Carbazole angular dioxygenation and mineralization by bacteria isolated from hydrocarbon-contaminated tropical African soil

Environmental Science and Pollution Research

Volumn 21, Issue 15, 2014, Pages 9311-9324

  Salam, L B ^a   Ilori, M O ^a   Amund, O O ^a   Numata, M ^b   Horisaki, T ^b   Nojiri, H ^b  

^a UNIVERSITY OF LAGOS   (Nigeria)

^b UNIVERSITY OF TOKYO   (Japan)

Author keywords

Achromobacter; Biodegradation; Carbazole; Microbacterium; Pseudomonas; Stenotrophomonas

Indexed keywords

ACHROMOBACTER; ACHROMOBACTER SP.; BACTERIA (MICROORGANISMS); MICROBACTERIUM; MICROBACTERIUM ESTERAROMATICUM; PSEUDOMONAS; PSEUDOMONAS SP.; STENOTROPHOMONAS; STENOTROPHOMONAS MALTOPHILIA;

CARBAZOLE; CARBAZOLE DERIVATIVE; HYDROCARBON; SOIL; SOIL POLLUTANT;

BACTERIUM; BIOREMEDIATION; CHEMISTRY; CLASSIFICATION; METABOLISM; MICROBIOLOGY; NIGERIA; PHYLOGENY; SOIL; SOIL POLLUTANT;

BACTERIA; BIODEGRADATION, ENVIRONMENTAL; CARBAZOLES; HYDROCARBONS; NIGERIA; PHYLOGENY; SOIL; SOIL MICROBIOLOGY; SOIL POLLUTANTS;

EID: 84905711187     PISSN: 09441344     EISSN: 16147499     Source Type: Journal    
DOI: 10.1007/s11356-014-2855-2     Document Type: Article

References (66)

