Skip to main content
PMC home page
Indian Journal of Microbiology logoLink to Indian Journal of Microbiology
. 2008 May 1;48(1):19–34. doi: 10.1007/s12088-008-0003-8

Bacterial degradation of phthalate isomers and their esters

C Vamsee-Krishna 1, Prashant S Phale 1,✉
PMCID: PMC3450200  PMID: 23100697

Abstract

Phthalate isomers and their esters are used heavily in various industries. Excess use and leaching from the product pose them as major pollutants. These chemicals are toxic, teratogenic, mutagenic and carcinogenic in nature. Various aspects like toxicity, diversity in the aerobic bacterial degradation, enzymes and genetic organization of the metabolic pathways from various bacterial strains are reviewed here. Degradation of these esters proceeds by the action of esterases to form phthalate isomers, which are converted to dihydroxylated intermediates by specific and inducible phthalate isomer dioxygenases. Metabolic pathways of phthalate isomers converge at 3,4-dihydroxybenzoic acid, which undergoes either ortho- or meta- ring cleavage and subsequently metabolized to the central carbon pathway intermediates. The genes involved in the degradation are arranged in operons present either on plasmid or chromosome or both, and induced by specific phthalate isomer. Understanding metabolic pathways, diversity and their genetic regulation may help in constructing bacterial strains through genetic engineering approach for effective bioremediation and environmental clean up.

Keywords: Phthalate esters, Toxicity, Biodegradation, Dioxygenases, Genetic regulation

Full Text

The Full Text of this article is available as a PDF (214.9 KB).

References

  • 1.Akita K., Naitou C., Maruyama K. Purification and characterization of an esterase from Micrococcus sp. YGJ1 hydrolyzing phthalate esters. Biosci Biotechnol Biochem. 2001;65:1680–1683. doi: 10.1271/bbb.65.1680. [DOI] [PubMed] [Google Scholar]
  • 2.Autian J. Toxicity and health threats of phthalate esters: review of the literature. Environ Health Perspect. 1973;4:3–26. doi: 10.2307/3428178. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3.Batie C.J., Ballou D.P. Phthalate dioxygenase Methods. Enzymol. 1990;188:61–70. doi: 10.1016/0076-6879(90)88013-Z. [DOI] [PubMed] [Google Scholar]
  • 4.Batie C.J., LaHaie E., Ballou D.P. Purification and characterization of phthalate oxygenase and phthalate oxygenase reductase from Pseudomonas cepacia. J Biol Chem. 1987;262:1510–1518. [PubMed] [Google Scholar]
  • 5.Bull C., Ballou D.P. Purification and properties of protocatechuate 3,4-dioxygenase from Pseudomonas putida. A new iron to subunit stoichiometry. J Biol Chem. 1981;256:12673–12680. [PubMed] [Google Scholar]
  • 6.Cartwright C.D., Owen S.A., Thompson I.P., Burns R.G. Biodegradation of diethyl phthalate in soil by a novel pathway FEMS. Microbiol Lett. 2000;186:27–34. doi: 10.1111/j.1574-6968.2000.tb09077.x. [DOI] [PubMed] [Google Scholar]
  • 7.Caughey W.S., Hellerman L., Smiley J.D. L-glutamic acid dehydrogenase; structural requirements for substrate competition; effect of thyroxine. J Biol Chem. 1957;224:591–607. [PubMed] [Google Scholar]
  • 8.Chang B.V., Liao C.S., Yuan S.Y. Anaerobic degradation of diethyl phthalate, di-n-butyl phthalate, and di-(2-ethylhexyl) phthalate from river sediment in Taiwan. Chemosphere. 2005;58:1601–1607. doi: 10.1016/j.chemosphere.2004.11.031. [DOI] [PubMed] [Google Scholar]
  • 9.Chang B.V., Liao G.S., Yuan S.Y. Anaerobic degradation of di-n-butyl phthalate and di-(2-ethylhexyl) phthalate in sludge. Bull Environ Contam Toxicol. 2005;75:775–782. doi: 10.1007/s00128-005-0818-5. [DOI] [PubMed] [Google Scholar]
