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Genomic and transcriptomic perspectives on mycoremediation of polycyclic aromatic hydrocarbons

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Abstract

Mycoremediation holds great potential in remedying toxic environments contaminated with polyaromatic organic pollutants. To harness the natural process for practical applications, understanding the genetic and molecular basis of the remediation process is prerequisite. Compared to known bacterial degradation pathways of aromatic pollutants, however, the fungal degradation system is less studied and understanding of the genetic basis for biochemical activity is still incomplete. In this review, we surveyed recent findings from genomic and transcriptomic approaches to mycoremediation of aromatic pollutants, in company with the genomic basis of polycyclic aromatic hydrocarbon (PAH) degradation by basidiomycete fungi, Dentipellis sp. KUC8613. Unique features in the fungal degradation of PAHs were outlined by multiple cellular processes: (i) the initial oxidation of recalcitrant contaminants by various oxidoreductases including mono- and dioxygenases, (ii) the following detoxification, and (iii) the mineralization of activated pollutants that are common metabolism in many fungi. Along with the genomic data, the transcriptomic analysis not only posits a full repertoire of inducible genes that are common or specific to metabolize different PAHs but also leads to the discovery of uncharacterized genes with potential functions for bioremediation processes. In addition, the metagenomic study accesses community level of mycoremediation process to seek for the potential species or a microbial consortium in the natural environments. The comprehensive understanding of fungal degradation in multiple levels will accelerate practical application of mycoremediation.

Key points

• Mycoremediation of polyaromatic pollutants exploits a potent fungal degrader.

• Fungal genomics provides a full repository of potential genes and enzymes.

• Mycoremediation is a concerted cellular process involved with many novel genes.

• Multi-omics approach enables the genome-scale reconstruction of remedying pathways.

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References

  • Abdel-Hamid AM, Solbiati JO, Cann IK (2013) Insights into lignin degradation and its potential industrial applications. In: Advances in applied microbiology. Academic Press, 1–28

  • Abdel-Shafy HI, Mansour MS (2016) A review on polycyclic aromatic hydrocarbons: source, environmental impact, effect on human health and remediation. Egypt J 25:107–123

    Google Scholar 

  • Acevedo F, Pizzul L, Castillo MP, Cuevas R, Diez MC (2011) Degradation of polycyclic aromatic hydrocarbons by the Chilean white-rot fungus Anthracophyllum discolor. J Hazard Mater 185:212–219

    Article  CAS  PubMed  Google Scholar 

  • Aitken MD, Venkatadri R, Irvine RL (1989) Oxidation of phenolic pollutants by a lignin degrading enzyme from the white-rot fungus Phanerochaete chrysosporium. Water Res 23:443–450

    Article  CAS  Google Scholar 

  • Alberts JF, Gelderblom WC, Botha A, van Zyl WH (2009) Degradation of aflatoxin B(1) by fungal laccase enzymes. Int J Food Microbiol 135:47–52

    Article  CAS  PubMed  Google Scholar 

  • Almagro Armenteros JJ, Sønderby CK, Sønderby SK, Nielsen H, Winther O (2017) DeepLoc: prediction of protein subcellular localization using deep learning. Bioinformatics 33:3387–3395

    Article  PubMed  CAS  Google Scholar 

  • Aranda E (2016) Promising approaches towards biotransformation of polycyclic aromatic hydrocarbons with Ascomycota fungi. Curr Opin Biotech 38:1–8

    Article  CAS  PubMed  Google Scholar 

  • Ashikawa Y, Fujimoto Z, Usami Y, Inoue K, Noguchi H, Yamane H, Nojiri H (2012) Structural insight into the substrate-and dioxygen-binding manner in the catalytic cycle of Rieske nonheme iron oxygenase system, carbazole 1, 9a-dioxygenase. BMC Struc Biol 12:15

    Article  CAS  Google Scholar 

  • Assress HA, Selvarajan R, Nyoni H, Ntushelo K, Mamba BB, Msagati TA (2019) Diversity, co-occurrence and implications of fungal communities in wastewater treatment plants. Sci Rep 9:1–15

    Article  CAS  Google Scholar 

  • Bezalel LEA, Hadar Y, Fu PP, Freeman JP, Cerniglia CE (1996) Metabolism of phenanthrene by the white rot fungus Pleurotus ostreatus. Appl Environ Microbiol 62:2547–2553

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bezalel L, Hadar Y, Cerniglia CE (1997) Enzymatic mechanisms involved in phenanthrene degradation by the white rot fungus Pleurotus ostreatus. Appl Environ Microbiol 63:2495–2501

