also show genotoxic, carcinogenic, mutagenic and teratogenic effect (Rostami and Juhasz 2011; Rengarajan et al. 2015). Thus, it is necessary to remediate the PAH compound from the environment. The United States Environmental Protection Agency (USEPA) has been listed 16 PAHs as priority pollutants, including phenanthrene and pyrene (Jin et al. 2007; Puglisi et al. 2007; Wu et al. 2016). Phenanthrene and pyrene are considered as model compounds for the PAH degradation study because they were found most abundantly in the PAH-polluted environment (Bezalel et al. 1996; Makkar and Rockne 2003; Mrozik and Piotrowska-Seget 2010).
Bioremediation is an efficient technique which utilizes the metabolic potential of microorganisms to degrade and transform of PAHs compound to non-toxic compound with less input of chemicals, energy and time (Haritash and Kaushik 2009; Adenipekun et al. 2012). Bioremediation technique removes the toxic compound permanently. It is a less-expensive technique can be used in the site directly (Boopathy 2000). Many bacterial species were able to degrade PAHs (Aitken et al. 1998; Singh 2006) but now researchers concentrate on the degradation of PAHs from the terrestrial and aquatic environment by fungi, because fungi remove PAHs by their cometabolic pathway. Fungi do not use PAHs as a source of their carbon and energy (Wunder et al. 1994; Pothuluri et al. 1995; Casillas et al. 1996). Fungi play robust roles in ecosystem functioning by regulating the flow of nutrients and energy over their mycelia networks; they act like natural ecosystem engineers (Lawton and Jones 1995; Tisma et al. 2010). White rot fungi perform a significant role in the process of mycoremediation (Dominguez et al. 2005; Casas et al. 2009; Wong 2009). White rot fungi produced nonspecific extracellular ligninolytic enzymes: laccase, lignin peroxidase (LiP) and manganese peroxidase (MnP) (Kitamura et al. 2005). These ligninolytic enzymes play an important role in the transformation and mineralization of various organic pollutants (Pointing 2001; Lee et al. 2004; Casas et al. 2009; Wang et al. 2009). The common white rot fungi used for the degradation of aromatic ring or pretreatment of lignin through ligninolytic enzymes are Phanerochaete chrysosporium, Pleurotus ostreatus, Trametes versicolor, Armillaria sp., and Bjerkandera adusta (Rigas et al. 2009; Balesteros et al. 2014; Kumar and Sharma 2017).
The objective of this study is to isolate polycyclic aromatic hydrocarbon-degrading white rot fungi G. lucidum from Chhattisgarh, India, identified by 18S rRNA sequencing and used for the analysis of phenanthrene and pyrene degradation on the basis of their ligninolytic activity. Degradation of phenanthrene and pyrene was estimated by HPLC and the ligninolytic enzyme production was quantified in phenanthrene- and pyrene-containing media.
Phenanthrene, pyrene, guaiacol, azure B, and 2,6-dimethoxy phenol (2,6-DMP) were purchased from Himedia, India. All other chemicals and solvents (ethyl acetate, acetonitrile) used were of analytical grade purchased from Himedia, India.
Microorganism and culture condition
A white rot fungi strain CCG1, found on the decayed wood surface, was collected from the Janjgir Champa district of (Latitude 21°58′13.9908ʺ, Longitude 82°28′30.9936ʺ and Elevation 258.7 m) Chhattisgarh, India, fungi were isolated from the fruiting body by the spore-drop method according to Choi et al. (1999). A piece of cap tissue was cut from the fruiting body and transferred in the top of a Petri dish containing sabouraud dextrose agar (SDA) media composition (g/L): dextrose (40), peptone (10), agar (15) and streptomycin (500 mg/L) antibiotic to inhibit the bacterial growth). After the pure culture was obtained, culture was maintained in SDA media and stored at 4 °C.
