Biotransformation of indole by Cupriavidus sp. strain KK10 proceeds through N-heterocyclic- and carbocyclic-aromatic ring cleavage and production of indigoids

International Biodeterioration and Biodegradation

Volumn 97, Issue , 2015, Pages 13-24

  Fukuoka, Kimiko ^a   Tanaka, Keita ^a   Ozeki, Yasuhiro ^a   Kanaly, Robert A ^a  

^a YOKOHAMA CITY UNIVERSITY   (Japan)

Author keywords

Biotransformation; Cupriavidus; Indigo; Indirubin; Indole; LC ESI MS MS; Pyrrole 2,3 dicarboxylic acid

Indexed keywords

AROMATIC COMPOUNDS; BACTERIA; BIOCONVERSION; ELECTROSPRAY IONIZATION; FISSION PRODUCTS; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; POLLUTION; RNA; STRAIN;

BIOTRANSFORMATION; CUPRIAVIDUS; INDIGO; INDIRUBIN; INDOLE; LC/ESI-MS/MS;

POLYCYCLIC AROMATIC HYDROCARBONS;

BACTERIUM; BIOTRANSFORMATION; CARBOXYLIC ACID; CHEMICAL COMPOUND; GENE; NEW SPECIES; OXIDATION; PHYLOGENETICS; POLLUTANT; SOIL MICROORGANISM;

CUPRIAVIDUS;

EID: 84911865762     PISSN: 09648305     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ibiod.2014.11.007     Document Type: Article

References (55)