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bhattacharya SS, Yadav JS (2018) Microbial P450 enzymes in bioremediation and drug discovery: emerging potentials and challenges. Curr Protein Pept Sc 19:75–86

    CAS  Google Scholar 

  • Blasi B, Tafer H, Kustor C, Poyntner C, Lopandic K (2017) Genomic and transcriptomic analysis of the toluene degrading black yeast Cladophialophora immunda. Sci Rep 7(1):1–13

    Article  CAS  Google Scholar 

  • Cerniglia CE, Sutherland JB (2010) Degradation of polycyclic aromatic hydrocarbons by fungi. In: Handbook of hydrocarbon and lipid microbiology

  • Chivukula M, Renganathan V (1995) Phenolic Azo dye oxidation by laccase from Pyricularia oryzae. Appl Environ Microbiol 61:4374–4377

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clemente AR, Anazawa TA, Durrant LR (2001) Biodegradation of polycyclic aromatic hydrocarbons by soil fungi. Braz J Microbiol 32:255–261

    Article  CAS  Google Scholar 

  • da Silva C-MJ, Maciel GM, Castoldi R, da Silva Mariano S, Inácio FD, Bracht A, Peralta RM (2013) Involvement of lignin-modifying enzymes in the degradation of herbicides In: Herbicides-advances in research

  • De Filippis F, Laiola M, Blaiotta G, Ercolini D (2017) Different amplicon targets for sequencing-based studies of fungal diversity. Appl Environ Microbiol 83:e00905–e00917

    Article  PubMed  PubMed Central  Google Scholar 

  • Deshmukh R, Khardenavis AA, Purohit HJ (2016) Diverse metabolic capacities of fungi for bioremediation. Indian J Microbiol 56:247–264

  • Durairaj P, Hur J-S, Yun H (2016) Versatile biocatalysis of fungal cytochrome P450 monooxygenases. Microb Cell Factories 15:125

    Article  CAS  Google Scholar 

  • El Amrani A, Dumas AS, Wick LY, Yergeau E, Berthomé R (2015) “Omics” insights into PAH degradation toward improved green remediation biotechnologies. Environ Sci Technol 49(19):11281–11291

    Article  PubMed  CAS  Google Scholar 

  • Escobar-Zepeda A, Vera-Ponce de Leon A, Sanchez-Flores A (2015) The road to metagenomics: from microbiology to DNA sequencing technologies and bioinformatics. Front Genet 6:348

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ezezika OC, Singer PA (2010) Genetically engineered oil-eating microbes for bioremediation: prospects and regulatory challenges. Technol Soc 32(4):331–335

    Article  Google Scholar 

  • Gigoriev IV, Nikitin R, Haridas S, Kuo A, Ohm R, Otillar R, Riley R, Salamov A, Zhao X, Korzeniewski F, Smirnova T, Nordberg H, Dubchak I, Shabalov I (2014) MycoCosm portal: gearing up for 1000 fungal genomes. Nucleic Acids Res 42:D699–D704

    Article  CAS  Google Scholar 

  • Guengerich FP (2018) Mechanisms of cytochrome P450-catalyzed oxidations. ACS Catal 8:10964–10976

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guengerich FP, Munro AW (2013) Unusual cytochrome P450 enzymes and reactions. J Biol Chem 288:17065–17073

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hadibarata T, Tachibana S, Itoh K (2007) Biodegradation of phenanthrene by fungi screened from nature. Pakistan J Biol Sci 10:2535–2543

    Article  CAS  Google Scholar 

  • Harms H, Schlosser D, Wick LY (2011) Untapped potential: exploiting fungi in bioremediation of hazardous chemicals. Nat Rev Microbiol 9:177–192. https://doi.org/10.1038/nrmicro2519

    Article  CAS  PubMed  Google Scholar 

  • Jacob J (1996) The significance of polycyclic aromatic hydrocarbons as environmental carcinogens. Pure Appl Chem 68:301–308

    Article  CAS  Google Scholar 

  • Jayasinghe C, Imtiaj A, Lee GW, Im KH, Hur H, Lee MW, Yang HS, Lee TS (2008) Degradation of three aromatic dyes by white rot fungi and the production of ligninolytic enzymes. Mycobiol 36:114–120

    Article  CAS  Google Scholar 

  • Kachienga L, Jitendra K, Momba M (2018) Metagenomic profiling for assessing microbial diversity and microbial adaptation to degradation of hydrocarbons in two South African petroleum-contaminated water aquifers. Sci Rep 8:1–6

