The aim of this study was to evaluate application of a crude enzymatic extract from the mixed culture of Trametes maxima (T. maxima) and Paecilomyces carneus (P. carneus) in removal of phenanthrene (PHE) from water. Since PHE belong to the polycyclic aromatic hydrocarbons (PAHs), it has been used as a model compound for bioremediation treatments. PAHs are highly stable molecules, and are resistant to conventional wastewater treatment. Production of crude extract from a mixed culture of T. maxima and P. carneus does not require special conditions yet the use of 20 g/L of glycerol as carbon source enhances laccase (Lcc) and manganese-dependent peroxidase (MnP) activities. Application of crude extracts becomes feasible because it does not require further purification. The crude enzymes entrapped in alginate beads in a fixed-bed packed column reached 94.3% ± 0.7% of PHE removal after 13 h of continuous treatment under nonsterile conditions, while the alginate beads without enzymes reached only 45.3% ± 23% of PHE removal. The difference between the removal of alginate beads with and without enzymes was the oxidative activity on the surface of the alginate beads, which was observed in the increase in the C═O group and in the X-ray spectroscopy analyses of the C 1s and O 1s regions. Beads without enzymes had less C═O groups. Polyoxyethylene sorbitan monooleate and dimethyl sulfoxide also influence enzymatic activity to carry out a level of PHE removal similar to a photocatalytic treatment.
Get full access to this article
View all access options for this article.
References
1.
AdenijiA.O., OkohO.O., and OkohA.I. (2017). Analytical methods for the determination of the distribution of total petroleum hydrocarbons in the water and sediment of aquatic systems: A review. J. Chem., 2017, 1.
2.
AsgherM., ShahidM., KamalS., and IqbalH.M.N. (2014). Recent trends and valorization of immobilization strategies and ligninolytic enzymes by industrial biotechnology. J. Mol. Catal. B Enzym. 101, 56.
3.
BhushanB., PalA., and JainV. (2015). Improved enzyme catalytic characteristics upon glutaraldehyde cross-linking of alginate entrapped xylanase isolated from Aspergillus flavus MTCC 9390. Enzyme Res. 2015, 1.
4.
BöhmerS., MessnerK., and SrebotnikE. (1998). Oxidation of phenanthrene by a fungal laccase in the presence of 1-hydroxybenotriazole and unsaturated lipids. Biochem. Biophys. Res. Commun., 244, 233.
5.
BorgognaM., Skjåk-BrækG., PaolettiS., and DonatiI. (2013). On the initial binding of alginate by calcium ions. The tilted egg-box hypothesis. J. Phys. Chem. B, 117, 7277.
6.
BuggT.H.D. (2014). How to break the rules of Dioxygen Activation. Chem. Biol., 21, 168.
7.
CantarellaG., GalliC., and GentiliP. (2003). Free radical versus electron-transfer routes of oxidation of hydrocarbons by laccase/mediator systems Catalytic or stoichiometric procedures. J. Mol. Catal. B Enzym., 22, 135.
8.
EibesG., CajthamlT., MoreiraM.T., GumersindoF., and LemaJ.M. (2006). Enzymatic degradation of anthracene, dibenzothiophene and pyrene by manganese peroxidase in media containing acetone. Chemosphere, 64, 408.
9.
ElisashviliV., and KachlishviliE. (2009). Physiological regulation of laccase and manganese peroxidase production by white-rot Basidiomycetes. J Biotechnol. 144, 37.
10.
FeiY., LiY., HanS., and MaJ. (2016). Adsorptive removal of ciprofloxacin by sodium alginate/graphene oxide composite beads from aqueous solution. J. Colloid Interface Sci., 484, 196.
11.
Fernández-GonzálezR., Yebra-PimentelI., Martínez-CarballoE., Simal-GándaraJ., and Pontevedra-PombalX. (2014). Atmospheric pollutants in fog and rain events at the northwestern mountains of the Iberian Peninsula. Sci. Total Environ. 497–498, 188.
12.
Garcia-MoralesR., Rodríguez-DelgadoM., Gomez-MariscalK., Orona-NavarC., Hernandez-LunaC., TorresE., ParraR., Cárdenaz-ChavezD., MahlknechtJ., and Ornelas-SotoN. (2015). Biotransformation of endocrine-disrupting compounds in groundwater: Bisphenol A, nonylphenol, ethynylestradiol and triclosan by a laccase cocktail from Pycnoporus sanguineus CS43. Water Air Soil Pollut. 226, 1.
