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Fluoranthene degradation and binding mechanism study based on the active-site structure of ring-hydroxylating dioxygenase in Microbacterium paraoxydans JPM1

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Abstract

In this study, a gram-positive fluoranthene-degrading bacterial strain was isolated from crude oil in Dagang Oilfield and identified as Microbacterium paraoxydans JPM1 by the analysis of 16S rDNA sequence. After 25 days of incubation, the strain JPM1 could degrade 91.78 % of the initial amount of fluoranthene. Moreover, four metabolites 9-fluorenone-1-carboxylic acid, 9-fluorenone, phthalic acid, and benzoic acid were detected in the culture solution. The gene sequence encoding the aromatic-ring-hydroxylating dioxygenase was amplified in the strain JPM1 by PCR. Based on the translated protein sequence, a homology modeling method was applied to build the crystal structure of dioxygenase. Subsequently, the interaction mechanism between fluoranthene and the active site of dioxygenase was simulated and analyzed by molecular docking. Consequently, a feasible degrading pathway of fluoranthene in the strain JPM1 was proposed based on the metabolites and the interaction analyses. Additionally, the thermodynamic analysis showed that the strain JPM1 had high tolerance for fluoranthene, and the influence of fluoranthene for the bacterial growth activity was negligible under 100 to 400 mg L−1 concentrations. Taken together, this study indicates that the strain JPM1 has high potential for further study in bioremediation of polycyclic aromatic hydrocarbon (PAH)-contaminated sites.

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References

  • Ahmed RZ, Ahmed N (2014) Effect of yeast extract on fluoranthene degradation and aromatic ring dioxygenase expressing bacterial community structure of a fluoranthene degrading bacterial consortium. Int Biodeterior Biodegrad 88:56–61

    Article  CAS  Google Scholar 

  • Boldrin B, Tiehm A, Fritzsche C (1993) Degradation of phenanthrene, fluorene, fluoranthene, and pyrene by a Mycobacterium sp. Appl Environ Microbiol 59:1927–1930

    CAS  Google Scholar 

  • Boyd DR, Bugg TD (2006) Arene cis-dihydrodiol formation: from biology to application. Org Biomol Chem 4:181–192

    Article  CAS  Google Scholar 

  • Cao J, Lai Q, Yuan J, Shao Z (2015) Genomic and metabolic analysis of fluoranthene degradation pathway in Celeribacter indicus P73T. Sci Rep 5:1–12

    Google Scholar 

  • Chen Y, Zhu L, Zhou R (2007) Characterization and distribution of polycyclic aromatic hydrocarbon in surface water and sediment from Qiantang River, China. J Hazard Mater 141:148–155

    Article  Google Scholar 

  • Cui Z, Xu G, Gao W, Li Q, Yang B, Yang G, Zheng L (2014) Isolation and characterization of Cycloclasticus strains from Yellow Sea sediments and biodegradation of pyrene and fluoranthene by their syntrophic association with Marinobacter strains. Int Biodeterior Biodegrad 91:45–51

    Article  CAS  Google Scholar 

  • Dean-Ross D, Moody J, Cerniglia C (2002) Utilization of mixtures of polycyclic aromatic hydrocarbons by bacteria isolated from contaminated sediment. FEMS Microbiol Ecol 41:1–7

    Article  CAS  Google Scholar 

  • Duan L, Naidu R, Thavamani P, Meaklim J, Megharaj M (2015) Managing long-term polycyclic aromatic hydrocarbon contaminated soils: a risk-based approach. Environ Sci Pollut Res 1–15

  • Folwell BD, McGenity TJ, Whitby C (2016) Biofilm and planktonic bacterial and fungal communities transforming high-molecular-weight polycyclic aromatic hydrocarbons. Appl Environ Microbiol 82:2288–2299

    Article  CAS  Google Scholar 

  • Fuchedzhieva N, Karakashev D, Angelidaki I (2008) Anaerobic biodegradation of fluoranthene under methanogenic conditions in presence of surface-active compounds. J Hazard Mater 153:123–127

    Article  CAS  Google Scholar 

  • Gan S, Lau E, Ng H (2009) Remediation of soils contaminated with polycyclic aromatic hydrocarbons (PAHs). J Hazard Mater 172:532–549