Ligninolytic enzyme production
To investigate the enzyme production, 8 mm of fungal mycelium disc was transferred in the 20 mL of mineral salt broth (composition g/L: glucose—10, KH2PO4—2, MgSO4·7H2O—0.5, CaCl2·2H2O—0.1, ammonium tartrate—0.2 and trace element solution—10 (mL) with 20 mg/L phenanthrene and 20 mg/L pyrene separately (0.2 µm membrane filter sterilized). A trace element solution comprised of (in mg/L) FeSO4·7H2O (12), MnSO4·7H2O (3), ZnSO4·7H2O (3), CoSO4·7H2O (1), (NH4)6Mo7O24·4H2O (1) (Hadibarata and Kristanti 2012). Then, incubate the culture at 27 °C in a rotatory shaker incubator for 2, 5, 10, 15, 20, 25 and 30 days. The ligninolytic enzyme activity was investigated in the presence of phenanthrene and pyrene separately. Control experiment (containing 20 mL of mineral salt broth with 20 mg/L phenanthrene and pyrene separately), was done at the same time when sample experiment was done. All the experiments were performed in triplicates.
The production of ligninolytic enzyme was investigated as the following procedure:
To investigate the laccase enzyme production, take 3 mL of reaction mixture containing 0.5 mL of the enzyme extract, 1.5 mL of sodium acetate buffer (10 mM, pH 5.0) and 1 mL of guaiacol (2 mM), then incubated for 2 h and absorbance read at 450 nm. The laccase enzyme activity has been expressed in international units per liter of enzyme extract (U/L) (Sandhu and Arora 1985).
Lignin peroxidase assay
For the lignin peroxidase enzyme production, take 0.5 mL of the culture filtrate, 1 mL of 125 mM sodium tartrate buffer (pH 3.0), 0.5 mL of 0.16 mM azure B, then add 0.5 mL of 2 mM hydrogen peroxide, after addition of hydrogen peroxide, reaction was initiated. One unit of enzyme activity was expressed as an O.D. decrease at 651 nm of 0.1 units per minute per liter of the culture filtrate (Archibald 1992).
Manganese peroxidase assay
According to de Jong et al. (1992) manganese peroxidase activity was accessed by the oxidation of 2,6-DMP at 468 nm. Take total 3 mL of reaction mixture containing 0.5 mL of culture filtrate, 1 mL of sodium tartrate buffer (50 mM, pH 4.0) and 1 mL of 2 mM 2,6-DMP. The reaction was started by the addition of 0.5 mL of 0.4 mM hydrogen peroxide.
Degradation of PAHs (phenanthrene and pyrene)
To investigate the phenanthrene and pyrene degradation mineral salt broth containing 20 mg/L phenanthrene and pyrene were taken separately. Then, 8 mm diameter, one culture mycelium disc was transferred in the broth media, control set containing mineral salt broth with phenanthrene and pyrene separately. Incubate the culture at 27 °C in a rotatory shaker incubator for 2, 5, 10, 15, 20, 30 days.
Extraction of degraded PAHs and analyzed by HPLC
Morphological and molecular characterization
Morphological observation of strain CCG1 was performed and molecular identification was conducted through 18S rRNA. 18S rRNA sequencing was carried out by the service provider Chromous Biotech Pvt. Ltd., Bangalore, India. They amplified the extracted DNA genome of the fungal strain CCG1 through polymerase chain reaction (PCR). The process of PCR amplification contains DNA template, primer (FP: GTAGTCATAKGCTNGTCTS, RP: GARACCTDGTTAVGACTY), taq DNA polymerase enzyme, dNTPs, buffer. PCR amplification was performed with following reactions: Started with 1st cycle at 94 °C for 5 min, 35 cycles at 940 °C for 30 s, 55 °C for 30 s, 72 °C for 2 min and ended with 1 cycle at 72 °C for 7 min. After that, sequencing reaction was performed using ABI 3500XL Genetic Analyzer sequencing machine. Later, closely related sequence was obtained from the National Center for Biotechnology Information (NCBI) database. Multiple alignments of all sequences were performed using CLUSTAL W. The neighbor-joining tree was constructed by Mega 7.0 software programs using bootstrapping at 1000 bootstraps (Tamura et al. 2007).