  • 10.Chang B.V., Yang C.M., Cheng C.H., Yuan S.Y. Biodegradation of phthalate esters by two bacteria strains. Chemosphere. 2004;55:533–538. doi: 10.1016/j.chemosphere.2003.11.057. [DOI] [PubMed] [Google Scholar]
  • 11.Chang H.K., Zylstra G.J. Novel organization of the genes for phthalate degradation from Burkholderia cepacia DBO1. J Bacteriol. 1998;180:6529–6537. doi: 10.1128/jb.180.24.6529-6537.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 12.Chang H.K., Zylstra G.J. Characterization of the phthalate permease OphD from Burkholderia cepacia ATCC 17616. J Bacteriol. 1999;181:6197–6199. doi: 10.1128/jb.181.19.6197-6199.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13.Chang H.K., Zylstra G.J. Role of quinolinate phosphoribosyl transferase in degradation of phthalate by Burkholderia cepacia. DBO1 J Bacteriol. 1999;181:3069–3075. doi: 10.1128/jb.181.10.3069-3075.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 14.Chatterjee S., Dutta T.K. Metabolism of butyl benzyl phthalate by Gordonia sp. strain MTCC 4818. Biochem Biophys Res Commun. 2003;309:36–43. doi: 10.1016/S0006-291X(03)01513-4. [DOI] [PubMed] [Google Scholar]
  • 15.Choi K.Y., Kim D., Chae J.C., Zylstra G.J., Kim E. Requirement of duplicated operons for maximal metabolism of phthalate by Rhodococcus sp. strain DK17. Biochem Biophys Res Commun. 2007;357:766–771. doi: 10.1016/j.bbrc.2007.04.009. [DOI] [PubMed] [Google Scholar]
  • 16.Choi K.Y., Kim D., Sul W.J., Chae J.C., Zylstra G.J., Kim Y.M., Kim E. Molecular and biochemical analysis of phthalate and terephthalate degradation by Rhodococcus sp. strain DK17. FEMS Microbiol Lett. 2005;252:207–213. doi: 10.1016/j.femsle.2005.08.045. [DOI] [PubMed] [Google Scholar]
  • 17.Colborn T., Saal F.S., Soto A.M. Developmental effects of endocrine-disrupting chemicals in wildlife and humans. Environ Health Perspect. 1993;101:378–384. doi: 10.2307/3431890. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 18.Correll C.C., Batie C.J., Ballou D.P., Ludwig M.L. Phthalate dioxygenase reductase: a modular structure for electron transfer from pyridine nucleotides to [2Fe-2S] Science. 1992;258:1604–1610. doi: 10.1126/science.1280857. [DOI] [PubMed] [Google Scholar]
  • 19.Cunliffe D., Leason M., Parkin D., Lea P.J. The inhibition of glutamate dehydrogenase by derivatives of isophthalic acid. Phytochemistry. 1983;22:1357–1360. doi: 10.1016/S0031-9422(00)84014-5. [DOI] [Google Scholar]
  • 20.Dai G., Cui L., Song L., Cheng J., Zhong Y., Zhao R., Wang X. Bladder epithelial cell proliferation of rats induced by terephthalic acid-calculi. Food Chem Toxicol. 2005;43:217–224. doi: 10.1016/j.fct.2004.09.017. [DOI] [PubMed] [Google Scholar]
  • 21.Dai G.D., Cui L.B., Song L., Zhao R.Z., Cheng J.F., Liu M.X., Zhou J.W., Xiao H., Wang X.R. Induction of bladder lesion by terephthalic acid and its mechanism. Biomed Environ Sci. 2005;18:211–219. [PubMed] [Google Scholar]
  • 22.Den H.E., Schoeters G. Endocrine disrupters and human puberty. Int J Androl. 2006;29:264–271. doi: 10.1111/j.1365-2605.2005.00561.x. [DOI] [PubMed] [Google Scholar]
  • 23.Deveryshetty J., Suvekbala V., Varadamshetty G., Phale P.S. Metabolism of 2-, 3-and 4-hydroxybenzoates by soil isolates Alcaligenes sp. strain PPH and Pseudomonas sp. strain PPD. FEMS Microbiol Lett. 2007;268:59–66. doi: 10.1111/j.1574-6968.2006.00561.x. [DOI] [PubMed] [Google Scholar]
  • 24.Dillingham E.O., Autian J. Teratogenicity, mutagenicity, and cellular toxicity of phthalate esters. Environ Health Perspect. 1973;3:81–89. doi: 10.2307/3428033. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 25.Durham D.R., Stirling L.A., Ornston L.N., Perry J.J. Intergeneric evolutionary homology revealed by the study of protocatechuate 3,4-dioxygenase from Azotobacter vinelandii. Biochemistry. 1980;19:149–155. doi: 10.1021/bi00542a023. [DOI] [PubMed] [Google Scholar]
