Abstract
Microbial degradation of dibenzothiophene (DBT) beyond 3-hydroxy-2-formylbenzothiophene (HFBT), a commonly detected metabolite of the Kodama pathway for DBT metabolism, and the catabolic intermediates leading to its mineralization are not fully understood. The enrichment cultures cultivated from crude oil contaminated soil led to isolation of ERI-11; a natural mixed culture, selected for its ability to deplete DBT in basal salt medium (BSM). A bacterial strain isolated from ERI-11, and tentatively named A11, degraded more than 90 % of the initial DBT (270 µM), present as the sole carbon and sulfur source, in 72 h. Gas chromatography–mass spectrophotometry (GC–MS) analyses of the DBT degrading A11 culture medium extracts led to detection of HFBT. The metabolite HFBT, produced using A11, was used in degradation assays to evaluate its metabolism by the bacteria isolated in this study. Ultra violet–visible spectrophotometry and high-performance liquid chromatography analyses established the ability of the strain A11 to deplete HFBT, present as the sole sulfur and carbon source in BSM. GC–MS analyses showed the presence of 2-mercaptobenzoic acid in the HFBT degrading A11 culture extracts. The findings in this study establish that the environmental isolate A11 possesses the metabolic capacity to degrade DBT beyond the metabolite HFBT. The compound 2-mercaptobenzoic acid is an intermediate formed on HFBT degradation by A11.
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References
Andersson JT, Hegazi AH, Roberz B (2006) Polycyclic aromatic sulfur heterocycles as information carriers in environmental studies. Anal Bioanal Chem 386:891–905
Baldwin JE, Krebs H (1981) The evolution of metabolic cycles. Nature 291:381–382
Bohonos N, Chou TW, Spangord RJ (1977) Some observations on biodegradation of pollutants in aquatic systems. Jpn J Antibiot 30:275–285
Bressler DC, Fedorak PM (2000) Bacterial metabolism of flourene, dibenzofuran, dibenzothiophene and carbazole. Can J Microbiol 46:392–409
Bressler DC, Fedorak PM (2001a) Purification, stability, and mineralization of 3-hydroxy-2-formylbenzothiophene, a metabolite of dibenzothiophene. Appl Environ Microbiol 67:821–826
Bressler DC, Fedorak PM (2001b) Identification of disulfides from the biodegradation of dibenzothiophene. Appl Environ Microbiol 67:5084–5093
Collins CH, Lyne PM (1976) Microbiological methods. Butterworths and Co Ltd., London
Denome SA, Stanley DC, Olson ES, Young KD (1993) Metabolism of dibenzothiophene and naphthalene in Pseudomonas strains: complete DNA sequence of an upper naphthalene catabolic pathway. J Bacteriol 175:6890–6901
Di Gregorio S, Zocca C, Sidler S, Toffanin A, Lizzari D, Vallini G (2004) Identification of two new sets of genes for dibenzothiophene transformation in Burkholderia sp. DBT1. Biodegradation 15:111–123
Eaton RW, Nitterauer JD (1994) Biotransformation of benzothiophene by isopropylbenzene-degrading bacteria. J Bacteriol 176:3992–4002
Fedorak PM, Grbić-Galić D (1991) Aerobic microbial cometabolism of benzothiophene and 3-methylbenzothiophene. Appl Environ Microbiol 57:932–940
Finkelstein ZI, Baskunov BP, Vavilova LN, Golovleva LA (1997) Microbial transformation of dibenzothiophene and 4,6-dimethyldibenzothiophene. Microbiology (Mikrobiologiya) 66:402–407
Foght JM, Westlake DW (1990) Expression of dibenzothiophene-degradative genes in two Pseudomonas species. Can J Microbiol 36:718–724
Frassinetti S, Setti L, Corti A, Farrinelli P, Montevecchi P, Vallini G (1998) Biodegradation of dibenzothiophene by a nodulating isolate of Rhizobium meliliti. Can J Microbiol 44:289–297
Fricourt MP, Berthou E, Picart D (1982) Dibenzothiphene derivatives as organic markers of oil pollution. Toxicol Environ Chem 5:205–215
Gai Z, Yu B, Wang X, Deng Z, Xu P (2008) Microbial transformation of benzothiophenes with carbazole as the auxiliary substrate, by Sphingomonas sp. strain XLDN2-5. Microbiology 154:3804–3812
Gallagher JR, Olson ES, Stanley DC (1993) Microbial desulfurization of dibenzothiophene: a sulfur-specific pathway. FEMS Microbiol Lett 107:31–36
Hegazi AH, Fathalla EM, Panda SK, Schrader W, Andersson JT (2012) High-molecular weight sulfur-containing aromatics refractory to weathering as determined by Fourier transform ion cyclotron resonance mass spectrometry. Chemosphere 89:205–212