One-way ANOVA (analysis of variance) test was performed to analysis of the difference in ligninolytic enzyme production in the presence of phenanthrene and pyrene in mineral salt broth as compared to control; by applying Dunnett’s multiple comparison test with the help of statistical program Graph Pad Prism 7.
Results and discussion
Isolation and identification of collected fungal strain
Fungal strain CCG1 was collected from the hardwood stump of Janjgir Champa district of Chhattisgarh, India during the rainy season. A collected CCG1 fungus was isolated from their fruiting body. Further strain CCG1 was used for the PAHs degradation investigation on the basis of their ligninolytic enzyme activity (Agrawal et al. 2017).
Morphological and molecular characterization
On the basis of morphological and molecular characterization through 18S rRNA gene sequencing fungal strain CCG1 was identified as G. lucidum (Accession no. KY464926). A phylogenetic tree was created with the gene sequence of strain CCG1 and with their similar sequences of reference strain which are obtained from NCBI database. On the basis of phylogenetic tree (Fig. 1b) strain, CCG1 (Accession no. KY464926) was more similar with G. lucidum strain GI-16 (Accession no. FJ379279.1) and another 99% similar strains are Ganoderma australe strain Wu 9302-56 (Accession no. AY336763.1), Amauroderma sp. MUCL40278 (Accession no. AF255199.1), Lentinus sp. WR2 (Acccession No. GQ899200.1), Lentinus tigrinus (Accession no. AY946269.1), Hexagonia hirta strain Wu 9906-35 (Accession no. AY336759.1), Ganoderma tsugae isolate AFTOL-ID 771 (Accession no. AY705969.1), Ganoderma boninense (Accession no. AF255198.1), Coriolopsis byrsina strain CRM-46 (Accession no. AY336773.1), Earliella scabrosa strain Wu 9704-83 (Accession no. AY336766.1), Hexagonia hirta strain CBS 515.96 (Accession no. AY336760.1), Hexagonia pobeguinii strain CBS 510.96 (Accession no. AY336758.1), Ganoderma australe (Accession no. AF026629.1), Diplomitoporus crustulinus strain FP 101824 (Accession no. AY336770.1), Diplomitoporus lindbladii strain HHB 5629 (Accession no. AY336768.1), Microporus xanthopus strain Wu 9705-42 (Accession no. AY336756.1), Lignosus rhinocerus strain CH2 (Accession no. FJ899144.1), and Coriolopsis polyzona strain OH-184-SP (Accession no. AY336771.1).
Ligninolytic enzyme production
Ligninolytic enzyme production by G. lucidum during phenanthrene and pyrene degradation
Laccase activity (U/L)
LiP activity (U/L)
MnP activity (U/L)
28.43 ± 2.95
2106.00 ± 482.30***
1135.00 ± 18.09**
91.50 ± 5.2
109.30 ± 22.52ns
355.20 ± 96.7**
1005.00 ± 43.8
4614.00 ± 286.5****
8530.00 ± 131.90****
83.40 ± 6.9
3412.00 ± 88.52****
1020.00 ± 93.95****
105.30 ± 8.8
1608.00 ± 45.11****
2779.00 ± 111.00****
1093.00 ± 66.1
7052.00 ± 30.45****
6505.00 ± 234.50****
904.10 ± 48.48
9538.00 ± 74.32****
336.40 ± 16.88****
720.00 ± 65.21
2097.00 ± 103.8****
1552.00 ± 105.4****
1056.00 ± 43.66
47,444.00 ± 590****
2320.00 ± 110.70**
1154.00 ± 77.2
10,788.00 ± 535.20****
6915.00 ± 144.10****
1175.00 ± 45.46
3283.00 ± 100.2****
2484.00 ± 250.2***
15,035.00 ± 62.76
31,516.00 ± 368.9****
50,977.00 ± 663.20****
829.50 ± 21.91
3949.00 ± 57.26****
3416.00 ± 58.02****
852.60 ± 41.78
2995.00 ± 62.22****
2508.00 ± 267.2****
2137.00 ± 88.29
8237.00 ± 193.6****
7413.00 ± 268.20****
996.00 ± 50.58
7548.00 ± 392.60****
9122.00 ± 39.56****
653.9 ± 29.99
2906.00 ± 105.4****
3613.00 ± 137.6****
3391.00 ± 148.3
32,712.00 ± 1581.0****