  • 26.Eaton R.W. Plasmid-encoded phthalate catabolic pathway in Arthrobacter keyseri 12B. J Bacteriol. 2001;183:3689–3703. doi: 10.1128/JB.183.12.3689-3703.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 27.Eaton R.W., Ribbons D.W. Metabolism of dimethylphthalate by Micrococcus sp. strain 12B. J Bacteriol. 1982;151:465–467. doi: 10.1128/jb.151.1.465-467.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 28.Ejlertsson J., Svensson B.H. Degradation of bis(2-ethylhexyl) phthalate constituents under methanogenic conditions. Biodegradation. 1996;7:501–506. doi: 10.1007/BF00115296. [DOI] [PubMed] [Google Scholar]
  • 29.Evans W.C. The early intermediate fromed in the oxidative metabolism of phthalic acid by certain soil bacteria. Biochem J. 1955;61:x. [Google Scholar]
  • 30.Fang H.H., Liang D., Zhang T. Aerobic degradation of diethyl phthalate by Sphingomonas sp. Bioresour Technol. 2007;98:717–720. doi: 10.1016/j.biortech.2006.02.010. [DOI] [PubMed] [Google Scholar]
  • 31.Fisher J.S. Environmental anti-androgens and male reproductive health: focus on phthalates and testicular dysgenesis syndrome. Reproduction. 2004;127:305–315. doi: 10.1530/rep.1.00025. [DOI] [PubMed] [Google Scholar]
  • 32.Fujisawa H., Hayaishi O. Protocatechuate 3,4-dioxygenase. I. Crystallization and characterization. J Biol Chem. 1968;243:2673–2681. [PubMed] [Google Scholar]
  • 33.Gassner G.T., Ballou D.P. Preparation and characterization of a truncated form of phthalate dioxygenase reductase that lacks an iron-sulfur domain. Biochemistry. 1995;34:13460–13471. doi: 10.1021/bi00041a025. [DOI] [PubMed] [Google Scholar]
  • 34.Gesler R.M. Toxicology of di-2-ethylhexyl phthalate and other phthalic acid ester plasticizers. Environ Health Perspect. 1973;3:73–79. doi: 10.2307/3428032. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 35.Gibson D.T., Subramanian V. Microbial degradation of aromatic hydrocarbons. In: Gibson D.T., editor. Microbial degradation of organic compounds. New York: Marcel Dekker; 1984. pp. 181–252. [Google Scholar]
  • 36.Gray L.E., Jr., Ostby J., Furr J., Price M., Veeramachaneni D.N., Parks L. Perinatal exposure to the phthalates DEHP, BBP, and DINP, but not DEP, DMP, or DOTP, alters sexual differentiation of the male rat. Toxicol Sci. 2000;58:350–365. doi: 10.1093/toxsci/58.2.350. [DOI] [PubMed] [Google Scholar]
  • 37.Grifoll M., Selifonov S.A., Chapman P.J. Evidence for a novel pathway in the degradation of fluorene by Pseudomonas sp. strain F274. Appl Environ Microbiol. 1994;60:2438–2449. doi: 10.1128/aem.60.7.2438-2449.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 38.Gross F.C., Colony J.A. The ubiquitous nature and objectionable characteristics of phthalate esters in aerospace technology. Environ Health Perspect. 1973;3:37–48. doi: 10.2307/3428028. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 39.Habe H., Miyakoshi M., Chung J., Kasuga K., Yoshida T., Nojiri H., Omori T. Phthalate catabolic gene cluster is linked to the angular dioxygenase gene in Terrabacter sp. strain DBF63. Appl Microbiol Biotechnol. 2003;61:44–54. doi: 10.1007/s00253-002-1166-6. [DOI] [PubMed] [Google Scholar]
  • 40.Hara H., Eltis L.D., Davies J.E., Mohn W.W. Transcriptomic analysis reveals a bifurcated terephthalate degradation pathway in Rhodococcus sp. strain RHA1. J Bacteriol. 2007;189:1641–1647. doi: 10.1128/JB.01322-06. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 41.Hauser R., Meeker J.D., Singh N.P., Silva M.J., Ryan L., Duty S., Calafat A.M. DNA damage in human sperm is related to urinary levels of phthalate monoester and oxidative metabolites. Hum Reprod. 2007;22:688–695. doi: 10.1093/humrep/del428. [DOI] [PubMed] [Google Scholar]