Hostettler FD, Kvenvolden KA (1994) Geochemical changes in crude oil spilled from the Exxon Valdez super tanker into Prince William Sound Alaska. Org Geochem 21:927–936
Hou CT, Laskin AI (1976) Microbial conversion of dibenzothiophene. Dev Ind Microbiol 17:351–362
Jiménez N, Viñas M, Guiu-Aragonés C, Bayona JM, Albaigés J, Solanas AM (2011) Polyphasic approach for assessing changes in an autochthonous marine bacterial community in the presence of Prestige fuel oil and its biodegradation potential. Appl Microbiol Biotechnol 91:823–834
Khedkar S (2005) Microbial transformation of organic sulfur compounds. Dissertation, Indian Institute of Technology Bombay
Kiyohara H, Nagao K, Yana K (1982) Rapid screen for bacteria degrading water insoluble, solid hydrocarbons on agar plates. Appl Environ Microbiol 43:454–457
Kodama K (1977) Cometabolism of dibenzothiophenes by Pseudomonas jianii. Agric Biol Chem 41:1305–1306
Kodama K, Nakatani S, Umehara K, Shimizu K, Minoda Y, Yamada K (1970) Microbial conversion of petro-sulfur compounds. Part III. Isolation and identification of products from dibenzothiophene. Agric Biol Chem 34:1320–1324
Kodama K, Umehara K, Shimizu K, Nakatani S, Minoda Y, Yamada K (1973) Identification of microbial products from dibenzothiophene and its proposed oxidation pathway. Agric Biol Chem 37:45–50
Kropp KG, Fedorak PM (1998) A review of the occurrence, toxicity and biodegradation of condensed thiophenes found in petroleum. Can J Microbiol 44:605–622
Kropp KG, Gonçalves JA, Andersson JT, Fedorak PM (1994) Microbial transformations of benzothiophene and methylbenzothiophenes. Environ Sci Technol 28:1348–1356
Kropp KG, Saftić S, Andersson JT, Fedorak PM (1996) Transformations of six isomers of dimethylbenzothiophene by three Pseudomonas strains. Biodegradation 3:203–221
Kropp KG, Andersson JT, Fedorak PM (1997a) Biotransformations of three dimethyldibenzothiophenes by pure and mixed bacterial cultures. Environ Sci Technol 31:1547–1554
Kropp KG, Andersson JT, Fedorak PM (1997b) Bacterial transformations of 1,2,3,4-tetrahydrodibenzothiophene and dibenzothiophene. Appl Environ Microbiol 63:3032–3042
Kumar S, Lin JM, Whysner J, Sikka HC, Amin S (2004) Mutagenicity of benzo[b]phenanthro[2,3-d]thiophene (BPT) and its metabolites in TA100 and base-specific tester strains (TA7001-TA7006) of Salmonella typhimurium: evidence of multiple pathways for the bioactivation of BPT. Mutat Res 545:11–21
Laborde AL, Gibson DT (1977) Metabolism of dibenzothiophene by a Beijerinckia sp. Appl Environ Microbiol 34:783–790
Li M, Wang TG, Simoneit BR, Shi S, Zhang L, Yang F (2012) Qualitative and quantitative analysis of dibenzothiophene, its methylated homologues, and benzonaphthothiophenes in crude oils, coal, and sediment extracts. J Chromatogr A 1233:126–136
Lu J, Nakajima-Kambe T, Shigeno T, Ohbo A, Nomura N, Nakahara T (1999) Biodegradation of dibenzothiophene and 4,6-dimethyldibenzothiophene by Sphingomonas paucimobilis strain TZS-7. J Biosci Bioeng 88:293–299
Mahjoubi M, Jaouani A, Guesmi A, Ben Amor S, Jouini A, Cherif H, Najjari A, Boudabous A, Koubaa N, Cherif A (2013) Hydrocarbonoclastic bacteria isolated from petroleum contaminated sites in Tunisia: isolation, identification and characterization of the biotechnological potential. N Biotechnol. doi:10.1016/j.nbt.2013.03.004
Manickam N, Pathak A, Saini HS, Mayilraj S, Shanker R (2010) Metabolic profiles and phylogenetic diversity of microbial communities from chlorinated pesticides contaminated sites of different geographical habitats of India. J Appl Microbiol 109:1458–1468
Meyer S, Steinhart H (2000) Effects of heterocyclic PAHs (N, S, O) on the biodegradation of typical tar oil PAHs in a soil/compost mixture. Chemosphere 40:359–367
Mohebali G, Ball AS (2008) Biocatalytic desulfurization (BDS) of petrodiesel fuels. Microbiology 154:2169–2183
Monticello DJ, Bakker D, Finnerty WR (1985) Plasmid-mediated degradation of dibenzothiophene by Pseudomonas species. Appl Environ Microbiol 49:756–760
Mormile MR, Atlas RM (1988) Mineralization of the dibenzothiophene biodegradation products 3-hydroxy-2-formyl benzothiophene and dibenzothiophene sulfone. Appl Environ Microbiol 54:3183–3184
