Abstract
As an efficient method to remove contaminants from highly polluted sites, enzyme biodegradation addresses unresolved issues such as bioremediation inefficiency. In this study, the key enzymes involved in PAH degradation were brought together from different arctic strains for the biodegradation of highly contaminated soil. These enzymes were produced via a multi-culture of psychrophilic Pseudomonas and Rhodococcus strains. As a result of biosurfactant production, the removal of pyrene was sufficiently prompted by Alcanivorax borkumensis. The key enzymes (e.g., naphthalene dioxygenase, pyrene dioxygenase, catechol-2,3 dioxygenase, 1-hydroxy-2-naphthoate hydroxylase, protocatechuic acid 3,4-dioxygenase) obtained via multi-culture were characterized by tandem LC–MS/MS and kinetic studies. To simulate in situ application of produced enzyme solutions, pyrene- and dilbit-contaminated soil was bioremediated in soil columns and flask tests by injecting enzyme cocktails from the most promising consortia. The enzyme cocktail contained about 35.2 U/mg protein pyrene dioxygenase, 61.4 U/mg protein naphthalene dioxygenase, 56.5 U/mg protein catechol-2,3-dioxygenase, 6.1 U/mg protein 1-hydroxy-2-naphthoate hydroxylase, and 33.5 U/mg protein protocatechuic acid (P3,4D) 3,4-dioxygenase enzymes. It was found that after 6 weeks, the average pyrene removal values showed that the enzyme solution could be effective in the soil column system (80–85% degradation of pyrene).
Similar content being viewed by others
Data availability
Data are available upon reasonable request.
References
American Society for Testing and Materials (2007) Standard test method for particle size analysis of soils. ASTM D422-63. ASTM, West Conshohocken, PA
Ausuri J, Vitale GA, Coppola D, Palma Esposito F, Buonocore C, de Pascale D (2021) Assessment of the degradation potential and genomic insights towards phenanthrene by Dietzia psychralcaliphila JI1D. Microorganisms 9:1327
Barkay T, Navon-Venezia S, Ron E, Rosenberg E (1999) Enhancement of solubilization and biodegradation of polyaromatic hydrocarbons by the bioemulsifier alasan. Appl Environ Microbiol 65:2697–2702
Bouchez M, Blanchet D, Bardin V, Haeseler F, Vandecasteele J-P (1999) Efficiency of defined strains and of soil consortia in the biodegradation of polycyclic aromatic hydrocarbon (PAH) mixtures. Biodegradation 10:429–435
Butler JD, Parkerton TF, Letinski DJ, Bragin GE, Lampi MA, Cooper KR (2013) A novel passive dosing system for determining the toxicity of phenanthrene to early life stages of zebrafish. Sci Total Environ 463:952–958
Catterall F, Williams P (1971) Some properties of the naphthalene oxygenase from Pseudomonas sp. NCIB 9816. Microbiology 67:117–124
Davoodi SM, Taheran M, Brar SK, Galvez-Cloutier R, Martel R (2019) Hydrophobic dolomite sorbent for oil spill clean-ups: kinetic modeling and isotherm study. Fuel 251:57–72
El Fantroussi S, Agathos SN (2005) Is bioaugmentation a feasible strategy for pollutant removal and site remediation? Curr Opin Microbiol 8:268–275
Heitkamp MA, Freeman JP, Miller DW, Cerniglia C (1988) Pyrene degradation by a Mycobacterium sp.: identification of ring oxidation and ring fission products. Appl Environ Microbiol 54:2556–2565
Jardine J, Stoychev S, Mavumengwana V, Ubomba-Jaswa E (2018) Screening of potential bioremediation enzymes from hot spring bacteria using conventional plate assays and liquid chromatography-tandem mass spectrometry (LC-MS/MS). J Environ Manage 223:787–796
Kadri T, Rouissi T, Magdouli S, Brar SK, Hegde K, Khiari Z, Daghrir R, Lauzon J-M (2018) Production and characterization of novel hydrocarbon degrading enzymes from Alcanivorax borkumensis. Int J Biol Macromol 112:230–240
Krishnan S, Prabhu Y, Phale PS (2004) o-Phthalic acid, a dead-end product in one of the two pathways of phenanthrene degradation in Pseudomonas sp. strain PP2
Kumar P, Rubio HDP, Hegde K, Brar SK, Cledon M, Kermanshahi-Pour A, Sauvé S, Roy-Lachapelle A, Galvez-Cloutier R (2019) Agro-industrial residues as a unique support in a sand filter to enhance the bioactivity to remove microcystin-leucine arginine and organics. Sci Total Environ 670:971–981
Kumar P, Pérez JAE, Cledon M, Brar SK, Duy SV, Sauvé S, Knystautas É (2020) Removal of microcystin-LR and other water pollutants using sand coated with bio-optimized carbon submicron particles: graphene oxide and reduced graphene oxide. Chem Eng J 397:125398
Li Z, Cabana H, Lecka J, Brar SK, Galvez R, Bellenger J-P (2021) Efficiencies of selected biotreatments for the remediation of PAH in diluted bitumen contaminated soil microcosms. Biodegradation 32:563–576
Marques M, Hogland W (2003) Hydrological performance of MSW incineration residues and MSW co-disposed with sludge in full-scale cells. Waste Manage 23:469–481
Miri S, Naghdi M, Rouissi T, Kaur Brar S, Martel R (2019) Recent biotechnological advances in petroleum hydrocarbons degradation under cold climate conditions: a review. Crit Rev Environ Sci Technol 49:553–586
Miri S, Davoodi SM, Brar SK, Rouissi T, Sheng Y, Martel R (2021) Psychrozymes as novel tools to biodegrade p-xylene and potential use for contaminated groundwater in the cold climate. Biores Technol 321:124464