31,856.00 ± 1606.00****
184.90 ± 9.95
6876.00 ± 373.10****
10,166.00 ± 222.30****
612.40 ± 10.95
1391.00 ± 234.3**
1564.00 ± 195.1**
3048.00 ± 82.79
30,593.00 ± 71.37****
25,209.00 ± 1632.00****
Degradation of phenanthrene
According to Bezalel et al. (1996), phenanthrene contains K-region and bay region in their structure. Phenanthrene was oxidized in K-region and formed 9,10-dihydroxy phenanthrene. Then, further the action of oxidation and ortho-ring cleavage reaction 2,2-diphenic acid was formed, and then it converted into phthalic acid and finally carbon dioxide (Bezalel et al. 1996, 1997; Hadibarata and Tachibana 2010). Hammel et al. (1992, 1995a) reported that the 2,2-diphenic acid produced by the action of MnP and LiP enzyme in Phanerochaete chrysosporium. Then, formed phthalic acid enters into basal metabolism pathway suggested by Pozdnyakova et al. (2010). According to Cerniglia et al. (1992) and Hammel (1995b) the characteristic feature of ligninolytic fungi is open and mineralize aromatic ring structure compounds.
Degradation of pyrene
As the pyrene degradation increases, the biomass and protein concentration of G. lucidum increases, maximum 257.00 mg biomass and 140.00 mg/L protein concentration were found in the pyrene-containing media (Fig. 3c).
Pyrene was oxidized at the 4,5 bond (K-region) and formed 4,5 dihydroxy pyrene in the ligninolytic condition, it may be converted from pyrene trans 4,5-dihydrodiol (Sack et al. 1997; Agrawal and Shahi 2017). Further, due to the oxidation process 4,5 dihydroxy pyrene converted into phenanthrene, phthalic acid and benzoic acid by the action laccase, LiP and MnP enzyme (Hadibarata and Kristanti 2013; Khudhair et al. 2015; Agrawal and Shahi 2017). According to Pozdnyakova et al. (2010) phthalic acid can be involved in basal metabolism. Bogan and Lamar (1996) and Field et al. (1992) also reported that laccase-producing fungi are capable to mineralize PAHs to CO2 and H2O.
PAHs are recalcitrant organic pollutants in the environment; their occurrence in the environment caused an adverse effect on the human and other animals. In this study, ligninolytic enzyme producing white rot fungi G. lucidum was used for the degradation of PAHs compound (phenanthrene and pyrene). G. lucidum degrade 99.65, 99.58% of phenanthrene and pyrene, respectively, in mineral salt broth. G. lucidum produced a significant amount of ligninolytic enzyme (p < 0.0001) in the presence of phenanthrene and pyrene containing media. Further, after successful pot and field trial G. lucidum strain CCG1 can be used as potent PAH degrader from the environment.
NA performed the research experiments and wrote the manuscript. PV helped in the experiments and manuscript writing. SKS guided both author during the experiments and manuscript preparation. All authors read and approved the final manuscript.
The authors are thankful to Mr. Anand Barapatre, post doc fellow, JNARDDC Campus, Nagpur for their support in the statistical analysis and to improve my research work. The authors are also thankful to Mr. Swaroop Biswas, JLA, CIF-PD Lab Bose Institute, Kolkata for HPLC analysis. The authors are thankful to Head, Department of Botany, Guru Ghasidas Vishwavidyalaya, providing infrastructural facilities. In addition, thanks to Guru Ghasidas Vishwavidyalaya, Bilaspur (C.G.) for providing financial assistance.
The authors declare that they have no competing interests.
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