Short communicationContrasting characteristics of anthracene and pyrene degradation by wood rot fungus Pycnoporus sanguineus H1
Graphical abstract
Introduction
Polycyclic aromatic hydrocarbons (PAHs) are a group of organic compounds with two or more fused benzene rings which have been identified as serious, persistent organic pollutants. The US Environmental Protection Agency (USEPA) has listed 16 PAHs as priority pollutants (Wu et al., 2010), including anthracene and pyrene. High molecular weight PAHs (HMW PAHs), such as benz[a]anthracene (BAA, four rings), benzo[a]pyrene (five rings), and dibenz[a,h]anthracene (five rings) feature the same basic structure of anthracene while exhibiting greater recalcitrant characteristics in the environment, greater toxicity, and more severe carcinogenic effects to humans than low molecular weight PAHs (LMW PAHs) (Giraud et al., 2001). Pyrene, a typical four-ring HMW PAH, exhibits teratogenicity and carcinogenicity producing mutagenicity (Wen et al., 2011). For these reasons, biodegradation studies on PAHs typically consider anthracene and pyrene to be model compounds.
Both bacteria and fungi are able to degrade PAHs (Bamforth and Singleton, 2005, Machín-Ramírez et al., 2010). Among these microorganisms, wood rot fungi are considered the most effective PAH degraders (Chupungars et al., 2009, Asgher et al., 2008), thus attracting increased attention from researchers and developers (Pointing, 2001). The most notable advantage of wood rot fungi is their secretion of extracellular ligninolytic enzymes that can extracellularly degrade substrates. Generally, these enzymes oxidize PAHs via a non-specific, radical-based reaction with corresponding quinones (Bamforth and Singleton, 2005). To date, three enzymes: lignin peroxidase (LiP), manganese peroxidase (MnP), and laccase, have been reported to successfully catalyze PAH oxidation (Bezalel et al., 1996, Baldrian et al., 2000, Singh and Pakshirajan, 2010). Prior research conducted in our laboratory confirmed that extracellular ligninolytic enzymes of the wood rot fungus Pycnoporus sanguineus, which contains mostly laccase, can convert anthracene to anthraquinone effectively (Li et al., 2014).
In recent years, studies have suggested that cytochrome P450 monooxygenase from wood rot fungi might be involved in the initial oxidation of PAHs (Chigu et al., 2010, Ning et al., 2010). Cytochrome P450 monooxygenases, a superfamily of monooxygenases (Chigu et al., 2010), are commonly present in living organisms. The detoxification of xenobiotics is an example of several P450-dependent reactions accomplishing a series of secondary metabolic processes. This information implies that PAHs can potentially be transformed by wood rot fungi through simultaneous intracellular and extracellular pathways, which makes their metabolic process very interesting.
In this study, anthracene and pyrene were employed as PAH models. Both in vivo and in vitro conversion experiments were performed to evaluate PAH degradation potential according to different fractions of P. sanguineus. The primary goals of the experiment were to characterize the involvement of particular enzymes in PAH degradation, including ligninolytic enzymes and intracellular fraction enzymes, and to explore the possible involvement of cytochrome P-450 and mycelium-associated laccase.
Section snippets
Microorganisms, chemicals, and media
Fungus, P. sanguineus H1, was supplied by Nanjing Forestry University, China. Anthracene, pyrene, piperonyl butoxide, and 2,2′-azinobis(3-ethylbenzthiazoline-6-sulfonate) (ABTS) were purchased from Sigma (St. Louis, MO, USA). All solvents used were of HPLC grade. All other chemicals and reagents used were of analytical reagent grade or higher purity.
The medium used (pH4.5) included the following: glucose 5.0 g L−1, bran 5.0 g L−1, KH2PO4 0.2 g L−1, MgSO4 0.05 g L−1, (NH4)2SO4 0.32 g L−1, CaCl2
In vivo PAH degradation by fungus
The ability of P. sanguineus H1 to degrade PAHs was evaluated in liquid culture, both with and without PB. During incubation, ligninolytic enzyme activities were assayed, but no obvious LiP or MnP activities were detected. Results indicated that the anthracene degradation capacity of this strain is quite considerable, where significant anthracene degradation occurred between 4 and 10 incubation days (Fig. 1). After 14 d of incubation, 67.5% of the total anthracene was removed. In this case, the
Acknowledgments
The work was financial supported by grants from the National Natural Science Foundation of China (41401350), Key Laboratory of Soil Environment and Pollution Remediation, Institute of Soil Science, Chinese Academy of Sciences (SEPR2014-05) and Key Scientific Research Projects of Colleges and Universities of Henan Province.
References (25)
- et al.
Laccase mediated decolorization of vat dyes by Coriolus versicolor IBL-04
Int. Biodeterior. Biodegrad.
(2008) - et al.
Polycyclic aromatic hydrocarbons degradation by Agrocybe sp CU-43 and its fluorene transformation
Int. Biodeterior. Biodegrad.
(2009) - et al.
Biodegradation of anthracene and fluoranthene by fungi isolated from an experimental constructed wetland for wastewater treatment
Water Res.
(2001) - et al.
Dissipation of polycyclic aromatic hydrocarbons (PAHs) in soil microcosms amended with mushroom cultivation substrate
Soil Biol. Biochem.
(2012) - et al.
Benzo[a]pyrene removal by axenic- and co-cultures of some bacterial and fungal
Int. Biodeterior. Biodegrad.
(2010) - et al.
Enzyme activities and decolourization of single and mixed azo dyes by the white-rot fungus Phanerochaete chrysosporium
Int. Biodeterior. Biodegrad.
(2010) - et al.
Implication of mycelium-associated laccase from Irpex lacteus in the decolorization of synthetic dyes
Bioresour. Technol.
(2008) - et al.
Genome-to-function characterization of novel fungal P450 monooxygenases oxidizing polycyclic aromatic hydrocarbons (PAHs)
Biochem. Biophys. Res. Commun.
(2010) - et al.
Biodegradation of phenanthrene and pyrene by Ganoderma lucidum
Int. Biodeterior. Biodegrad.
(2011) - et al.
Potential use of oxidative enzymes for the detoxification of organic pollutants
Appl. Catal. B Environ.
(2003)
Preliminary evidence of the role of hydrogen peroxide in the degradation of benzo a pyrene by a non-white rot fungus Fusarium solani
Environ. Pollut. Barking Essex 1987
Co-metabolic degradation of pyrene by indigenous white-rot fungus Pseudotrametes gibbosa from the northeast China
Int. Biodeterior. Biodegrad.
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