The potential application of carbazole-degrading bacteria for dioxin bioremediation

Abstract

Extensive research has been conducted over the years on the bacterial degradation of dioxins and their related compounds including carbazole, because these chemicals are highly toxic and has been widely distributed in the environment. There is a pressing need to explore and develop more bacterial strains with unique catabolic features to effectively remediate dioxin-polluted sites. Carbazole has a chemical structure similar to dioxins, and the degradation pathways of these two chemicals are highly homologous. Some carbazole-degrading bacterial strains have been demonstrated to have the ability to degrade dioxins, such as Pseudomonas sp. strain CA10 và Sphingomonas sp. KA1. The introduction of strain KA1 into dioxin-contaminated model soil resulted in the degradation of 96% and 70% of 2-chlorodibenzo-p-dioxin (2-CDD) and 2,3-dichlorodibenzo-p-dioxin (2,3-DCDD), respectively, after 7-day incubation period. These degradation rates were similar to those achieved with strain CA10, which removed 96% of 2-CDD and 80% of 2,3-DCDD from the same model soil. Therefore, carbazole-degrading bacteria hold significant promise as potential candidates for dioxin bioremediation. This paper overviews the connection between the bacterial degradation of dioxins and carbazole, highlighting the potential for dioxin biodegradation by carbazole-degrading bacterial strains.

Keywords

Angular dioxygenation / Bacterial degradation / Carbazole / Dioxins

References

[1] Armengaud J, Timmis KN. Biodegradation of dibenzo-p-dioxin and dibenzofuran by bacteria. J Microbiol, 1997, 35: 241-252.

[2] Ashikawa FY, Noguchi H, Habe H, Omori T, Yamane H, Nojiri H. Crystallization and preliminary X-ray diffraction analysis of the electron-transfer complex between the terminal oxygenase component and ferredoxin in the Rieske non-haem iron oxygenase system carbazole 1,9a-dioxygenase. Acta Crystallograph Sect F Struct Biol Cryst Commun, 2005, 61: 577-580.

[3] Bedard DL. A case study for microbial biodegradation: anaerobic bacterial reductive dechlorination of polychlorinated biphenyls-from sediment to defined medium. Ann Rev Microbiol, 2008, 62: 253-270.

[4] Bertazzi PA, Bernucci I, Brambilla G, Consonni D, Pesatori AC. The Seveso studies on early and long-term effects of dioxin exposure: a review. Environ Health Perspect, 1998, 106(Suppl 2): 625-633.

[5] Bertazzi PA, Consonni D, Bachetti S, Rubagotti M, Baccarelli A, Zocchetti C, Pesatori AC. Health effects of dioxin exposure: a 20-year mortality study. Am J Epidemiol, 2001, 153: 1031-1044.

[6] Bressler DC, Fedorak PM. Bacterial metabolism of fluorene, dibenzofuran, dibenzothiophene, and carbazole. Can J Microbiol, 2000, 46: 397-409.

[7] Chen WY, Wu JH, Lin SC, Chang JE. Bioremediation of polychlorinated-p dioxins/dibenzofurans contaminated soil using simulated compost amended landfill reactors under hypoxic conditions. J Hazard Mater, 2016, 312: 159-168.

[8] Field JA, Sierra-Alvarez R. Microbial degradation of chlorinated dioxins. Chemosphere, 2008, 71: 1005-1018.

[9] Fortnagel P, Harms H, Wittich RM, Krohn S, Meyer H, Sinnwell V, Wilkes H, Francke W. Metabolism of dibenzofuran by Pseudomonas sp. strain HH69 and the mixed culture HH27. Appl Environ Microbiol, 1990, 56: 1148-1156.

[10] Gai Z, Yu B, Li L, Wang Y, Ma C, Feng J, Deng Z, Xu P. Cometabolic degradation of dibenzofuran and dibenzothiophene by a newly isolated carbazole-degrading Sphingomonas sp. strain. Appl Environ Microbiol, 2007, 73: 2832-2838.

[11] Gai Z, Wang X, Liu X, Tai C, Tang H, He X, Wu G, Deng Z, Xu P. The genes coding for the conversion of carbazole to catechol are flanked by IS6100 elements in Sphingomonas sp. strain XLDN2-5. PLoS ONE, 2010, 5(4): e10018.

[12] Gai Z, Wang X, Tang H, Tai C, Tao F, Wu G, Xu P. Genome sequence of Sphingobium yanoikuyae XLDN2-5, an efficient carbazole-degrading strain. J Bacteriol, 2011, 193: 6404-6405.

