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. 2008 May 1;48(1):95–113. doi: 10.1007/s12088-008-0010-9

Bacterial metabolism of polycyclic aromatic hydrocarbons: strategies for bioremediation

Archana Chauhan 1, Fazlurrahman 1, John G Oakeshott 2, Rakesh K Jain 1,✉
PMCID: PMC3450204  PMID: 23100704

Abstract

Polycyclic aromatic hydrocarbons (PAHs) are compounds of intense public concern due to their persistence in the environment and potentially deleterious effects on human, environmental and ecological health. The clean up of such contaminants using invasive technologies has proven to be expensive and more importantly often damaging to the natural resource properties of the soil, sediment or aquifer. Bioremediation, which exploits the metabolic potential of microbes for the clean-up of recalcitrant xenobiotic compounds, has come up as a promising alternative. Several approaches such as improvement in PAH solubilization and entry into the cell, pathway and enzyme engineering and control of enzyme expression etc. are in development but far from complete. Successful application of the microorganisms for the bioremediation of PAH-contaminated sites therefore requires a deeper understanding of the physiology, biochemistry and molecular genetics of potential catabolic pathways. In this review, we briefly summarize important strategies adopted for PAH bioremediation and discuss the potential for their improvement.

Keywords: Polycyclic aromatic hydrocarbons, Bioremediation, Chemotaxis, Surfactants, Bioavailability, Genetic engineering