    Article  CAS  Google Scholar 

  • Gauthier E, Déziel E, Villemur R, Juteau P, Lépine F, Beaudet R (2003) Initial characterization of new bacteria degrading high-molecular weight polycyclic aromatic hydrocarbons isolated from a 2-year enrichment in a two-liquid-phase culture system. J Appl Microbiol 94:301–311

    Article  CAS  Google Scholar 

  • Gordon L, Dobson AD (2001) Fluoranthene degradation in Pseudomonas alcaligenes PA-10. Biodegradation 12:393–400

    Article  CAS  Google Scholar 

  • Grifoll M, Selifonov SA, Chapman PJ (1995) Transformation of substituted fluorenes and fluorene analogs by Pseudomonas sp. strain F274. Appl Environ Microbiol 61:3490–3493

    CAS  Google Scholar 

  • Hadibarata T, Kristanti RA (2014) Effect of surfactants and identification of metabolites on the biodegradation of fluoranthene by basidiomycetes fungal isolate Armillaria sp. F022. Bioprocess Biosyst Eng 37:593–600

    Article  CAS  Google Scholar 

  • Han XM, Liu YR, Zheng YM, Zhang XX, He JZ (2014) Response of bacterial pdo1, nah, and C12O genes to aged soil PAH pollution in a coke factory area. Environ Sci Pollut Res 21:9754–9763

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Hilyard EJ, Jones-Meehan JM, Spargo BJ, Hill RT (2008) Enrichment, isolation, and phylogenetic identification of polycyclic aromatic hydrocarbon-degrading bacteria from Elizabeth River sediments. Appl Environ Microbiol 74:1176–1182

    Article  CAS  Google Scholar 

  • Isaac P, Lozada M, Dionisi HM, Estévez MC, Ferrero MA (2015) Differential expression of the catabolic nahAc gene and its effect on PAH degradation in Pseudomonas strains isolated from contaminated Patagonian coasts. Int Biodeterior Biodegrad 105:1–6

    Article  CAS  Google Scholar 

  • Jin JN, Yao J, Zhang QY, Yu C, Chen P, Liu WJ, Choi MMF (2015) An integrated approach of bioassay and molecular docking to study the dihydroxylation mechanism of pyrene by naphthalene dioxygenase in Rhodococcus sp. ustb-1. Chemosphere 128:307–313

    Article  CAS  Google Scholar 

  • Kauppi B, Lee K, Carredano E, Parales RE, Gibson DT, Eklund H, Ramaswamy S (1998) Structure of an aromatic-ring-hydroxylating dioxygenase-naphthalene 1, 2-dioxygenase. Structure 6:571–586

    Article  CAS  Google Scholar 

  • Kelley I, Freeman J, Evans F, Cerniglia C (1993) Identification of metabolites from the degradation of fluoranthene by Mycobacterium sp. strain PYR-1. Appl Environ Microbiol 59:800–806

    CAS  Google Scholar 

  • Kim YH, Freeman JP, Moody JD, Engesser KH, Cerniglia CE (2005) Effects of pH on the degradation of phenanthrene and pyrene by Mycobacterium vanbaalenii PYR-1. Appl Microbiol Biot 67:275–285

    Article  CAS  Google Scholar 

  • Kim SJ et al (2006) Molecular cloning and expression of genes encoding a novel dioxygenase involved in low-and high-molecular-weight polycyclic aromatic hydrocarbon degradation in Mycobacterium vanbaalenii PYR-1. Appl Environ Microbiol 72:1045–1054

    Article  CAS  Google Scholar 

  • Lee SE, Seo JS, Keum YS, Lee KJ, Li QX (2007) Fluoranthene metabolism and associated proteins in Mycobacterium sp. JS14. Proteomics 7:2059–2069

    Article  CAS  Google Scholar 

  • Lopez Z, Vila J, Minguillon C, Grifoll M (2006) Metabolism of fluoranthene by Mycobacterium sp. strain AP1. Appl Microbiol Biotechnol 70:747–756

    Article  CAS  Google Scholar 

  • Lovell SC et al (2003) Structure validation by Cα geometry: ϕ, ψ and Cβ deviation. Proteins: Struct, Funct, Bioinf 50:437–450