[13] Gibbs PR, Riddle RR, Marchal L, Benedik MJ, Willson RC. Purification and characterization of 2′aminobiphenyl-2,3-diol 1,2-dioxygenase from Pseudomonas sp. LD2. Protein Expr Purif, 2003, 32: 35-43.

[14] Habe H, Chung JS, Lee JH, Kasuga K, Yoshida T, Nojiri H, Omori T. Degradation of chlorinated dibenzofurans and dibenzo-p-dioxins by two types of bacteria having angular dioxygenases with different features. Appl Environ Microbiol, 2001, 67: 3610-3617.

[15] Habe H, Ashikawa Y, Saiki Y, Yoshida T, Nojiri H, Omori T. Sphingomonas sp. strain KA1, carrying a carbazole dioxygenase gene homologue, degrades chlorinated dibenzo-p-dioxins in soil. FEMS Microbiol Lett, 2002, 211: 43-49.

[16] Halden RU, Dwyer DF, Halden RU, Dwyer DF. Biodegradation of dioxin-related compounds: a review. Bioremediat J, 2008, 1: 11-25.

[17] Hay A. Dioxin: the 10-year battle that began with agent orange. Nature, 1979, 278: 108-109.

[18] Hiraishi A. Biodiversity of dioxin-degrading microorganisms and potential utilization in bioremediation. Microbes Environ, 2003, 18: 105-125.

[19] Hoekstra EJ, de Weerd H, de Leer EW, Brinkman UAT. Natural formation of chlorinated phenols, dibenzo-p-dioxins, and dibenzofurans in soil of a Douglas fir forest. Environ Sci Technol, 1999, 33: 2543-2549.

[20] Inoue K, Widada J, Nakai S, Endoh T, Urata M, Ashikawa Y, Shintani M, Saiki Y, Yoshida T, Habe H, Omori T, Nojiri H. Divergent structures of carbazole degradative car operons isolated from Gram-negative bacteria. Biosci Biotechnol Biochem, 2004, 68: 1467-1480.

[21] Inoue K, Habe H, Yamane H, Omori T, Nojiri H. Diversity of carbazole-degrading bacteria having the car gene cluster: isolation of a novel gram-positive carbazole-degrading bacterium. FEMS Microbiol Lett, 2005, 245: 145-153.

[22] Inoue K, Habe H, Yamane H, Nojiri H. Characterization of novel carbazole catabolism genes from gram-positive carbazole degrader Nocardioides aromaticivorans IC177. Appl Environ Microbiol, 2006, 72: 3321-3329.

[23] Ito Y, Maeda R, Iwata K, Omori T. Genetic characterisation of genes involved in the upper pathway of carbazole metabolism from the putative Kordiimonas sp. Biotechnol Lett, 2011, 33: 1859-1864.

[24] Jaiswal PK, Kohli S, Gopal M, Thakur IS. Isolation and characterization of alkalo tolerant Pseudomonas sp. strain ISTDF1 for degradation of dibenzofuran. J Ind Microbiol Biotechnol, 2011, 38: 503-511.

[25] Jha AM, Bharti MK. Mutagenic profiles of carbazole in the male germ cells of Swiss albino mice. Mutat Res Fundam Mol Mech Mutagen, 2002, 500: 97-101.

[26] Jha AM, Singh AC, Bharti MK. Clastogenicity of carbazole in mouse bone marrow cells in vivo. Mutat Res, 2002, 521: 11-17.

[27] Kearny PC, Woolson EA, Ellington CP Jr. Persistence and metabolism of chlorodioxins in soils. Environ Sci Technol, 1972, 6: 1017-1019.

[28] Kilbane JJ II, Daram A, Abbasian J, Kayser KJ. Isolation and characterization of Sphingomonas sp. GTIN11 capable of carbazole metabolism in petroleum. Biochem Biophys Res Commun, 2002, 297: 242-248.

[29] Klees M, Hiester E, Bruckmann P, Molt K, Schmidt TC. Polychlorinated biphenyls, polychlorinated dibenzo-p-dioxins and dibenzofurans in street dust of North Rhine-Westphalia, Germany. Sci Total Environ, 2015, 511: 72-81.

[30] Kobayashi S, Hayaishi O. Anthranilic acid conversion to catechol (Pseudomonas). Methods Enzymol, 1970, 17A: 505-510.