13.
GombotzW.R., and WeeS.F. (2012). Protein release from alginate matrices. Adv. Drug Deliv. Rev., 64, 194.
14.
González-RamírezD.F., Ávila-PérezP., Torres-BustillosL.G., Aguilar-LópezR., Montes-HorcasitasM.C., Esparza-GarcíaF.J., and Rodríguez-VázquezR. (2017). Removal of phenanthrene in aqueous solution containing photon competitors by TiO2-C-Ag film supported on fiberglass. J. Environ. Sci. Health A., 52, 742.
15.
GreczynskiG., and HultmanL. (2017). C 1s peak of adventitious carbon aligns to the vacuum level: Dire consequences for material's bonding assignment by photoelectron spectroscopy. ChemPhysChem. 18, 1507.
16.
HaileiW., GuangliY., PingL., YanchangG., JunL., GuoshengL., and JianmingY. (2009). Overproduction of Trametes versicolor laccase by making glucose starvation using yeast. Enzyme Microb. Technol., 45, 146.
17.
HammelK.E., GaiW.Z., GreenB., and MoenM.A. (1992). Oxidative degradation of phenanthrene by the ligninolytic fungus Phanerochete chrysosporium. Appl. Environ. Microbiol., 58, 1832.
18.
HanM.J., ChoiH.T., and SongH.G. (2004). Degradation of phenanthrene by Trametes versicolor and its laccase. J. Microbiol., 42, 94.
19.
Harris-ValleC., EsquedaM., SánchezA., Beltrán-GarcíaM., and Valenzuela-SotoE.M. (2007). Polar vineyard pruning extracts increase the activity of the main ligninolytic enzymes in Lentinula edodes cultures. Can. J. Microbiol., 53, 1150.
20.
JiL., YangJ., FanH., YangY., LiB., YuX., ZhuN., and YuanH. (2014). Synergy of crude enzyme cocktail from cold-adapted Cladosporium cladosporioides Ch2-2 with commercial xylanase achieving high sugars yield at low cost. Biotechnol. Biofuels., 7, 130.
21.
LeT.T., MurugesanK., LeeC.S., VuC.H., ChangY.S., and JeonJ.R. (2016). Degradation of synthetic pollutants in real wastewater using laccase encapsulated in core-shell magnetic copper alginate beads. Bioresour. Technol., 216, 203.
22.
LeeA.H., KangC.M., LeeY.M., LeeH., YunC.W., KimG.H., and KimJ.J. (2016). Heterologous expression of a new manganese-dependent peroxidase gene from Peniophora incarnata KUC8836 and its ability to remove anthracene in Saccharomyces cerevisiae. J. Biosci. Bioeng., 122, 716.
23.
LeeH., JangY., ChoiY.S., KimM.J., LeeJ., LeeH., HoungJ.H., LeeY.M., KimG.H., and KimJ.J. (2014). Biotechnological procedures to select white rot fungi for the degradation of PAHs. J. Microbiol. Methods., 97, 56.
24.
LiP., WangH., LiuG., LiX., and YaoJ. (2011). The effect of carbon source succession on laccase activity in the co-culture process of Ganoderma lucidum and a yeast. Enzyme Microb. Technol., 48, 1.
25.
LigarayM., BaekS.S., KwonH.O., ChoiS.D., and ChoK.H. (2016). Watershed-scale modeling on the fate and transport of polycyclic aromatic hydrocarbons (PAHs). J. Hazard. Mater. 320, 442.
26.
ManavalanT., ManavalanA., and HeeseK. (2014). Characterization of lignocellulolytic enzymes from white-rot fungi. Curr. Microbiol., 70, 485.
27.
McArthurS.L., MishraG., and EastonC.D. (2014). Applications of XPS in biology and biointerface analysis. In: SmentkowskiV (ed). Surface Analysis and Techniques in Biology. Switzerland: Springer International Publishing, p. 29.
28.
MinussiR.C., de MoraesS.G., PastoreG.M., and DuranN. (2001). Biodecolorization screening of synthetic dyes by four white-rot fungi in a solid medium: Possible role of siderophores. Lett. Appl. Microbiol., 33, 21.
29.