    Article  CAS  Google Scholar 

  • Kadri T, Rouissi T, Brar SK, Cledon M, Sarma S, Verma M (2017) Biodegradation of polycyclic aromatic hydrocarbons (PAHs) by fungal enzymes: a review. J Environ Sci 51:52–74

    Article  Google Scholar 

  • Kapley A, Purohit HJ (2009) Genomic tools in bioremediation. Indian J Microbiology 49:108–113

    Article  CAS  Google Scholar 

  • Karigar CS, Rao SS (2011) Role of microbial enzymes in the bioremediation of pollutants: a review. Enz Res 2011

  • Kelly SL, Kelly DE (2013) Microbial cytochromes P450: biodiversity and biotechnology. Where do cytochromes P450 come from, what do they do and what can they do for us? Philos T R Soc B: Biol Sci 368:20120476

    Article  CAS  Google Scholar 

  • Kristanti RA, Hadibarata T, Toyama T, Tanaka Y, Mori K (2011) Bioremediation of crude oil by white rot fungi Polyporus sp. S133. J Microbiol Biotechnol 21:995–1000

    Article  CAS  PubMed  Google Scholar 

  • Kumavath RN, Deverapalli P (2013) Scientific swift in bioremediation: an overview. Int J Pharm Sci 4:375–388

    Google Scholar 

  • Liang C, Huang Y, Wang Y, Ye Q, Zhang Z, Wang H (2019) Distribution of bacterial polycyclic aromatic hydrocarbon (PAH) ring-hydroxylating dioxygenases genes in oilfield soils and mangrove sediments explored by gene-targeted metagenomics. Appl Mcrobiol Biot 103:2427–2440

    Article  CAS  Google Scholar 

  • Liu Q, Luo L, Zheng L (2018) Lignins: biosynthesis and biological functions in plants. Int J Mol Sci 19:335

    Article  PubMed Central  CAS  Google Scholar 

  • Lladó S, Covino S, Solanas AM, Viñas M, Petruccioli M, D’annibale A (2013) Comparative assessment of bioremediation approaches to highly recalcitrant PAH degradation in a real industrial polluted soil. J Hazard 248:407–414

    Article  CAS  Google Scholar 

  • Malla MA, Dubey A, Yadav S, Kumar A, Hashem A (2018) Understanding and designing the strategies for the microbe-mediated remediation of environmental contaminants using omics approaches. Front Microbiol 9. https://doi.org/10.3389/fmicb.2018.01132

  • Marcelino VR, Irinyi L, Eden JS, Meyer W, Holmes EC, Sorrell TC (2019) Metatranscriptomics as a tool to identify fungal species and subspecies in mixed communities–a proof of concept under laboratory conditions. IMA Fungus 10:8

    Article  Google Scholar 

  • Mclaren MR, Willis AD, Callahan BJ (2019) Consistent and correctable bias in metagenomic sequencing experiments. Elife 8:1–31

    Article  Google Scholar 

  • Megharaj M, Ramakrishnan B, Venkateswarlu K, Sethunathan N, Naidu R (2011) Bioremediation approaches for organic pollutants: a critical perspective. Environ Int 37(8):1362–1375

    Article  CAS  PubMed  Google Scholar 

  • Min B, Park H, Jang Y, Kim J-J, Kim KH, Pangilinan J, Lipzen A, Riley R, Grigoriev IV, Spatafora JW, Choi I-G (2015) Genome sequence of a white rot fungus Schizopora paradoxa KUC8140 for wood decay and mycoremediation. J Biotechnol 211:42–43

    Article  CAS  PubMed  Google Scholar 

  • Morales LT, González-garcía LN, Orozco MC, Restrepo S, Vives MJ (2017) The genomic study of an environmental isolate of Scedosporium apiospermum shows its metabolic potential to degrade hydrocarbons. Stand Genomic Sci 12(1):1–12. https://doi.org/10.1186/s40793-017-0287-6

    Article  CAS  Google Scholar 

  • Nayak V, Pai PV, Pai A, Pai S, Sushma YD, Rao CV (2013) A comparative study of caffeine degradation by four different fungi. Bioremediat J 17:79–85

    Article  CAS  Google Scholar 

  • Nelson DR (2018) Cytochrome P450 diversity in the tree of life. BBA-Proteins Proteom 1866:141–154

    Article  CAS  Google Scholar 

  • Nolan LC, O’Connor KE (2008) Dioxygenase-and monooxygenase-catalysed synthesis of cis-dihydrodiols, catechols, epoxides and other oxygenated products. Biotechnol Lett 30:1879–1891