[31] Kubota M, Kawahara K, Sekiya K, Uchida T, Hattori Y, Futamata H, Hiraishi A. Nocardioides aromaticivorans sp. nov., a dibenzofuran-degrading bacterium isolated from dioxin-polluted environments. Syst Appl Microbiol, 2005, 28: 165-174.

[32] Kulkarni PS, Crespo JG, Afonso CAM. Dioxins sources and current remediation technologies—a review. Environ Int, 2008, 34: 139-153.

[33] Le TT, Murugesan K, Nam IH, Jeon JR, Chang YS. Degradation of dibenzofuran via multiple dioxygenation by a newly isolated Agrobacterium sp. PH-08. J Appl Microbiol, 2014, 116: 542-553.

[34] Li Q, Wang X, Yin G, Gai Z, Tang H, Ma C, Deng Z, Xu P. New metabolites in dibenzofuran cometabolic degradation by a biphenyl-cultivated Pseudomonas putida strain B6–2. Environ Sci Technol, 2009, 43: 8635-8642.

[35] Lin X, Yan M, Dai A, Zhan M, Fu J, Li X, Yan J. Simultaneous suppression of PCDD/F and NOx during municipal solid waste incineration. Chemosphere, 2015, 126: 60-66.

[36] Lin JL, Lin WC, Liu JK, Surampalli RY, Zhang TC, Kao CM. Aerobic biodegradation of OCDD by P. mendocina NSYSU: effectiveness and gene inducement studies. Water Environ Res, 2017, 89: 2113-2121.

[37] Liu X, Wang J, Wang X, Zhu T. Simultaneous removal of PCDD/Fs and NOx from the flue gas of a municipal solid waste incinerator with a pilot plant. Chemosphere, 2015, 133: 90-96.

[38] Maddalwar S, Nayak KK, Kumar M, Singh L. Plant microbial fuel cell: Opportunities, challenges, and prospects. Bioresour Technol, 2021, 341: 125772.

[39] Maeda R, Nagashima H, Zulkharnain AB, Iwata K, Omori T. Isolation and characterization of a car gene cluster from the naphthalene, phenanthrene, and carbazole-degrading marine isolate Lysobacter sp. strain OC7. Curr Microbiol, 2009, 59: 154-159.

[40] Maeda R, Ishii T, Ito Y, Zulkharnain AB, Iwata K, Omori T. Isolation and characterization of the gene encoding the chloroplast-type ferredoxin component of carbazole 1,9a-dioxygenase from a putative Kordiimonas sp. Biotechnol Lett, 2010, 32: 1725-1731.

[41] Maeda R, Ito Y, Iwata K, Omori T. Comparison of marine and terrestrial carbazole-degrading bacteria. Curr Res Technol Educ Top Appl Microbiol Microb Biotechnol, 2010, 2: 1311-1321.

[42] Murata T, Ohnishi M, Ara T, Kaneko J, Han CG, Li YF, Takashima K, Nojima H, Nakayama K, Kaji A, Kamio Y, Miki T, Mori H, Ohtsubo E, Terawaki Y, Hayashi T. Complete nucleotide sequence of plasmid Rts1: implications for evolution of large plasmid genomes. J Bacteriol, 2002, 184: 3194-3202.

[43] Nagashima H, Zulkharnain AB, Maeda R, Fuse H, Iwata K, Omori T. Cloning and nucleotide sequences of carbazole degradation genes from marine bacterium Neptuniibacter sp. strain CAR-SF. Curr Microbiol, 2010, 61: 50-56.

[44] Nam J, Nojiri H, Noguchi H, Uchimura H, Yoshida T, Habe H, Yamane H, Omori T. Purification and characterization of carbazole 1,9a-dioxygenase, a three-component dioxygenase system of Pseudomonas resinovorans strain CA10. Appl Environ Microbiol, 2002, 68: 5882-5890.

[45] Nam I, Hong H, Kim Y, Kim B, Murugesan K, Chang YS. Biological removal of polychlorinated dibenzo-p-dioxins from incinerator fly ash by Sphingomonas wittichii RW1. Water Res, 2005, 39: 4651-4660.

[46] Nguyen DB, Nguyen TKO, Parkpian P. Photodegradation of dioxin in contaminated soil in the presence of solvents and nanoscale TiO₂ particles. Environ Technol, 2014, 15(9): 1121-1132.

[47] Nguyen THN, Nguyen XTT, Vo DL, Wei Y, Fujita T. A review of soil contaminated with dioxins and biodegradation technologies: current status and future prospects. Toxics, 2022, 10(6): 278.