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References

  • 1.Kästner M. Degradation of aromatic and polyaromatic compounds. In: Rehm H.-J., Reed G., editors. Biotechnology. Weinheim, Germany: Wiley-VCH; 2000. pp. 211–239. [Google Scholar]
  • 2.Blumer M. Polycyclic aromatic compounds in nature. Sci American. 1976;234:35–45. [PubMed] [Google Scholar]
  • 3.Ramdahl T. PAH emissions from combustion of biomass. In: Bjørseth A., Ramdahl T., editors. Handbook of Polycyclic Aromatic Hydrocarbons. N.Y.: Macel Dekker; 1985. pp. 61–85. [Google Scholar]
  • 4.Saraswathy A., Hallberg R. Degradation of pyrene by indigenous fungi from a former gasworks site. FEMS Microbiol Lett. 2002;210:227–232. doi: 10.1111/j.1574-6968.2002.tb11185.x. [DOI] [PubMed] [Google Scholar]
  • 5.Stefen KT (2003) Degradation of recalcitrant biopolymers and polycyclic aromatic hydrocarbons by litter-decomposing basidiomycetous fungi. Academic Dissertation in Microbiology, University of Helsinki Finland
  • 6.Brandt H.C.A., Watson W.P. Monitoring human occupational and environmental exposures to polycyclic aromatic compounds. Ann Occup Hyg. 2003;47:349–378. doi: 10.1093/annhyg/meg052. [DOI] [PubMed] [Google Scholar]
  • 7.Hammond E.C., Selikof I.J., Lawther P.L., Seidman H. Inhalation of benz[a]pyrene and cancer in man. Ann NY Acad Sci. 1976;271:116–124. doi: 10.1111/j.1749-6632.1976.tb23100.x. [DOI] [PubMed] [Google Scholar]
  • 8.Grimmer G. In Environmental carcinogens. Lyon: IARC; 1979. Selected methods of analysis; p. 31. [Google Scholar]
  • 9.Environmental Health Criteria 202. Geneva: International Programme on Chemical Safety, World Health Organization; 1998. Selected non-heterocyclic polycyclic aromatic hydrocarbons. [Google Scholar]
  • 10.Liu K. Polycyclic aromatic hydrocarbon (PAH) emissions from a coal fired pilot FBC system. J Hazard Mater. 2001;84:175–188. doi: 10.1016/S0304-3894(01)00196-0. [DOI] [PubMed] [Google Scholar]
  • 11.Mastrangela G. Polycyclic aromatic hydrocarbons and cancer in man. Environ Health Perspect. 1997;104:1166–1170. doi: 10.2307/3432909. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 12.Sram R.J. Adverse reproductive outcomes from exposure to environmental mutagens. Mutat Res. 1999;428:203–215. doi: 10.1016/s1383-5742(99)00048-4. [DOI] [PubMed] [Google Scholar]
  • 13.Wilson S.C., Jones K.C. Bioremediation of soil contaminated with polynucleararomatic hydrocarbons (PAHs): a review. Environ Poll. 1993;81:229–249. doi: 10.1016/0269-7491(93)90206-4. [DOI] [PubMed] [Google Scholar]
  • 14.Cerniglia C.E., Heitkamp M.A. Microbial degradation of polycyclic aromatic hydrocarbons (PAH) in the aquatic environment. In: Varanasi U., editor. Metabolismof Polycyclic Aromatic Hydrocarbons in the Aquatic Environment. BocaRaton, Florida: CRC Press, Inc.; 1989. pp. 41–68. [Google Scholar]
  • 15.Goldman R. Smoking increases carcinogenic polycyclic aromatic hydrocarbons in human lung tissue. Cancer Res. 2001;61:6367–6371. [PubMed] [Google Scholar]
  • 16.Kaiser J. Endocrine disrupters: Synergy paper questioned at toxicology meeting. Science. 1997;275:1879–1880. doi: 10.1126/science.275.5308.1879. [DOI] [PubMed] [Google Scholar]
  • 17.Pothuluri JV and Cerniglia CE (1994) Microbial metabolism of polycyclic aromatic hydrocarbons. In: G.R. Chaudhry, Editor, Biological degradation and Bioremediation of Toxic Chemicals, Chapman and Hall, 92–124
  • 18.Howard P.H., Boethling R.S., Jarvis W.F., Meylan W.M., Michalenko E.M. In: Handbook of Environmental Degradation Rates. Printup H.T., editor. Chelsea, MI: Lewis Publishers; 1991. [Google Scholar]
  • 19.Bamforth S.M., Singleton I. Bioremediation of polycyclic aromatic hydrocarbons: current knowledge and future directions. J Chemical Technol Biotechnol. 2005;80:723–736. doi: 10.1002/jctb.1276. [DOI] [Google Scholar]
  • 20.Ulric W. Contaminated soil areas, different countries and contaminants, monitoring of contaminants. In: Rehm H.J., Reed G., Pühler A., Stadler P., editors. Biotechnology Vol. 11b: environmental Processes II. Weihheim, FRG: Wiley-VCH; 2000. pp. 5–42. [Google Scholar]