  • 42.Heitkamp M.A., Freeman J.P., Miller D.W., Cerniglia C.E. Pyrene degradation by a Mycobacterium sp.: identification of ring oxidation and ring fission products. Appl Environ Microbiol. 1988;54:2556–2565. doi: 10.1128/aem.54.10.2556-2565.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 43.Hudson R.C., Daniel R.M. L-glutamate dehydrogenases: distribution, properties and mechanism. Comp Biochem Physiol B. 1993;106:767–792. doi: 10.1016/0305-0491(93)90031-Y. [DOI] [PubMed] [Google Scholar]
  • 44.Ito R., Seshimo F., Haishima Y., Hasegawa C., Isama K., Yagami T., Nakahashi K., Yamazaki H., Inoue K., Yoshimura Y., Saito K., Tsuchiya T., Nakazawa H. Reducing the migration of di-2-ethylhexyl phthalate from polyvinyl chloride medical devices. Int J Pharm. 2005;303:104–112. doi: 10.1016/j.ijpharm.2005.07.009. [DOI] [PubMed] [Google Scholar]
  • 45.Jaeger R.J., Rubin R.J. Extraction, localization, and metabolism of di-2-ethylhexyl phthalate from PVC plastic medical devices. Environ Health Perspect. 1973;3:95–102. doi: 10.2307/3428035. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 46.Jaeger R.J., Rubin R.J. Plasticizers from plastic devices extraction, metabolism, and accumulation by biological systems. Science. 1970;170:460–462. doi: 10.1126/science.170.3956.460. [DOI] [PubMed] [Google Scholar]
  • 47.Jianlong W., Lujun C., Hanchang S., Yi Q. Microbial degradation of phthalic acid esters under anaerobic digestion of sludge. Chemosphere. 2000;41:1245–1248. doi: 10.1016/S0045-6535(99)00552-4. [DOI] [PubMed] [Google Scholar]
  • 48.Kelley I., Freeman J.P., Evans F.E., Cerniglia C.E. Identification of metabolites from the degradation of fluoranthene by Mycobacterium sp. strain PYR-1. Appl Environ Microbiol. 1993;59:800–806. doi: 10.1128/aem.59.3.800-806.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 49.Keyser P., Pujar B.G., Eaton R.W., Ribbons D.W. Biodegradation of the phthalates and their esters by bacteria. Environ Health Perspect. 1976;18:159–166. doi: 10.2307/3428698. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 50.Kimura T., Ito Y. Two bacterial mixed culture systems suitable for degrading terephthalate in wastewater. J Biosci Bioeng. 2001;91:416–418. doi: 10.1263/jbb.91.416. [DOI] [PubMed] [Google Scholar]
  • 51.Kleerebezem R., Hulshoff Pol L.W., Lettinga G. The role of benzoate in anaerobic degradation of terephthalate. Appl Environ Microbiol. 1999;65:1161–1167. doi: 10.1128/aem.65.3.1161-1167.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 52.Kleerebezem R., Hulshoff Pol L.W., Lettinga G. Anaerobic degradation of phthalate isomers by methanogenic consortia. Appl Environ Microbiol. 1999;65:1152–1160. doi: 10.1128/aem.65.3.1152-1160.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 53.Kleerebezem R., Pol L.W., Lettinga G. Anaerobic biodegradability of phthalic acid isomers and related compounds. Biodegradation. 1999;10:63–73. doi: 10.1023/A:1008321015498. [DOI] [PubMed] [Google Scholar]
  • 54.Koch H.M., Drexler H., Angerer J. An estimation of the daily intake of di(2-ethylhexyl)phthalate (DEHP) and other phthalates in the general population. Int J Hyg Environ Health. 2003;206:77–83. doi: 10.1078/1438-4639-00205. [DOI] [PubMed] [Google Scholar]
  • 55.Krauskopf L.G. Studies on the toxicity of phthalates via ingestion. Environ Health Perspect. 1973;3:61–72. doi: 10.2307/3428031. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 56.Krishnan S., Prabhu Y., Phale P. o-Phthalic acid, a dead-end product in one of the two pathways of phenanthrene degradation in Pseudomonas sp. strain PP2. Indian J Biochem Biophys. 2004;41:227–232. [PubMed] [Google Scholar]