  • Novotný Č, Svobodová K, Erbanová P, Cajthaml T, Kasinath A, Lang E , Šašek V (2004) Ligninolytic fungi in bioremediation: extracellular enzyme production and degradation rate. Soil Biol Biochem 36 (10):1545–1551

  • Park H, Min B, Jang Y, Kim J, Lipzen A, Sharma A, Andreopoulos B, Johnson J, Riley R, Spatafora JW (2019) Comprehensive genomic and transcriptomic analysis of polycyclic aromatic hydrocarbon degradation by a mycoremediation fungus, Dentipellis sp. KUC8613. Appl Microbiol Biot 103:8145–8155

    Article  CAS  Google Scholar 

  • Petsas AS, Vagi MC (2019) Trends in the bioremediation of pharmaceuticals and other organic contaminants using native or genetically modified microbial strains: a review. Curr Pharm Biotechnol 20:787–824

    Article  CAS  PubMed  Google Scholar 

  • Phale PS, Sharma A, Gautam K (2019) Microbial degradation of xenobiotics like aromatic pollutants from the terrestrial environments. In: Pharmaceuticals and personal care products: waste management and treatment technology. Elsevier, 259–278

  • Pizzul L, del Pilar CM, Stenström J (2009) Degradation of glyphosate and other pesticides by ligninolytic enzymes. Biodegradation 20:751–759

    Article  CAS  PubMed  Google Scholar 

  • Pointing S (2001) Feasibility of bioremediation by white-rot fungi. Appl Microbiol Biotechnol 57:20–33

    Article  CAS  PubMed  Google Scholar 

  • Pozdnyakova NN (2012) Involvement of the ligninolytic system of white-rot and litter-decomposing fungi in the degradation of polycyclic aromatic hydrocarbons. Biotechnol Res Int 2012:1–20

    Article  CAS  Google Scholar 

  • Přenosilová L, Křesinová Z, Amemori AS, Cajthaml T, Svobodová K (2013) Transcriptional response of lignin-degrading enzymes to 17α-ethinyloestradiol in two white rots. Microb Biotechnol 6:300–306

    Article  PubMed  CAS  Google Scholar 

  • Pu Y, Kosa M, Kalluri UC, Tuskan GA, Ragauskas AJ (2011) Challenges of the utilization of wood polymers: how can they be overcome? Appl Microbiol Biotechnol 91:1525–1536

    Article  CAS  PubMed  Google Scholar 

  • Raghukumar C, D’Souza-Ticlo D, Verma A (2008) Treatment of colored effluents with lignin-degrading enzymes: an emerging role of marine-derived fungi. Crit Rev Microbiol 34:189–206

    Article  CAS  PubMed  Google Scholar 

  • Ruiz-Dueñas FJ, Martínez ÁT (2009) Microbial degradation of lignin: how a bulky recalcitrant polymer is efficiently recycled in nature and how we can take advantage of this. Microb Biotechnol 2:164–177

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Senda T, Yamada T, Sakurai N, Kubota M, Nishizaki T, Masai E, Fukuda M, Mitsui Y (2000) Crystal structure of NADH-dependent ferredoxin reductase component in biphenyl dioxygenase. J Mol Biol 304:397–410

    Article  CAS  PubMed  Google Scholar 

  • Shah MP (2014) Environmental bioremediation: a low cost nature’s natural biotechnology for environmental clean-up. J Pet Environ Biot 5:1

    CAS  Google Scholar 

  • Sigoillot JC, Berrin JG, Bey M, Lesage-Meessen L, Levasseur A, Lomascolo A, Record E, Uzan-Boukhris E (2012) Fungal strategies for lignin degradation. In: Advances in botanical research. Elsevier, 263–308

  • Singh OV, Jain RK (2003) Phytoremediation of toxic aromatic pollutants from soil. Appl Microbiol Biotechnol 63:128–135

    Article  CAS  PubMed  Google Scholar 

  • Singh PP, Jaiswar A, Srivastava D, Adholeya A (2019) Draft genome sequence of Aspergillus flavus isolate TERIBR1, a highly tolerant fungus to chromium stress. BMC Res Notes 12(1):443

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Syed K, Doddapaneni H, Subramanian V, Lam YW, Yadav JS (2010) Genome-to-function characterization of novel fungal P450 monooxygenases oxidizing polycyclic aromatic hydrocarbons (PAHs). Biochem Bioph Res Co 399:492–497

    Article  CAS  Google Scholar 

  • Syed K, Porollo A, Lam YW, Yadav JS (2011) A fungal P450 (CYP5136A3) capable of oxidizing polycyclic aromatic hydrocarbons and endocrine disrupting alkylphenols: role of Trp129 and Leu324. PLoS One 6:e28286