    Article  CAS  Google Scholar 

  • Ma J, Xu L, Jia L (2013) Characterization of pyrene degradation by Pseudomonas sp. strain Jpyr-1 isolated from active sewage sludge. Bioresour Technol 140:15–21

    Article  CAS  Google Scholar 

  • Mason JR, Cammack R (1992) The electron-transport proteins of hydroxylating bacterial dioxygenases. Annu Rev Microbiol 46:277–305

    Article  CAS  Google Scholar 

  • Mueller JG, Chapman PJ, Blattmann BO, Pritchard PH (1990) Isolation and characterization of a fluoranthene-utilizing strain of Pseudomonas paucimobilis. Appl Environ Microbiol 56:1079–1086

    CAS  Google Scholar 

  • Parales RE, Lee K, Resnick SM, Jiang H, Lessner DJ, Gibson DT (2000) Substrate specificity of naphthalene dioxygenase: effect of specific amino acids at the active site of the enzyme. J Bacteriol 182:1641–1649

    Article  CAS  Google Scholar 

  • Qi J, Wang B, Li J, Ning H, Wang Y, Kong W, Shen L (2015) Genetic determinants involved in the biodegradation of naphthalene and phenanthrene in Pseudomonas aeruginosa PAO1. Environ Sci Pollut Res 22:6743–6755

    Article  CAS  Google Scholar 

  • Rehmann K, Hertkorn N, Kettrup AA (2001) Fluoranthene metabolism in Mycobacterium sp. strain KR20: identity of pathway intermediates during degradation and growth. Microbiol 147:2783–2794

    Article  CAS  Google Scholar 

  • Schippers A, Bosecker K, Spröer C, Schumann P (2005) Microbacterium oleivorans sp. nov. and Microbacterium hydrocarbonoxydans sp. nov., novel crude-oil-degrading gram-positive bacteria. Int J Syst Evol Microbiol 55:655–660

    Article  CAS  Google Scholar 

  • Seo JS, Keum YS, Li QX (2009) Bacterial degradation of aromatic compounds. Int J Environ Res Public Health 6:278–309

    Article  CAS  Google Scholar 

  • Sheng X, He LY, Zhou L, Shen YY (2009) Characterization of Microbacterium sp. F10a and its role in polycyclic aromatic hydrocarbon removal in low-temperature soil. Can J Microbiol 55:529–535

    Article  CAS  Google Scholar 

  • Vila J, Lopez Z, Sabate J, Minguillon C, Solanas AM, Grifoll M (2001) Identification of a novel metabolite in the degradation of pyrene by Mycobacterium sp. strain AP1: actions of the isolate on two- and three-ring polycyclic aromatic hydrocarbons. Appl Environ Microbiol 67:5497–5505

    Article  CAS  Google Scholar 

  • Wang F et al (2010) Short-time effect of heavy metals upon microbial community activity. J Hazard Mater 173:510–516

    Article  CAS  Google Scholar 

  • Weissenfels W, Beyer M, Klein J, Rehm H (1991) Microbial metabolism of fluoranthene: isolation and identification of ring fission products. Appl Microbiol Biotechnol 34:528–535

    Article  CAS  Google Scholar 

  • Zhang H, Kallimanis A, Koukkou AI, Drainas C (2004) Isolation and characterization of novel bacteria degrading polycyclic aromatic hydrocarbons from polluted Greek soils. Appl Microbiol Biotechnol 65:124–131

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work is supported in part by grants from the International Joint Key Project from Chinese Ministry of Science and Technology (2010DFB23160), the National Natural Science Foundation of China (41273092, 41430106), and Public Welfare Project of Chinese Ministry of Environmental Protection (201409042, 201509049).

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Correspondence to Jun Yao.

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Responsible editor: Gerald Thouand

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Jin, J., Yao, J., Liu, W. et al. Fluoranthene degradation and binding mechanism study based on the active-site structure of ring-hydroxylating dioxygenase in Microbacterium paraoxydans JPM1. Environ Sci Pollut Res 24, 363–371 (2017). https://doi.org/10.1007/s11356-016-7809-4

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