  • 57.Latini G. Monitoring phthalate exposure in humans. Clin Chim Acta. 2005;361:20–29. doi: 10.1016/j.cccn.2005.05.003. [DOI] [PubMed] [Google Scholar]
  • 58.Li J., Gu J.D. Biodegradation of dimethyl terephthalate by Pasteurella multocida Sa follows an alternative biochemical pathway. Ecotoxicology. 2006;15:391–397. doi: 10.1007/s10646-006-0070-8. [DOI] [PubMed] [Google Scholar]
  • 59.Li L.H., Jester W.F., Orth J.M. Effects of Relatively Low Levels of Mono-(2-Ethylhexyl) Phthalate on Cocultured Sertoli Cells and Gonocytes from Neonatal Rats. Toxicology and Applied Pharmacology. 1998;153:258–265. doi: 10.1006/taap.1998.8550. [DOI] [PubMed] [Google Scholar]
  • 60.Lovekamp-Swan T., Davis B.J. Mechanisms of phthalate ester toxicity in the female reproductive system. Environ Health Perspect. 2003;111:139–145. doi: 10.1289/ehp.5658. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 61.Lu K.Y., Tseng F.W., Wu C.J., Liu P.S. Suppression by phthalates of the calcium signaling of human nicotinic acetylcholine receptors in human neuroblastoma SH-SY5Y cells. Toxicology. 2004;200:113–121. doi: 10.1016/j.tox.2004.03.018. [DOI] [PubMed] [Google Scholar]
  • 62.Ludwig M.L., Ballou D.P., Noodleman L. Phthalate dioxygenase reductase. In: Messerschmidt A., Huber R., Poulos T., Weighardt K., editors. Handbook of Metalloproteins, Vol 1. New York: John Whiley and Sons, Co.; 2001. pp. 652–667. [Google Scholar]
  • 63.Malterud K.E., Rydland K.M., Haugli T. Inhibition of 15-lipoxygenase by phthalate plasticizers. Bull Environ Contam Toxicol. 1999;62:352–355. doi: 10.1007/s001289900881. [DOI] [PubMed] [Google Scholar]
  • 64.Mampel J., Providenti M.A., Cook A.M. Protocatechuate 4,5-dioxygenase from Comamonas testosteroni T-2: biochemical and molecular properties of a new subgroup within class III of extradiol dioxygenases. Arch Microbiol. 2005;183:130–139. doi: 10.1007/s00203-004-0755-4. [DOI] [PubMed] [Google Scholar]
  • 65.Marcel Y.L. Determination of di-2-ethylhexyl phthalate levels in human blood plasma and cryoprecipitates. Environ Health Perspect. 1973;3:119–121. doi: 10.2307/3428037. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 66.Maruyama K., Akita K., Naitou C., Yoshida M., Kitamura T. Purification and characterization of an esterase hydrolyzing monoalkyl phthalates from Micrococcus sp. YGJ1. J Biochem (Tokyo) 2005;137:27–32. doi: 10.1093/jb/mvi004. [DOI] [PubMed] [Google Scholar]
  • 67.Maruyama K., Shibayama T., Ichikawa A., Sakou Y., Yamada S., Sugisaki H. Cloning and characterization of the genes encoding enzymes for the protocatechuate meta-degradation pathway of Pseudomonas ochraceae NGJ1. Biosci Biotechnol Biochem. 2004;68:1434–1441. doi: 10.1271/bbb.68.1434. [DOI] [PubMed] [Google Scholar]
  • 68.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. doi: 10.1128/AEM.67.4.1476-1483.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 69.Moore N.P. The oestrogenic potential of the phthalate esters. Reprod Toxicol. 2000;14:183–192. doi: 10.1016/S0890-6238(00)00068-X. [DOI] [PubMed] [Google Scholar]
  • 70.Nallii S., Cooper D.G., Nicell J.A. Biodegradation of plasticizers by Rhodococcus rhodochrous. Biodegradation. 2002;13:343–352. doi: 10.1023/A:1022313810852. [DOI] [PubMed] [Google Scholar]
  • 71.Niazi J.H., Prasad D.T., Karegoudar T.B. Initial degradation of dimethylphthalate by esterases from Bacillus species. FEMS Microbiol Lett. 2001;196:201–205. doi: 10.1111/j.1574-6968.2001.tb10565.x. [DOI] [PubMed] [Google Scholar]