Miri S, Davoodi SM, Robert T, Brar SK, Martel R, Rouissi T (2022a) Enzymatic biodegradation of highly p-xylene contaminated soil using cold-active enzymes: a soil column study. J Hazard Mater 423:127099
Miri S, Ravula A, Akhtarian S, Brar SK, Martel R, Rouissi T (2022) Immobilized Cold-Active Enzymes onto Magnetic Chitosan Microparticles as a Highly Stable and Reusable Carrier for p-xylene Biodegradation in Soil
Olu-Owolabi BI, Diagboya PN, Adebowale KO (2014) Evaluation of pyrene sorption–desorption on tropical soils. J Environ Manage 137:1–9
Peng RH, Xiong AS, Xue Y, Fu XY, Gao F, Zhao W, Tian YS, Yao QH (2008) Microbial biodegradation of polyaromatic hydrocarbons. FEMS Microbiol Rev 32:927–955
Penning TM, Burczynski ME, Hung CF, McCoull KD, Palackal NT, Tsuruda LS (1999) Dihydrodiol dehydrogenases and polycyclic aromatic hydrocarbon activation: generation of reactive and redox active o-quinones. Chem Res Toxicol 12(1):1–18
Quesada E, Bejar V, Valderrama MJ, Ramos-Cormenzana A (1987) Growth characteristics and salt requirement of Deleya halophila in a defined medium. Curr Microbiol 16:21–25
Robert T, Martel R, Lefebvre R, Lauzon J-M, Morin A (2017) Impact of heterogeneous properties of soil and LNAPL on surfactant-enhanced capillary desaturation. J Contam Hydrol 204:57–65
Rowbotham T, Cross T (1977) Ecology of Rhodococcus coprophilus and associated actinomycetes in fresh water and agricultural habitats. Microbiology 100:231–240
Sadalage PS, Dar MA, Chavan AR, Pawar KD (2020) Formulation of synthetic bacterial consortia and their evaluation by principal component analysis for lignocellulose rich biomass degradation. Renew Energy 148:467–477
Shaw JP, Harayama S (1995) Characterization in vitro of the hydroxylase component of xylene monooxygenase, the first enzyme of the TOL-plasmid-encoded pathway for the mineralization of toluene and xylenes. J Ferment Bioeng 79:195–199
Smith KE, Oostingh GJ, Mayer P (2010) Passive dosing for producing defined and constant exposure of hydrophobic organic compounds during in vitro toxicity tests. Chem Res Toxicol 23:55–65
Thompson IP, Van Der Gast CJ, Ciric L, Singer AC (2005) Bioaugmentation for bioremediation: the challenge of strain selection. Environ Microbiol 7:909–915
Tomás-Gallardo L, Canosa I, Santero E, Camafeita E, Calvo E, López JA, Floriano B (2006) Proteomic and transcriptional characterization of aromatic degradation pathways in Rhodoccocus sp. strain TFB. Proteomics 6:S119–S132
Voth W, Jakob U (2017) Stress-activated chaperones: a first line of defense. Trends Biochem Sci 42:899–913
Walter U, Beyer M, Klein J, Rehm H-J (1991) Degradation of pyrene by Rhodococcus sp. UW1. Appl Microbiol Biotechnol 34:671–676
Weber WJ Jr, McGinley PM, Katz LE (1992) A distributed reactivity model for sorption by soils and sediments. 1. Conceptual basis and equilibrium assessments. Environ Sci Technol 26:1955–1962
Whelan M, Coulon F, Hince G, Rayner J, McWatters R, Spedding T, Snape I (2015) Fate and transport of petroleum hydrocarbons in engineered biopiles in polar regions. Chemosphere 131:232–240
Wojcieszyńska D, Hupert-Kocurek K, Jankowska A, Guzik U (2012) Properties of catechol 2, 3-dioxygenase from crude extract of Stenotrophomonas maltophilia strain KB2 immobilized in calcium alginate hydrogels. Biochem Eng J 66:1–7
Wu X (2003) Investigating the stability mechanism of water-in-diluted bitumen emulsions through isolation and characterization of the stabilizing materials at the interface. Energy Fuels 17:179–190
Xu R, Zhou Q, Li F, Zhang B (2013) Laccase immobilization on chitosan/poly (vinyl alcohol) composite nanofibrous membranes for 2, 4-dichlorophenol removal. Chem Eng J 222:321–329
Zhao B, Wang H, Mao X, Li R (2009) Biodegradation of phenanthrene by a halophilic bacterial consortium under aerobic conditions. Curr Microbiol 58:205–210
Acknowledgements
Support from the James and Joanne Love Chair in Environmental Engineering is equally appreciated.
Funding
This work received financial support from the Natural Sciences and Engineering Research Council of Canada (No. 284111, Discovery; No. 476649–14, Strategic Research Grant). Love Chair in Environmental Engineering at York University, Institute National de la Recherche Scientifique-Eau Terre Environnement, and Laval University have been acknowledged.
Author information
Authors and Affiliations
Contributions
Study conception and design and acquisition of data: SMD.
Analysis and interpretation of the data: SM.
Drafting of the manuscript: RM.
Critical revision: SKB.
All authors approved the final version to be submitted.
Corresponding author
Ethics declarations
Ethics approval
Not applicable.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Additional information
Responsible Editor: Robert Duran
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Davoodi, S.M., Miri, S., Brar, S.K. et al. Formulation of synthetic bacteria consortia for enzymatic biodegradation of polyaromatic hydrocarbons contaminated soil: soil column study. Environ Sci Pollut Res 30, 72793–72806 (2023). https://doi.org/10.1007/s11356-023-27233-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-023-27233-5