1. Andreoni V, Gianfreda L (2007) Bioremediation and monitoring of aromatic-polluted habitats. Appl Microbiol Biotechnol 76: 287-308.
2. Andrew RWJ, Jackson JM (1996) Pollution and waste management. In: The natural environment and human impact. Longman Publishers, Singapore, pp 281-297.
3. Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K (ed.) (1990) Current protocols in molecular biology. John Wiley & Sons, Inc., New York, N. Y.
4. Balaban AT, Oniciu DC, Katritzky AR (2004) Aromaticity as a cornerstone of heterocyclic chemistry. Chem Rev 104(5): 2777-2812.
5. Black CA (1965) Methods of soil analysis. No. 9, Part 2. American Society of Agronomy, Madison, Wisconsin.
6. Blum P, Sagner A, Tiehm A, Martus P, Wendel T, Grathwohl P (2011) Importance of heterocyclic aromatic compounds in monitored natural attenuation for coal tar contaminated aquifers: a review. J Contam Hydrol 126: 181-194.
7. Chikere BO, Okpokwasili GC (2002) Seasonal dynamics of the pollution in a Niger Delta river receiving petrochemical effluents. Trop Freshw Biol 11: 11-22.
8. Dibble JT, Bartha R (1979) Effect of environmental parameters on the biodegradation of oily sludge. Appl Environ Microbiol 37: 729-739.
9. Eixarch H, Constanti M (2010) Biodegradation of MTBE by Achromobacter xylosoxidans MCM1/1 induces synthesis of proteins that may be related to cell survival. Process Biochem 45: 794-798.
10. Farajzadeh Z, Karbalaei-Heidari HR (2012) Isolation and characterization of a new Achromobacter sp. strain CAR1389 as a carbazole-degrading bacterium. World J Microbiol Biotechnol 28: 3075-3080.
11. Gibson F, Pittard J (1968) Pathways of biosynthesis of aromatic amino acids and vitamins and their control in microorganisms. Bacteriol Rev 32: 465-492.
12. Gieg LM, Otter A, Fedorak PM (1996) Carbazole degradation by Pseudomonas sp. LD2: metabolic characteristics and the identification of some metabolites. Environ Sci Technol 30: 575-585.
13. Giordani G, Donnelly A, Azzoni R (1998) The uptake of inorganic phosphate by Z. noltii in the Basin d' Arcachon. In: Proceedings (Handbook) of Summer Conference of the Society for Applied Microbiology, University of Lancaster, UK, pp. 22-23.
14. Grifoll M, Selifonov SA, Chapman PJ (1995) Transformation of substituted fluorenes and fluorine analogs by Pseudomonas sp. strain F274. Appl Environ Microbiol 61: 3490-3493.
15. Grosser RJ, Warshawsky D, Vestal JR (1991) Indigenous and enhanced mineralization of pyrene, benzo(a)pyrene and carbazole in soils. Appl Environ Microbiol 57: 3462-3469.
16. Guo S, Seo J-S, Wang J, Keum Y-S, Li J, Li QX (2013) Multiple degradation pathways of phenanthrene by Stenotrophomonas maltophilia C6. Int Biodeterior Biodegrad 79: 98-104.
17. Habe H, Ashikawa Y, Saiki Y, Yoshida T, Nojiri H, Omori T (2002) Sphingomonas sp. strain KA1, carrying a carbazole dioxygenase gene homologue, degrades chlorinated dibenzo-p-dioxins in soil. FEMS Microbiol Lett 211: 43-49.
18. Heuer H, Kresk M, Baker P, Smalla K, Wellington EM (1997) Analysis of actinomycete communities by specific amplification of genes encoding 16S rRNA and gel-electrophoretic separation in denaturing gradients. Appl Environ Microbiol 63: 3233-3241.
19. Holt JG, Krieg NR, Sneath PHA (1994) Bergey's manual of determinative bacteriology. William and Wilkins, Baltimore, Maryland.
20. Hong Q, Dong X, He L, Jiang X, Li S (2008) Isolation of a biphenyl-degrading bacterium, Achromobacter sp. BP3, and cloning of the bph gene cluster. Int Biodeterior Biodegrad 63: 365-370.
21. Ilori MO, Robinson GK, Adebusoye SA (2008) Degradation and mineralization of 2-chloro-, 3-chloro-, and 4-chlorobiphenyl by a newly characterized natural bacterial strain isolated from an electrical transformer fluid-contaminated soil. J Environ Sci 20: 1250-1257.
22. Inoue K, Habe H, Yamane H, Omori T, Nojiri H (2005) Diversity of carbazole-degrading bacteria having the car gene cluster: isolation of a novel Gram-positive carbazole-degrading bacterium. FEMS Microbiol Lett 245: 145-153.