1. Alvarez D.A., Maruya K.A., Dodder N.G., Lao W., Furlong E.T., Smalling K.L. Occurrence of contaminants of emerging concern along the California coast (2009-2010) using passive sampling devices. Mar. Pollut. Bull. 2014, 81:347-354.
2. Atlas R.M. Handbook of Microbiological Media 1993, CRC Press, Boca Raton, FL.
3. Beier R.C., Anderson R.C., Krueger N.A., Edrington T.S., Callaway T.R., Nisbet D.J. Effect of nitroethane and nitroethanol on the production of indole and 3-methylindole (skatole) from bacteria in swine feces by gas chromatography. J.Environ. Sci. Health B 2009, 44:613-620.
4. Bell R., Carmeli S., Sar N. Vibrindole A, a metabolite of the marine bacterium, Vibrio parahaemolyticus, isolated from the toxic mucus of the boxfish Ostracion cubicus. J.Nat. Prod. 1994, 57:1587-1590.
5. Botalova O., Schwarzbauer J. Geochemical characterization of organic pollutants in effluents discharged from various industrial sources to riverine systems. Water Air Soil Pollut. 2011, 221:77-98.
6. Botalova O., Schwarzbauer J., Frauenrath T., Dsikowitzky L. Identification and chemical characterization of specific organic constituents of petrochemical effluents. Water Res. 2009, 43:3797-3812.
7. Céspedes C., Alarcon J., Valdez-Morales M., Paredes-Lopez O. Antioxidant activity of an unusual 3-hydroxyindole derivative isolated from fruits of Aristotelia chilensis (Molina) Stuntz. Z.Naturforsch. C 2009, 64:759-762.
8. Claus G., Kutzner H.J. Degradation of indole by Alcaligenes spec. Syst. Appl. Microbiol. 1983, 4:169-180.
9. Costa C., Bertazzo A., Allegri G., Catinella S., Traldi P. Electron impact mass spectrometric investigation of pyrrole mono-, di- and tri-carboxylic acids. Org. Mass Spectrom. 1991, 26:972-976.
10. d'Ischia M., Wakamatsu K., Napolitano A., Briganti S., Garcia-Borron J.C., Kovacs D., Meredith P., Pezzella A., Picardo M., Sarna T., Simon J.D., Ito S. Melanins and melanogenesis: methods, standards, protocols. Pigment Cell Melanoma Res. 2013, 26:616-633.
11. Doukyu N., Aono R. Biodegradation of indole at high concentration by persolvent fermentation with Pseudomonas sp. ST-200. Extremophiles 1997, 1:100-105.
12. Drewlo S., Brämer C.O., Madkour M., Mayer F., Steinbüchel A. Cloning and expression of a Ralstonia eutropha HF39 gene mediating indigo formation in Escherichia coli. Appl. Environ. Microbiol. 2001, 67:1964-1969.
13. Eaton R.W., Chapman P.J. Formation of indigo and related compounds from indolecarboxylic acids by aromatic acid-degrading bacteria: chromogenic reactions for cloning genes encoding dioxygenases that act on aromatic acids. J.Bacteriol. 1995, 177:6983-6988.
14. Ensley B.D., Ratzkin B.J., Osslund T.D., Simon M.J., Wackett L.P., Gibson D.T. Expression of naphthalene oxidation genes in Escherichia coli results in the biosynthesis of indigo. Science 1983, 222:167-169.
15. Evans C., Catinella S., Traldi P., Vettori U., Allegri G. Ion-trap mass spectrometry in ion structure studies. 1. Characterization of isomeric hydroxyindoles by electron ionization and energy-resolved collision-activated mass spectrometry. Rapid Commun. Mass Spectrom. 1990, 4:335-340.
16. Fabian J., Nakazumi H., Matsuoka M. Near-infrared absorbing dyes. Chem. Rev. 1992, 92:1197-1226.
17. Fetzner S. Bacterial degradation of pyridine, indole, quinoline, and their derivatives under different redox conditions. Appl. Microbiol. Biotechnol. 1998, 49:237-250.
18. Fujioka M., Wada H. The bacterial oxidation of indole. Biochim. Biophys. Acta (BBA) - General Subjects 1968, 158:70-78.
19. Gillam E.M., Notley L.M., Cai H., De Voss J.J., Guengerich F.P. Oxidation of indole by cytochrome P450 enzymes. Biochemistry (Mosc.) 2000, 39:13817-13824.
20. Guardado P., Balon M., Carmona C., Muñoz M.A., Domene C. Partition coefficients of indoles and betacarbolines. J.Pharm. Sci. 1997, 86:106-109.
21. Hamill R., Elander R., Mabe J., Gorman M. Metabolism of tryptophans by Pseudomonas aureofaciens. V. Conversion of tryptophan to pyrrolnitrin. Antimicrob. Agents Chemother. 1967, 7:388.
22. Han G.H., Gim G.H., Kim W., Seo S.I., Kim S.W. Enhanced indirubin production in recombinant Escherichia coli harboring a flavin-containing monooxygenase gene by cysteine supplementation. J.Biotechnol. 2012, 164:179-187.
23. Higashio Y., Shoji T. Heterocyclic compounds such as pyrrole, pyridines, pyrrolidine, piperidine, indole, imidazol and pyrazines. Appl. Catal. A: General 2004, 260:251-259.
24. Hoessel R., Leclerc S., Endicott J.A., Nobel M.E., Lawrie A., Tunnah P., Leost M., Damiens E., Marie D., Marko D. Indirubin, the active constituent of a Chinese antileukaemia medicine, inhibits cyclin-dependent kinases. Nat. Cell Biol. 1999, 1:60-67.
25. 14C] benzo[a]pyrene added in crude oil to uncontaminated soil. Appl. Environ. Microbiol. 1997, 63:4511-4515.
26. Kanaly R.A., Bartha R., Watanabe K., Harayama S. Rapid mineralization of benzo[a]pyrene by a microbial consortium growing on diesel fuel. Appl. Environ. Microbiol. 2000, 66:4205-4211.
27. Kanaly R.A., Manzanero L.I., Foley G., Panneerselvam S., Macer D. Energy Flow, Environment and Ethical Implications for Meat Production 2010, UNESCO, Bangkok.
28. Kanaly R.A., Watanabe K. Multiple mechanisms contribute to the biodegradation of benzo[a]pyrene by petroleum-derived multicomponent nonaqueous-phase liquids. Environ. Toxicol. Chem. 2004, 23:850-856.
