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.
Similar content being viewed by others
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
Boldrin B, Tiehm A, Fritzsche C (1993) Degradation of phenanthrene, fluorene, fluoranthene, and pyrene by a Mycobacterium sp. Appl Environ Microbiol 59:1927–1930
Boyd DR, Bugg TD (2006) Arene cis-dihydrodiol formation: from biology to application. Org Biomol Chem 4:181–192
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
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
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
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
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
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
Gan S, Lau E, Ng H (2009) Remediation of soils contaminated with polycyclic aromatic hydrocarbons (PAHs). J Hazard Mater 172:532–549
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
Gordon L, Dobson AD (2001) Fluoranthene degradation in Pseudomonas alcaligenes PA-10. Biodegradation 12:393–400
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
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
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
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
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
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
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
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
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
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
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
Lee SE, Seo JS, Keum YS, Lee KJ, Li QX (2007) Fluoranthene metabolism and associated proteins in Mycobacterium sp. JS14. Proteomics 7:2059–2069
Lopez Z, Vila J, Minguillon C, Grifoll M (2006) Metabolism of fluoranthene by Mycobacterium sp. strain AP1. Appl Microbiol Biotechnol 70:747–756
Lovell SC et al (2003) Structure validation by Cα geometry: ϕ, ψ and Cβ deviation. Proteins: Struct, Funct, Bioinf 50:437–450
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
Mason JR, Cammack R (1992) The electron-transport proteins of hydroxylating bacterial dioxygenases. Annu Rev Microbiol 46:277–305
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
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
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
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
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
Seo JS, Keum YS, Li QX (2009) Bacterial degradation of aromatic compounds. Int J Environ Res Public Health 6:278–309
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
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
Wang F et al (2010) Short-time effect of heavy metals upon microbial community activity. J Hazard Mater 173:510–516
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
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
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).
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Gerald Thouand
Electronic supplementary material
Fig. S1
(DOCX 169 kb)
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-016-7809-4