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Syed K, Porollo A, Lam YW, Grimmett PE, Yadav JS (2013) CYP63A2, a catalytically versatile fungal P450 monooxygenase capable of oxidizing higher-molecular-weight polycyclic aromatic hydrocarbons, alkylphenols, and alkanes. Appl Environ Microbiol 79:2692–2702

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tekere M (2019) Microbial bioremediation and different bioreactors designs applied. In: Biotechnology and bioengineering. IntechOpen

  • Tkavc R, Matrosova VY, Grichenko OE, Gostinčar C, Volpe RP, Klimenkova P, Gaidamakova EK, Zhou CE, Stewart BJ, Lyman MG (2018) Prospects for fungal bioremediation of acidic radioactive waste sites: characterization and genome sequence of Rhodotorula taiwanensis MD1149. Front Microbiol 8:2528

    Article  PubMed  PubMed Central  Google Scholar 

  • Torres-Duarte C, Roman R, Tinoco R, Vazquez-Duhalt R (2009) Halogenated pesticide transformation by a laccase-mediator system. Chemosphere 77:687–692

    Article  CAS  PubMed  Google Scholar 

  • Tuomela M, Hatakka A (2019) Oxidative fungal enzymes for bioremediation. In: Comprehensive biotechnology: environmental and related biotechnologies. Elsevier, 224–239

  • Ventorino V, Pascale A, Adamo P, Rocco C, Fiorentino N, Mori M, Faraco V, Pepe O, Fagnano M (2018) Comparative assessment of autochthonous bacterial and fungal communities and microbial biomarkers of polluted agricultural soils of the Terra dei Fuochi. Sci Rep 8:1–13

    Article  CAS  Google Scholar 

  • Vrsanska M, Voberkova S, Langer V, Palovcikova D, Moulick A, Adam V, Kopel P (2016) Induction of laccase, lignin peroxidase and manganese peroxidase activities in white-rot fungi using copper complexes. Molecules 21:1553

    Article  PubMed Central  CAS  Google Scholar 

  • Yergeau E, Sanschagrin S, Beaumier D, Greer CW (2012) Metagenomic analysis of the bioremediation of diesel-contaminated Canadian high arctic soils PloS one 7

  • Young D, Rice J, Martin R, Lindquist E, Lipzen A, Grigoriev I, Hibbett D (2015) Degradation of bunker C fuel oil by white-rot fungi in sawdust cultures suggests potential applications in bioremediation. PLoS One 10:e0130381

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yu G, Wen X, Li R, Qian Y (2006) In vitro degradation of a reactive azo dye by crude ligninolytic enzymes from nonimmersed liquid culture of Phanerochaete chrysosporium. Process Biochem 41:1987–1993

    Article  CAS  Google Scholar 

  • Zafra G, Taylor TD, Absalón AE, Cortés-Espinosa DV (2016) Comparative metagenomic analysis of PAH degradation in soil by a mixed microbial consortium. J Hazard Mater 318:702–710

    Article  CAS  PubMed  Google Scholar 

  • Zafra G, Absalón ÁE, Anducho-Reyes MÁ, Fernandez FJ, Cortés-Espinosa DV (2017) Construction of PAH-degrading mixed microbial consortia by induced selection in soil. Chemosphere 172:120–126

    Article  CAS  PubMed  Google Scholar 

  • Zhang Z, Wen J, Li J, Ma X, Yu Y, Tan X, Wang Q, Liu B, Li X, Li Y, Gong L (2018) The evolution of genomic and epigenomic features in two Pleurotus fungi. Sci Rep 8:1–15

    Article  CAS  Google Scholar 

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Funding

This work is supported by the Cooperative Research Program for Agriculture Science & Technology Development (Project No. PJ01337602) and Rural Development Administration and New and Renewable Energy Core Technology Program of the Korea Institute of Energy Technology Evaluation and Planning (KETEP) grants from the Ministry of Trade, Industry, and Energy (No. 20173010092460), Republic of Korea.

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HP and I-GC conceived and designed research. HP conducted experiments. HG and I-GC analyzed data. HP and I-GC wrote and approved the manuscript.

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Correspondence to In-Geol Choi.

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Park, H., Choi, IG. Genomic and transcriptomic perspectives on mycoremediation of polycyclic aromatic hydrocarbons. Appl Microbiol Biotechnol 104, 6919–6928 (2020). https://doi.org/10.1007/s00253-020-10746-1

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