29. Keil H., Saint C., Williams P. Gene organization of the first catabolic operon of TOL plasmid pWW53: production of indigo by the xylA gene product. J.Bacteriol. 1987, 169:764-770.
30. Kunihiro M., Ozeki Y., Nogi Y., Hamamura N., Kanaly R.A. Benz[a]anthracene biotransformation and production of ring fission products by Sphingobium sp. strain KK22. Appl. Environ. Microbiol. 2013, 79:4410-4420.
31. Lathourakis G.E., Litinas K.E. Synthesis and study of 3-(triphenylphosphoranylidene)-2, 3-dihydro-1H-indol-2-one. J.Chem. Soc. Perkin Trans. 1996, 1:491-493.
32. Maeda A.H., Nishi S., Hatada Y., Ozeki Y., Kanaly R.A. Biotransformation of the high-molecular-weight polycyclic aromatic hydrocarbon (PAH) benzo[k]fluoranthene by Sphingobium sp. strain KK22 and identification of new products of non-alternant PAH biodegradation by liquid chromatography electrospray ionization tandem mass spectrometry. Microb. Biotechnol. 2014, 7:114-129.
33. Makkar N., Casida L. Cupriavidus necator gen. nov., sp. nov.; a nonobligate bacterial predator of bacteria in soil. Int. J. Syst. Bacteriol. 1987, 37:323-326.
34. McClay K., Boss C., Keresztes I., Steffan R.J. Mutations of toluene-4-monooxygenase that alter regiospecificity of indole oxidation and lead to production of novel indigoid pigments. Appl. Environ. Microbiol. 2005, 71:5476-5483.
35. Mermod N., Harayama S., Timmis K. New route to bacterial production of indigo. Nat. Biotechnol. 1986, 4:321-324.
36. Meyer A., Würsten M., Schmid A., Kohler H.-P.E., Witholt B. Hydroxylation of indole by laboratory-evolved 2-hydroxybiphenyl 3-monooxygenase. J.Biol. Chem. 2002, 277:34161-34167.
37. Mohn T., Plitzko I., Hamburger M. Acomprehensive metabolite profiling of Isatis tinctoria leaf extracts. Phytochemistry 2009, 70:924-934.
38. Moody J.D., Freeman J.P., Doerge D.R., Cerniglia C.E. Degradation of phenanthrene and anthracene by cell suspensions of Mycobacterium sp. strain PYR-1. Appl. Environ. Microbiol. 2001, 67:1476-1483.
39. Mushrush G.W., Beal E.J., Hardy D.R., Hughes J.M. Nitrogen compound distribution in middle distillate fuels derived from petroleum, oil shale, and tar sand sources. Fuel Process Technol. 1999, 61:197-210.
40. Pérez-Pantoja D., De la Iglesia R., Pieper D.H., Gonzalez B. Metabolic reconstruction of aromatic compounds degradation from the genome of the amazing pollutant-degrading bacterium Cupriavidus necator JMP134. FEMS Microbiol. Rev. 2008, 32:736-794.
41. Powers J.C. Mass spectrometry of simple indoles. J.Org. Chem. 1968, 33:2044-2050.
42. Puchalska M., Połeć-Pawlak K., Zadrozna I., Hryszko H., Jarosz M. Identification of indigoid dyes in natural organic pigments used in historical art objects by high-performance liquid chromatography coupled to electrospray ionization mass spectrometry. J.Mass Spectrom. 2004, 39:1441-1449.
43. Qu Y., Xu B., Zhang X., Ma Q., Zhou H., Kong C., Zhang Z., Zhou J. Biotransformation of indole by whole cells of recombinant biphenyl dioxygenase and biphenyl-2,3-dihydrodiol-2,3-dehydrogenase. Biochem. Eng. J. 2013, 72:54-60.
44. Rodríguez J.G., Urrutia A., Canoira L. Electron impact mass spectrometry of oxindole, pseudoindoxyle and indolenine derivatives. Int. J. Mass Spectrom. Ion Process. 1997, 161:113-122.
45. Rui L., Reardon K.F., Wood T.K. Protein engineering of toluene ortho-monooxygenase of Burkholderia cepacia G4 for regiospecific hydroxylation of indole to form various indigoid compounds. Appl. Microbiol. Biotechnol. 2005, 66:422-429.
46. Sadler P. Ultra-violet and infra-red spectra of substituted isoindigos and indirubins. Spectrochim. Acta 1960, 16:1094-1099.
47. Sakamoto Y., Uchida M., Ichihara K. The bacterial decomposition of indole. I. Studies on its metabolic pathway by successive adaptation. Med. J. Osaka Univ. 1953, 3:477-486.
48. Schüssler W., Nitschke L. Death of fish due to surface water pollution by liquid manure or untreated wastewater: analytical preservation of evidence by HPLC. Water Res. 1999, 33:2884-2887.
49. Stull T.L., Hyun L., Sharetzsky C., Wooten J., McCauley J.P., Smith A.B. Production and oxidation of indole by Haemophilus influenzae. J.Biol. Chem. 1995, 270:5-8.
50. Trabue S., Scoggin K., McConnell L., Maghirang R., Razote E., Hatfield J. Identifying and tracking key odorants from cattle feedlots. Atmos. Environ. 2011, 45:4243-4251.
51. Ward W.C., Lamb E.C., Gooden D., Chen X., Burinsky D.J., Simon J.D. Quantification of naturally occurring pyrrole acids in melanosomes. Photochem. Photobiol. 2008, 84:700-705.
52. Xu X., Zhang J., Zhang L., Liu W., Weisel C.P. Selective detection of monohydroxy metabolites of polycyclic aromatic hydrocarbons in urine using liquid chromatography/triple quadrupole tandem mass spectrometry. Rapid Commun. Mass Spectrom. 2004, 18:2299-2308.
53. Yager T.J.B., Furlong E.T., Kolpin D.W., Kinney C.A., Zaugg S.D., Burkhardt M.R. Dissipation of contaminants of emerging concern in biosolids applied to nonirrigated farmland in eastern Colorado. J.Am. Water Resour. Assoc. 2014, 50:343-357.
54. Yasuhara A. Identification of volatile compounds in poultry manure by gas chromatography-mass spectrometry. J.Chromatogr. 1987, 387:371-378.
55. Zou P., Koh H.L. Determination of indican, isatin, indirubin and indigotin in Isatis indigotica by liquid chromatography/electrospray ionization tandem mass spectrometry. Rapid Commun. Mass Spectrom. 2007, 21:1239-1246.