  • 72.Nishioka T., Iwata M., Imaoka T., Mutoh M., Egashira Y., Nishiyama T., Shin T., Fujii T. A mono-2-ethylhexyl phthalate hydrolase from a Gordonia sp. that is able to dissimilate di-2-ethylhexyl phthalate. Appl Environ Microbiol. 2006;72:2394–2399. doi: 10.1128/AEM.72.4.2394-2399.2006. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 73.Nomura Y., Harashima S., Oshima Y. A simple method for detection of enzyme activities involved in the initial step of phthalate degradation in microorganisms. J Ferment Bioeng. 1989;67:291–296. doi: 10.1016/0922-338X(89)90234-1. [DOI] [Google Scholar]
  • 74.Nozawa T., Maruyama Y. Anaerobic metabolism of phthalate and other aromatic compounds by a denitrifying bacterium. J Bacteriol. 1988;170:5778–5784. doi: 10.1128/jb.170.12.5778-5784.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 75.Orville A.M., Lipscomb J.D., Ohlendorf D.H. Crystal structures of substrate and substrate analog complexes of protocatechuate 3,4-dioxygenase: endogenous Fe3+ ligand displacement in response to substrate binding. Biochemistry. 1997;36:10052–10066. doi: 10.1021/bi970469f. [DOI] [PubMed] [Google Scholar]
  • 76.Overhage J., Kresse A.U., Priefert H., Sommer H., Krammer G., Rabenhorst J., Steinbuchel A. Molecular characterization of the genes pcaG and pcaH, encoding protocatechuate 3,4-dioxygenase, which are essential for vanillin catabolism in Pseudomonas sp. strain HR199. Appl Environ Microbiol. 1999;65:951–960. doi: 10.1128/aem.65.3.951-960.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 77.Pan G., Hanaoka T., Yoshimura M., Zhang S., Wang P., Tsukino H., Inoue K., Nakazawa H., Tsugane S., Takahashi K. Decreased serum free testosterone in workers exposed to high levels of di-n-butyl phthalate (DBP) and di-2-ethylhexyl phthalate (DEHP): a cross-sectional study in China. Environ Health Perspect. 2006;114:1643–1648. doi: 10.1289/ehp.9016. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 78.Patil N.K., Kundapur R., Shouche Y.S., Karegoudar T.B. Degradation of plasticizer di-n-butylphthalate by Delftia sp. TBKNP-05. Curr Microbiol. 2006;52:369–374. doi: 10.1007/s00284-005-5258-2. [DOI] [PubMed] [Google Scholar]
  • 79.Prabhu Y., Phale P.S. Biodegradtion of phenanthrene by Pseudomonas sp. strain PP2: novel metabolic pathway, role of biosurfactant and cell surface hydrophobicity in hydrocarbon assimilation. Appl Microbiol Biotechnol. 2003;61:342–351. doi: 10.1007/s00253-002-1218-y. [DOI] [PubMed] [Google Scholar]
  • 80.Pujar B.G., Ribbons D.W. Phthalate metabolism in Pseudomonas fluorescens PHK: purification and properties of 4,5-dihydroxyphthalate decarboxylase. Appl Environ Microbiol. 1985;49:374–376. doi: 10.1128/aem.49.2.374-376.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 81.Qiu Y.L., Sekiguchi Y., Hanada S., Imachi H., Tseng I.C., Cheng S.S., Ohashi A., Harada H., Kamagata Y. Pelotomaculum terephthalicum sp. nov. and Pelotomaculum isophthalicum sp. nov.: two anaerobic bacteria that degrade phthalate isomers in syntrophic association with hydrogenotrophic methanogens. Arch Microbiol. 2006;185:172–182. doi: 10.1007/s00203-005-0081-5. [DOI] [PubMed] [Google Scholar]
  • 82.Qiu Y.L., Sekiguchi Y., Imachi H., Kamagata Y., Tseng I.C., Cheng S.S., Ohashi A., Harada H. Identification and isolation of anaerobic, syntrophic phthalate isomerdegrading microbes from methanogenic sludges treating wastewater from terephthalate manufacturing. Appl Environ Microbiol. 2004;70:1617–1626. doi: 10.1128/AEM.70.3.1617-1626.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 83.Quan C.S., Liu Q., Tian W.J., Kikuchi J., Fan S.D. Biodegradation of an endocrine-disrupting chemical, di-2-ethylhexyl phthalate, by Bacillus subtilis No. 66. Appl Microbiol Biotechnol. 2005;66:702–710. doi: 10.1007/s00253-004-1683-6. [DOI] [PubMed] [Google Scholar]