[48] Nojiri H. Structural and molecular genetic analyses of the bacterial carbazole degradation system. Biosci Biotechnol Biochem, 2012, 76(1): 1-18.

[49] Nojiri H, Omori T. Molecular bases of aerobic bacterial degradation of dioxins: Involvement of angular deoxygenation. Biosci Biotech Biochem, 2002, 66: 2001-2016.

[50] Nojiri H, Omori T. Ramos J-L, Filloux A. Carbazole metabolism by Pseudomonads. Pseudomonas, 2007, New York: Springer, 107-145.

[51] Nojiri H, Nam JW, Kosaka M, Morii KI, Takemura T, Furihata K, Yamane H, Omori T. Diverse oxygenations catalyzed by carbazole 1,9a-dioxygenase from Pseudomonas sp. strain CA10. J Bacteriol, 1999, 181: 3105-3113.

[52] Nojiri H, Habe H, Omori T. Bacterial degradation of aromatic compounds via angular dioxygenation. J Gen Appl Microbiol, 2001, 47: 279-305.

[53] Nojiri H, Maeda K, Sekiguchi H, Urata M, Shintani M, Yoshida T, Habe H, Omori T. Organization and transcriptional characterization of catechol degradation genes involved in carbazole degradation by Pseudomonas resinovorans strain CA10. Biosci Biotechnol Biochem, 2002, 66: 897-901.

[54] Nojiri H, Taira H, Iwata K, Morii K, Nam JW, Yoshida T, Habe H, Nakamura S, Shimizu K, Yamane H, Omori T. Purification and characterization of meta-cleavage hydrolase from carbazole degrader Pseudomonas resinovorans strain CA10. Biosci Biotechnol Biochem, 2003, 67: 36-45.

[55] Oba S, Suzuki T, Maeda R, Omori T, Fuse H. Characterization and genetic analyses of a carbazole-degrading gram-positive marine isolate, Janibacter sp. strain OC11. Biosci Biotechnol Biochem, 2014, 78: 1094-1101.

[56] Odabasi M, Cetin B, Sofuoglu A. Henry’s law constant, octanol-air partition coefficient and super cooled liquid vapour pressure of carbazole as a function of temperature: application to gas/particle partitioning in the atmosphere. Chemosphere, 2006, 62: 1087-1096.

[57] Ouchiyama N, Zhang Y, Omori T, Kodama T. Biodegradation of Carbazole by Pseudomonas spp. CA06 and CA10. Biosci Biotechnol Biochem, 1993, 57: 455-460.

[58] Ouchiyama N, Miyachi S, Omori T. Cloning and nucleotide sequence of carbazole catabolic genes from Pseudomonas stutzeri strain OM1, isolated from activated sludge. J Gen Appl Microbiol, 1998, 44: 57-63.

[59] Palanisami N, Chung SJ, Moon IS. Cerium(IV)-mediated electrochemical oxidation process for removal of polychlorinated dibenzo-p-dioxins and dibenzofurans. J Ind Eng Chem, 2015, 28: 28-31.

[60] Peng P, Yang H, Jia R, Li L. Biodegradation of dioxin by a newly isolated Rhodococcus sp. with the involvement of self-transmissible plasmids. Appl Microbiol Biotechnol, 2013, 97: 5585-5595.

[61] Romine MF, Stillwell LC, Wong KK, Thurston SJ, Sisk EC, Sensen C, Gaasterland T, Fredrickson JK, Saffer JD. Complete sequence of a 184- kilobase catabolic plasmid from Sphingomonas aromaticivorans F199. J Bacteriol, 1999, 181: 1585-1602.

[62] Saibu S, Adebusoye SA, Oyetibo G. Aerobic bacterial transformation and biodegradation of dioxins: a review. Bioresour Bioprocess, 2020, 7: 7.

[63] Salam LB, Ilori MO, Amund OO. Properties, environmental fate and biodegradation of carbazole. Biotech, 2017, 7: 111.

[64] Sato S, Nam JW, Kasuga K, Nojiri H, Yamane H, Omori T. Identification and characterization of genes encoding carbazole 1,9a-dioxygenase in Pseudomonas sp. strain CA 10. J Bacteriol, 1997, 179: 4850-4858.

[65] Sato S, Ouchiyama N, Kimura T, Nojiri H, Yamane H, Omori T. Cloning of genes involved in carbazole degradation of Pseudomonas sp. strain CA10: nucleotide sequences of genes and characterization of meta-cleavage enzymes and hydrolase. J Bacteriol, 1997, 179: 4841-4849.