Mormile MR, Atlas RM (1989) Biotransformation of dibenzothiophene to dibenzothiophene sulfone by Pseudomonas putida. Can J Microbiol 35:603–605
Nakatani S, Akasaki T, Kodama K, Minoda Y, Yamada K (1968) Microbial conversion of petrosulfur-compounds. Part II. Culture conditions of dibenzothiophene-utilizing bacteria. Agric Biol Chem 32:1205–1211
Nojiri H, Habe H, Omori T (2001) Bacterial degradation of aromatic compounds via angular dioxygenation. J Gen Appl Microbiol 47:279–305
Panda SK, Schrader W, Andersson JT (2007) Distribution of polycyclic aromatic sulfur heterocycles in three Saudi Arabian crude oils as determined by Fourier transform ion cyclotron resonance mass spectrometry. Energy Fuels 21:1071–1077
Piccoli S, Andreolli M, Giorgetti A, Zordan F, Lampis S, Vallini G (2013) Identification of aldolase and ferredoxin reductase within the dbt operon of Burkholderia fungorum DBT1. J Basic Microbiol. doi:10.1002/jobm.201200408
Prasad MN, Prasad R (2012) Nature’s cure for cleanup of contaminated environment: a review of bioremediation strategies. Rev Environ Health 27:181–189
Rayu S, Karpouzas DG, Singh BK (2012) Emerging technologies in bioremediation: constraints and opportunities. Biodegradation 23:917–926
Saftić S, Fedorak PM, Andersson JT (1992) Diones, sulfoxides and sulfones from the aerobic cometabolism of methylbenzothiophenes by Pseudomonas strain BT1. Environ Sci Technol 26:1756–1784
Saftić S, Fedorak PM, Andersson JT (1993) Transformations of methyldibenzothiophenes by three Pseudomonas isolates. Environ Sci Technol 27:2577–2584
Seo JS (2012) Multiple pathways in the degradation of dibenzothiophene by Mycobacterium aromativorans strain JS19b1T. J Korean Soc Appl Biol Chem 55:613–618
Seo JS, Keum YS, Li QX (2009) Bacterial degradation of aromatic compounds. Int J Environ Res Public Health 6:278–309
Shanker R, Purohit HJ, Khanna P (1998) Bioremediation for hazardous waste management: The Indian Scenario. In: Sikdar SK, Irvine RL (eds) Bioremediation: principles and practices, vol III. Bioremediation Technologies Technomic Publishing Co. Inc., Lancaster, pp 81–96
Stolp H, Starr MP (1986) Principles of isolation, cultivation and conservation of bacteria. In: Starr MP, Stolp H, Trupper HG, Balows A, Schlegel HG (eds) The prokaryotes: a handbook on habitat, isolation and identification of bacteria. Springer, Berlin Heidelberg New York Tokyo, pp 135–175
Swartz CD, King LC, Nesnow S, Umbach DM, Kumar S, Sikka H, Demarini DM (2009) Mutagenicity, stable DNA adducts, and abasic sites induced in Salmonella by phenanthro[3,4-b]- and phenanthro[4,3-b]thiophenes, sulfur analogs of benzo[c]phenanthrene. Mutat Res 661:47–56
Thaens D, Heinzelmann D, Böhme A, Paschke A, Schüürmann G (2012) Chemoassay screening of DNA-reactive mutagenicity with 4-(4-nitrobenzyl)pyridine—application to epoxides, oxetanes, and sulfur heterocycles. Chem Res Toxicol 25(10):2092–2102
Van Afferden M, Tappe D, Beyer M, Truper HG, Klein J (1993) Biochemical mechanisms for the desulfurization of coal-relevant organic sulfur compounds. Fuel 72:635–643
Wasi S, Tabrez S, Ahmad M (2013) Use of Pseudomonas spp. for the bioremediation of environmental pollutants: a review. Environ Monit Assess 185:8147–8155
Yamada K, Minoda Y, Kodama K, Nakatani S, Akasaki T (1968) Microbial conversion petrosulfur compounds. Part I. Isolation and identification of dibenzothiophene utilizing bacteria. Agric Biol Chem 32:840–845
Yang B, Hou W, Zhang K, Wang X (2013) Application of solid-phase microextraction to the determination of polycyclic aromatic sulfur heterocycles in Bohai Sea crude oils. J Sep Sci 16:2646–2655
Young RF, Cheng SM, Fedorak PM (2006) Aerobic biodegradation of 2,2′-dithiodibenzoic acid produced from dibenzothiophene metabolites. Appl Environ Microbiol 72:491–496
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This work was supported by a grant from the Department of Biotechnology, Ministry of Science and Technology, Government of India.
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Khedkar, S., Shanker, R. Degradation of dibenzothiophene and its metabolite 3-hydroxy-2-formylbenzothiophene by an environmental isolate. Biodegradation 25, 643–654 (2014). https://doi.org/10.1007/s10532-014-9688-z
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DOI: https://doi.org/10.1007/s10532-014-9688-z