  • 84.Rani M., Prakash D., Sobti R.C., Jain R.K. Plasmid-mediated degradation of o-phthalate and salicylate by a Moraxella sp. Biochem Biophys Res Commun. 1996;220:377–381. doi: 10.1006/bbrc.1996.0413. [DOI] [PubMed] [Google Scholar]
  • 85.Rogers K.S., Boots M.R., Boots S.G. Molecular interactions of six aromatic competitive inhibitors with bovine liver glutamate dehydrogenase. Biochim Biophys Acta. 1972;258:343–350. doi: 10.1016/0005-2744(72)90225-2. [DOI] [PubMed] [Google Scholar]
  • 86.Rubin R.J., Jaeger R.J. Some pharmacologic and toxicologic effects of di-2-ethylhexyl phthalate (DEHP) and other plasticizers. Environ Health Perspect. 1973;3:53–59. doi: 10.2307/3428030. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 87.Sasoh M., Masai E., Ishibashi S., Hara H., Kamimura N., Miyauchi K., Fukuda M. Characterization of the terephthalate degradation genes of Comamonas sp. strain E6. Appl Environ Microbiol. 2006;72:1825–1832. doi: 10.1128/AEM.72.3.1825-1832.2006. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 88.Schlafli H.R., Weiss M.A., Leisinger T., Cook A.M. Terephthalate 1,2-dioxygenase system from Comamonas testosteroni T-2: purification and some properties of the oxygenase component. J Bacteriol. 1994;176:6644–6652. doi: 10.1128/jb.176.21.6644-6652.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 89.Shelton D.R., Boyd S.A., Tiedje J.M. Anaerobic biodegradation of phthalaic acid esters in sludge. Environ Sci Technol. 1984;18:93–97. doi: 10.1021/es00120a008. [DOI] [PubMed] [Google Scholar]
  • 90.Shigematsu T., Yumihara K., Ueda Y., Morimura S., Kida K. Purification and gene cloning of the oxygenase component of the terephthalate 1,2-dioxygenase system from Delftia tsuruhatensis strain T7 FEMS. Microbiol Lett. 2003;220:255–260. doi: 10.1016/S0378-1097(03)00124-1. [DOI] [PubMed] [Google Scholar]
  • 91.Stingley R.L., Brezna B., Khan A.A., Cerniglia C.E. Novel organization of genes in a phthalate degradation operon of Mycobacterium vanbaalenii PYR-1. Microbiology. 2004;150:3749–3761. doi: 10.1099/mic.0.27263-0. [DOI] [PubMed] [Google Scholar]
  • 92.Suemori A., Kurane R., Tomizuka N. Purification and properties of phthalate oxygenase from Rhodococcus erythropolis S-1. Biosci Biotechnol Biochem. 1993;57:1482–1486. doi: 10.1271/bbb.57.1482. [DOI] [Google Scholar]
  • 93.Suemori A., Nikajama N., Kurane R., Nakamura Y. Production of 3,4-dihydroxyphthalate from phthalate by a membrane-bound two-enzyme system from Rhodococcus erythropolis. Appl Microbiol Biotechnol. 1995;43:470–472. doi: 10.1007/BF00218451. [DOI] [Google Scholar]
  • 94.Sugatt R.H., O’grady D.P., Banerjee S., Howard P.H., Gledhill W.E. Shake Flask Biodegradation of 14 Commercial Phthalate Esters. Appl Environ Microbiol. 1984;47:601–606. doi: 10.1128/aem.47.4.601-606.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 95.Sugimoto K., Senda T., Aoshima H., Masai E., Fukuda M., Mitsui Y. Crystal structure of an aromatic ring opening dioxygenase LigAB, a protocatechuate 4,5-dioxygenase, under aerobic conditions. Structure. 1999;7:953–965. doi: 10.1016/S0969-2126(99)80122-1. [DOI] [PubMed] [Google Scholar]
  • 96.Tarasev M., Kaddis C.S., Yin S., Loo J.A., Burgner J., Ballou D.P. Similar enzymes, different structures: Phthalate dioxygenase is an alpha(3)alpha(3) stacked hexamer, not an alpha(3)beta(3) trimer like “normal” Rieske oxygenases. Arch Biochem Biophys. 2007;466:31–39. doi: 10.1016/j.abb.2007.07.001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 97.Teil M.J., Blanchard M., Chevreuil M. Atmospheric fate of phthalate esters in an urban area (Paris-France) Sci Total Environ. 2006;354:212–223. doi: 10.1016/j.scitotenv.2004.12.083. [DOI] [PubMed] [Google Scholar]