23. Jain RK, Kapur M, Labana S, Lal B, Sarma PM, Bhattacharya D, Thakur IS (2005) Microbial diversity: application of microorganisms for the biodegradation of xenobiotics. Curr Sci 89: 101-112.
24. Juhasz AL, Stanley GA, Britz ML (2000) Microbial degradation and detoxification of high molecular weight polycyclic aromatic hydrocarbons by Stenotrophomonas maltophilia strain VUN 10, 003. Lett Appl Microbiol 30: 396-401.
25. Juhasz AL, Stanley GA, Britz ML (2002) Metabolite repression inhibits degradation of benzo(a)pyrene and dibenz (a, h)anthracene by Stenotrophomonas maltophilia VUN 10, 003. J Ind Microbiol Biotechnol 28: 88-96.
26. Kaczorek E, Salek K, Guzik U, Dudzinska-Bajorek B, Olszanowski A (2013) The impact of long-term contact of Achromobacter sp. 4(2010) with diesel oil-changes in biodegradation, surface properties and hexadecane monooxygenase activity. Int Biodeterior Biodegrad 78: 7-16.
27. Kanaly RA, Harayama S (2010) Advances in the field of high molecular-weight polycyclic aromatic hydrocarbon biodegradation by bacteria. Microbiol Biotechnol 3: 132-164.
28. Kilbane JJ II, Daram A, Abbasian J, Kayser KJ (2002) Isolation and characterization of Sphingomonas sp. GTIN11 capable of carbazole mineralization in petroleum. Biochem Biophys Res Commun 297: 242-248.
29. Kimura T, Omori T (1995) Microbial degradation of azaarene related compounds. Life Chem Rep 12: 207-225.
30. Kirimura K, Nakagawa H, Tsuji K, Matsuda K, Kurane R, Usami S (1999) Selective and continuous degradation of carbazole contained in petroleum oil by resting cells of Sphingomonas sp. CDH-7. Biosci Biotechnol Biochem 63: 1563-1568.
31. Larkin MJ, Kulakov LA, Allen CC (2005) Biodegradation and Rhodococcus-masters of catabolic versatility. Curr Opin Biotechnol 16: 282-290.
32. Leahy JG, Colwell RR (1990) Microbial degradation of hydrocarbons in the environment. Microbiol Rev 54: 305-315.
33. Li L, Li Q, Li F, Shi Q, Yu B, Liu F, Yu P (2006) Degradation of carbazole and its derivatives by a Pseudomonas sp. Appl Microbiol Biotechnol 73: 941-948.
34. Lobastova TG, Sukhodolokaya GV, Nikolayeva VM, Baskunov BP, Turchin KF, Donova MV (2004) Hydroxylation of carbazoles by Aspergillus flavus VKM F-1024. FEMS Microbiol Lett 235: 51-56.
35. Maeda R, Nagashima H, Widada J, Iwata K, Omori T (2009) Novel marine carbazole-degrading bacteria. FEMS Microbiol Lett 292: 203-209.
36. Maier RM (2009) Microorganisms and organic pollutants. In: Maier RM, Pepper IL, Gerba CP (eds) Environmental Microbiology, 2nd edn. Academic Press, London, pp 387-420.
37. Mutnuri S, Vasudevan N, Kaestner M (2005) Degradation of anthracene and pyrene supplied by microcrystals and non-aqueous-phase liquids. Appl Microbiol Biotechnol 67: 569-576.
38. Mwegoha WJS, Kilampa C (2010) Heavy metal contamination in agricultural soils and water in Dae es Salaam city, Tanzania. Afr J Environ Sci Technol 4(11): 763-769.
39. Nayak AS, Veeranagouda Y, Lee K, Karegoudar TB (2009) Metabolism of acenaphthylene via 1, 2-dihydroxynaphthalene and catechol by Stenotrophomonas sp. RMSK Biodegradation 20: 837-843.
40. Nies DH (1999) Microbial heavy metal resistance. Appl Microbiol Biotechnol 51: 730-750.
41. Nies DH, Silver S (1995) Ion efflux systems involved in bacterial metal resistances. J Ind Microbiol 14: 186-199.
42. Nojiri H (2012) Structural and molecular genetic analyses of the bacterial carbazole degradation system. Biosci Biotechnol Biochem 76(1): 1-18.
43. Nojiri H, Omori T (2002) Molecular bases of aerobic bacterial degradation of dioxins: involvement of angular dioxygenation. Biosci Biotechnol Biochem 66: 2001-2016.
44. Nojiri H, Omori T (2007) Carbazole metabolism by Pseudomonads. In: Ramos J-L, Filloux A (eds) Pseudomonas, 5th edn. Springer, New York, pp 107-145.
45. Nojiri H, Nam J-W, Kosaka M, Morii K-I, Takemura T, Furihata K, Yamane H, Omori T (1999) Diverse oxygenations catalyzed by carbazole 1, 9a-dioxygenase from Pseudomonas sp. strain CA10. J Bacteriol 181(10): 3105-3113.
46. Nojiri H, Sekiguchi H, Maeda K, Urata M, Nakai S, Yoshida T, Habe H, Omori T (2001) Genetic characterization and evolutionary implications of a car gene cluster in the carbazole degrader Pseudomonas sp. strain CA10. J Bacteriol 183: 3663-3679.