[66] Sauber K, Fröhner C, Rosenberg G, Eberspächer J, Lingens F. Purification and properties of pyrazon dioxygenase from pyrazon-degrading bacteria. Eur J Biochem, 1977, 74: 89-97.

[67] Seo JS, Keum YS, Li QX. Bacterial degradation of aromatic compounds. Int J Environ Res Public Health, 2009, 6: 278-309.

[68] Shepherd JM, Lloyd-Jones G. Novel carbazole degradation genes of Sphingomonas CB3: sequence analysis, transcription, and molecular ecology. Biochem Biophys Res Commun, 1998, 247: 129-135.

[69] Sherburne CK, Lawley TD, Gilmour MW, Blattner FR, Burland V, Grotbeck E, Rose DJ, Taylor DE. The complete DNA sequence and analysis of R27, a large IncHI plasmid from Salmonella typhi that is temperature sensitive for transfer. Nucleic Acids Res, 2000, 28: 2177-2186.

[70] Shintani M, Nojiri H, Yoshida T, Habe H, Omori T. Carbazole/dioxin - degrading car gene cluster is located on the chromosome of Pseudomonas stutzeri strain OM1 in a form different from the simple transposition of Tn4676. Biotechnol Lett, 2003, 25: 1255-1261.

[71] Shintani M, Habe H, Tsuda M, Omori T, Yamane H, Nojiri H. Recipient range of IncP-7 conjugative plasmid pCAR2 from Pseudomonas putida HS01 is broader than from other Pseudomonas strains. Biotechnol Lett, 2005, 27: 1847-1853.

[72] Shintani M, Urata M, Inoue K, Eto K, Habe H, Omori T, Yamane H, Nojiri H. The Sphingomonas plasmid pCAR3 is involved in complete mineralization of carbazole. J Bacteriol, 2007, 189: 2007-2020.

[73] Takagi T, Nojiri H, Yoshida T, Habe H, Omori T. 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, 2002, 24: 2099-2106.

[74] Tue NM, Goto A, Takahashi S, Itai T, Asante KA, Kunisue T, Tanabe S. Release of chlorinated, brominated and mixed halogenated dioxin related compounds to soils from open burning of e-waste in Agbogbloshie (Accra, Ghana). J Hazard Mater, 2016, 302: 151-157.

[75] Ulbrich B, Stahlmann R. Developmental toxicity of polychlorinated biphenyls (PCBs): a systematic review of experimental data. Arch Toxicol, 2004, 78: 252-268.

[76] Urata M, Uchimura H, Noguchi H, Sakaguchi T, Takemura T, Eto K, Habe H, Omori T, Yamane H, Nojiri H. Plasmid pCAR3 contains multiple gene sets involved in the conversion of carbazole to anthranilate. Appl Environ Microbiol, 2006, 72: 3198-3205.

[77] Vejarano F, Suzuki-Minakuchi C, Ohtsubo Y, Tsuda M, Okada K, Nojiri H. Complete genome sequence of the marine carbazole-degrading bacterium Erythrobacter sp. Strain KY5. Microbiol Resour Announc, 2018, 7: e00935-e1018.

[78] Vejarano F, Suzuki-Minakuchi C, Ohtsubo Y, Tsuda M, Okada K, Nojiri H. Complete genome sequence of Thalassococcus sp. strain S3, a Marine Roseobacter clade member capable of degrading carbazole. Microbiol Resour Announc, 2019, 8: e00231-e319.

[79] Ward CT, Matsumura F. Fate of 2,3,7,8-tetrachlorodi- benzo-p-dioxin (TCDD) in a model aquatic environment. Arch Environ Contam Toxicol, 1978, 7: 349-357.

[80] White SS, Birnbaum LS. An overview of the effects of dioxins and dioxin-like compounds on vertebrates, as documented in human and ecological epidemiology. J Environ Sci Health C Environ Carciong Ecotoxicol Rev, 2009, 27: 197-211.

[81] Wittich RM. Degradation of dioxin-like compounds by microorganisms. Appl Microbiol Biotechnol, 1998, 49: 489-499.

[82] Wittich RM, Wilkes H, Sinnwell V, Francke W, Fortnagel P. Metabolism of dibenzo-p-dioxin by Sphingomonas sp. strain RW1. Appl Environ Microbiol, 1992, 58: 1005-1010.

[83] Xu P, Yu B, Li FL, Cai XF, Ma CQ. Microbial degradation of sulfur, nitrogen and oxygen heterocycles. Trends Microbiol, 2006, 14: 398-405.