  • 98.Tepper L.B. Phthalic acid esters — an overview. Environ Health Perspect. 1973;3:179–182. doi: 10.2307/3428046. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 99.Vamsee-Krishna C., Mohan Y., Phale P.S. Biodegradation of phthalate isomers by Pseudomonas aeruginosa PP4, Pseudomonas sp. PPD and Acinetobacter lwoffii ISP4. Appl Microbiol Biotechnol. 2006;72:1263–1269. doi: 10.1007/s00253-006-0413-7. [DOI] [PubMed] [Google Scholar]
  • 100.Vega D., Bastide J. Dimethylphthalate hydrolysis by specific microbial esterase. Chemosphere. 2003;51:663–668. doi: 10.1016/S0045-6535(03)00035-3. [DOI] [PubMed] [Google Scholar]
  • 101.Vetting M.W., D’Argenio D.A., Ornston L.N., Ohlendorf D.H. Structure of Acinetobacter strain ADP1 protocatechuate 3,4-dioxygenase at 2.2 A resolution: implications for the mechanism of an intradiol dioxygenase. Biochemistry. 2000;39:7943–7955. doi: 10.1021/bi000151e. [DOI] [PubMed] [Google Scholar]
  • 102.Wang Y., Fan Y., Gu J.D. Microbial degradation of the endocrine-disrupting chemicals phthalic acid and dimethyl phthalate ester under aerobic conditions. Bull Environ Contam Toxicol. 2003;71:810–818. doi: 10.1007/s00128-003-0207-x. [DOI] [PubMed] [Google Scholar]
  • 103.Wang Y.P., Gu J.D. Degradability of dimethyl terephthalate by Variovorax paradoxus T4 and Sphingomonas yanoikuyae DOS01 isolated from deep-ocean sediments. Ecotoxicology. 2006;15:549–557. doi: 10.1007/s10646-006-0093-1. [DOI] [PubMed] [Google Scholar]
  • 104.Wang Y.Z., Zhou Y., Zylstra G.J. Molecular analysis of isophthalate and terephthalate degradation by Comamonas testosteroni YZW-D. Environ Health Perspect. 1995;103:9–12. doi: 10.2307/3432469. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 105.Whittaker J.W., Orville A.M., Lipscomb J.D. Protocatechuate 3,4-dioxygenase from Brevibacterium fuscum. Methods Enzymol. 1990;188:82–88. doi: 10.1016/0076-6879(90)88016-4. [DOI] [PubMed] [Google Scholar]
  • 106.Wilkinson C.F., Lamb J.C. The potential health effects of phthalate esters in children’s toys: a review and risk assessment. Regul Toxicol Pharmacol. 1999;30:140–155. doi: 10.1006/rtph.1999.1338. [DOI] [PubMed] [Google Scholar]
  • 107.Yan H., Pan G. Increase in biodegradation of dimethyl phthalate by Closterium lunula using inorganic carbon. Chemosphere. 2004;55:1281–1285. doi: 10.1016/j.chemosphere.2003.12.019. [DOI] [PubMed] [Google Scholar]
  • 108.Yoshida R., Hori K., Fujiwara M., Saeki Y., Kagamiyama H. Nonidentical subunits of protocatechuate 3,4-dioxygenase. Biochemistry. 1976;15:4048–4053. doi: 10.1021/bi00663a020. [DOI] [PubMed] [Google Scholar]
  • 109.Yun S.H., Yun C.Y., Kim S.I. Characterization of protocatechuate 4,5-dioxygenase induced from p-hydroxybenzoate-cultured Pseudomonas sp. K82. J Microbiol. 2004;42:152–155. [PubMed] [Google Scholar]
  • 110.Zhu J., Phillips S.P., Feng Y.L., Yang X. Phthalate esters in human milk: concentration variations over a 6-month postpartum time. Environ Sci Technol. 2006;40:5276–5281. doi: 10.1021/es060356w. [DOI] [PubMed] [Google Scholar]
  • 111.Zylstra G.J., Olsen R.H., Ballou D.P. Cloning, expression, and regulation of the Pseudomonas cepacia protocatechuate 3,4-dioxygenase genes. J Bacteriol. 1989;171:5907–5914. doi: 10.1128/jb.171.11.5907-5914.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 112.Zylstra G.J., Olsen R.H., Ballou D.P. Genetic organization and sequence of the Pseudomonas cepacia genes for the alpha and beta subunits of protocatechuate 3,4-dioxygenase. J Bacteriol. 1989;171:5915–5921. doi: 10.1128/jb.171.11.5915-5921.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Indian Journal of Microbiology are provided here courtesy of Springer

RESOURCES