47. Nucifora G, Chu L, Misra TK, Silver S (1989) Cadmium resistance from Staphylococcus aureus plasmid p1258 cadA gene results from cadmium-efflux ATPase. Proc Natl Acad Sci U S A 86: 3544-3548.
48. Obayori OS, Ilori MO, Adebusoye SA, Amund OO, Oyetibo GO (2008a) Microbial population changes in tropical agricultural soil experimentally contaminated with crude petroleum. Afr J Biotechnol 7(24): 4512-4520.
49. Obayori OS, Ilori MO, Adebusoye SA, Oyetibo GO, Amund OO (2008b) Pyrene-degradation potentials of Pseudomonas species isolated from polluted tropical soils. World J Microbiol Biotechnol 24: 2639-2646.
50. Odabasi M, Cetin B, Sofuoglu A (2006) Henry's law constant, octanol-air partition coefficient and supercooled liquid vapour pressure of carbazole as a function of temperature: application to gas/particle partitioning in the atmosphere. Chemosphere 62: 1087-1096.
51. Ouchiyama N, Zhang Y, Omori T, Kodama T (1993) Biodegradation of carbazole by Pseudomonas spp. CA06 and CA10. Biosci Biotechnol Biochem 57: 455-460.
52. Ouchiyama N, Miyachi S, Omori T (1998) Cloning and nucleotide sequence of carbazole catabolic genes from Pseudomonas stutzeri strain OM1, isolated from activated sludge. J Gen Appl Microbiol 44: 57-63.
53. Outten FW, Outten CE, O'Halloran T (2000) Metalloregulatory systems at the interface between bacterial metal homeostasis and resistance. In: Storz G, Hengge-Aronis R (eds) Bacterial stress responses. ASM Press, Washington D. C, pp 145-157.
54. Peddinghaus S, Brinkmann M, Bluhm K, Sagner A, Hinger G, Braunbeck T, Eisentrager A, Tiehm A, Hollert H, Keiter S (2012) Quantitative assessment of the embryotoxic potential of NSO-heterocyclic compounds using zebrafish (Danio rerio). Reprod Toxicol 33: 224-232.
55. Sandrin TR, Chech AM, Maier RM (2000) A rhamnolipid biosurfactant reduces cadmium toxicity during biodegradation of naphthalene. Appl Environ Microbiol 66: 4585-4588.
56. Santos SCC, Alviano DS, Alviano CS, Padula M, Leitao AC, Martins OB, Ribeiro CMS, Sassaki MYM, Matta CPS, Bevilaqua J, Sebastian GV, Seldin L (2006) Characterization of Gordonia sp. strain F. 5. 25. 8 capable of dibenzothiophene desulfurization and carbazole utilization. Appl Microbiol Biotechnol 71: 355-362.
57. Schneider J, Grosser RJ, Jayasimhulu K, Xue W, Kinkle B, Warshawsky D (2000) Biodegradation of carbazole by Ralstonia sp. RJGII. 123 isolated from a hydrocarbon-contaminated soil. Can J Microbiol 46: 269-277.
58. Seo J-S, Keum Y-S, Cho IK, Li QX (2006) Degradation of dibenzothiophene and carbazole by Arthrobacter sp. p 1-1. Int Biodeterior Biodegrad 58: 36-43.
59. Shintani M, Fukushima N, Tezuka M, Yamane H, Nojiri H (2008) Conjugative transfer of the IncP-7 carbazole degradative plasmid, pCAR1, in river water samples. Biotechnol Lett 30: 117-122.
60. Shotbolt-Brown J, Hunter DWF, Aislabie J (1996) Isolation and description of carbazole-degrading bacteria. Can J Microbiol 42: 79-82.
61. Smith CJ, Hansch C (2000) The relative toxicity of compounds in mainstream cigarette smoke condensate. Food Chem Toxicol 38: 637-646.
62. Takagi T, Nojiri H, Yoshida T, Habe H, Omori T (2002) Detailed comparison between the substrate specificities of two angular dioxygenases, dibenzofuran 4, 4a-dioxygenase from Terrabacter sp. and carbazole 1, 9a-dioxygenase from Pseudomonas resinovorans. Biotechnol Lett 24: 2099-2106.
63. Vankateswaran K, Hoaki T, Kato M, Murayama T (1995) Microbial degradation of resins fractionated for Arabian light crude oil. Can J Microbiol 41: 418-424.
64. Vidali M (2001) Bioremediation. An overview. Pure Appl Chem 73: 1163-1172.
65. Wang B, Lai Q, Cui Z, Tan T, Shao Z (2008) A pyrene-degrading consortium from deep sea sediment of the West Pacific and its key member Cycloclasticus sp. P1. Environ Microbiol 10(8): 1948-1963.
66. Yoon B-J, Lee D-H, Kang Y-S, Oh D-C, Kim S-I, Oh K-H, Kahng H-Y (2002) Evaluation of carbazole degradation by Pseudomonas rhodesiae strain KK1 isolated from soil contaminated with coal tar. J Basic Microbiol 42: 434-443.