MoenM. A., and HammelE. (1994). Lipid peroxidation by the manganese peroxidase of Phanerochete chrysosporium is the basis for phenanthrene oxidation by the intact fungus. Appl. Environ. Microbiol., 60, 1956.
30.
MogharabiM., and FaramarziM. A. (2014). Laccase and laccase-mediated systems in the synthesis of organic compounds. Adv. Synth. Catal., 356, 897.
31.
National Institute of Standards and Technology (NIST). (2012). X-ray Photoelectron Spectroscopy Database Version 4.1. Gaithersburg: National Institute of Standards and Technology, 2012. Available at: http://srdata.nist.gov/xps (accessed August15, 2017).
32.
NetzkerT., FischerJ., WeberJ., MatternD.J., KönigC.C., ValianteV., SchroeckhV., and BrakhageA.A. (2015). Microbial communication leading to the activation of silent fungal secondary metabolite gene clusters. Front. Microbiol., 6, 299.
33.
OllerI., MalatoS., and Sánchez-PérezA. (2011). Combination of advanced oxidation process and biological treatments for wastewater decontamination—A review. Sci. Total Environ., 409, 4141.
34.
PalmieriG., GiardinaP., DesiderioB., MarzulloL., GiamberiniM., and SanniaG. (1994). A new enzyme immobilization procedure using copper alginate gel: Application to a fungal phenol oxidase. Enzyme Microb. Technol., 16, 151.
35.
RaoM.A., ScelzaR., AcevedoF., DiezM.C., and GianfredaL. (2014). Enzymes as useful tools for environmental purposes. Chemosphere, 107, 145.
36.
RevankarM.S., and LeleS.S. (2007). Synthetic dye decolorization by white rot fungus Ganoderma sp. WR-1. Bioresour. Technol., 98, 775.
37.
SackU., HofrichterM., and FritscheW. (1997). Degradation of polycyclic aromatic hydrocarbons by manganese peroxidase of Nematoloma frowardii. FEMS Microbiol. Lett., 152, 227.
38.
ScadutoR.C. (1995). Oxidation of DMSO and methanesulfinic acid by the hydroxyl radical. Free Radic. Biol. Med., 18, 271.
39.
ShenT., PiY., BaoM., XuN., LiY., and LuJ. (2015). Biodegradation of different petroleum hydrocarbons by free and immobilized microbial consortia. Environ. Sci. Process Impacts., 17, 2022.
40.
SoiB., and SteinerR.A. (2016). New insight into cofactor-free oxygenation from combined experimental and computational approached. Curr. Opin. Struct. Biol., 41, 109.
41.
SolomonE.I., ChenP., MetzM., LeeS.K., and PalmerA.E. (2001). Oxygen binding, activation, and reduction to water by copper proteins, Angew. Chem. Int. Ed., 40, 4070.
42.
SutherlandJ.B., SelbyA.L., FreemanJ.P., EvansF.E., and CernigliaC.E. (1991). Metabolism of phenanthrene by Phanerochete chrysosporium. Appl. Environ. Microbiol., 57, 3310.
43.
TorrettaV. (2012). PAHs in wastewater: Removal efficiency in a conventional wastewater treatment plant and comparison with model predictions. Environ. Technol., 33, 851.
44.
WangB., YanY., TianY., ZhaoW., LiZ., GaoJ., PengR., and YaoQ. (2016). Heterologous expression and characterization of a laccase from Colletotrichum lagenarium and decolourisation of different synthetic dyes. World J. Microbiol. Biotechnol., 32, 40.
45.
WatanabeT., KatayamaS., EnokioM., HondaY., and KuwaharaM. (2000). Formation of acyl radical in lipid peroxidation of linoleic acid by manganese-dependent peroxidase from Ceriporiopsis subvermispora and Bjerkandera adusta. Eur. J. Biochem., 267, 4222.
46.
WeiF., HongY., LiuJ., YuanJ., FangW., PengH., and XiaoY. (2010). Gongronella sp. induces overproduction of laccase in Panus rudis. J. Basic Microbiol., 50, 98.
47.
WolfendenB.S., and WillsonR.L. (1982). Radical-cations as reference chromogens in kinetic studies of one-electron transfer reactions: Pulse radiolysis studies of 2,2′-azinobis-(3-ethylbenzthiazoline-6-sulphonate). J. Chem. Soc. Perkin Trans., 2, 805.