  • 21.Mueller J.G., Lantz S.E., Ross D., Colvin R.J., Middaugh D.P., Pritchard P.H. Strategy using bioreactors and specially selected micro-organisms for bioremediation of groundwater contaminated with creosote and pentachlorophenol. Environ Sci Technol. 1993;27:691–698. doi: 10.1021/es00041a012. [DOI] [Google Scholar]
  • 22.Cerniglia C.E. Biodegradation of polycyclic aromatic hydrocarbons. Curr Opn Biotechnol. 1993;4:331–338. doi: 10.1016/0958-1669(93)90104-5. [DOI] [Google Scholar]
  • 23.Samanta S.K., Singh O.V., Jain R.K. Polycyclic aromatic hydrocarbons: environmental pollution and bioremediation. Trends Biotechnol. 2002;20:243–248. doi: 10.1016/S0167-7799(02)01943-1. [DOI] [PubMed] [Google Scholar]
  • 24.Patel T.R., ainsley E.A. Napthelene metabolism by Pseudomonads: Purification and properties of 1,2-dihydroxynaphthalene oxygenase. J Bateriol. 1980;143:668–673. doi: 10.1128/jb.143.2.668-673.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 25.Samanta S.K., Rani M., Jain R.K. Segregational and structural instability of a recombinant plasmid carrying genes for naphthalene degradation. Lett Appl Microbiol. 1998;26:265–269. doi: 10.1046/j.1472-765X.1998.00316.x. [DOI] [PubMed] [Google Scholar]
  • 26.Johnsen A.R., Lukas Yand Hauke H. Principles of microbial PAH-degradation in soil. Environ Poll. 2005;1:71–84. doi: 10.1016/j.envpol.2004.04.015. [DOI] [PubMed] [Google Scholar]
  • 27.Smith M.R. The biodegradation of aromatic hydrocarbons by bacteria. Biodegradation. 1990;1:191–206. doi: 10.1007/BF00058836. [DOI] [PubMed] [Google Scholar]
  • 28.Watanabe K. Microrganisms relevant to bioremediation. Curr Opin Biotechnol. 2001;12:237–241. doi: 10.1016/S0958-1669(00)00205-6. [DOI] [PubMed] [Google Scholar]
  • 29.Bakermans C., Hohnstock-Ashe A.M., Padmanabhan S., Padmanabhan P., Madsen E.L. Geochemical and physiological evidence for mixed aerobic and anaerobic field biodegradation of coal tar waste by subsurface microbial communities. Microbial Ecol. 2002;44:107–117. doi: 10.1007/s00248-002-3011-y. [DOI] [PubMed] [Google Scholar]
  • 30.Bewley R.J.F., Webb G. In situ bioremediation of groundwater contaminated with phenols, BTEX and PAHs using nitrate as electron acceptor. Land Contam Reclam. 2001;9:335–347. [Google Scholar]
  • 31.Meckenstock R.U., Annweiler E., Michaelis W., Richnow H.H., Schink B. Anaerobic naphthalene degradation by a sulphate reducing enrichment culture. Appl Environ Microbiol. 2000;66:2743–2747. doi: 10.1128/AEM.66.7.2743-2747.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 32.Genthner B.R.S., Townsend G.T., Lantz S.E., Mueller J.G. Persistence of polycyclic aromatic hydrocarbon components of creosote under anaerobic enrichment conditions. Arch Environ Contam Toxicol. 1997;32:99–105. doi: 10.1007/s002449900160. [DOI] [PubMed] [Google Scholar]
  • 33.Coates J.D., Anderson R.T., Lovley D.R. Oxidation of polycyclic aromatic hydrocarbons under sulfate-reducing conditions. Appl Environ Microbiol. 1996;62:1099–1101. doi: 10.1128/aem.62.3.1099-1101.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 34.Ohkouchi N., Kawamura K., Kawahata H. Distributions of three to seven-ring polynuclear aromatic hydrocarbons on the deep sea floor in the central pacific. Environ Sci Technol. 1999;33:3086–3090. doi: 10.1021/es981181w. [DOI] [Google Scholar]
  • 35.Zhang X., Sullivan E.R., Young L.Y. Evidence for aromatic ring reduction in the biodegradation pathway of carboxylated naphthalene by a sulphate-reducing consortium. Biodegradation. 2000;11:117–124. doi: 10.1023/A:1011128109670. [DOI] [PubMed] [Google Scholar]
  • 36.Ambrosoli R., Petruzzelli L., Minati J.L., Marsan F.A. Anaerobic PAH degradation in soil by a mixed bacterial consortium under denitrifying conditions. Chemosphere. 2005;60:1231–1236. doi: 10.1016/j.chemosphere.2005.02.030. [DOI] [PubMed] [Google Scholar]
  • 37.Quantin C., Joner E.J., Portal J.M., Berthelin J. PAH dissipation in a contaminated river sediment under oxic and anoxic conditions. Environ Poll. 2005;134:315–322. doi: 10.1016/j.envpol.2004.07.022. [DOI] [PubMed] [Google Scholar]
  • 38.Xu-Xiang Z., Shu-Pei C., Cheng-Jun Z., Shi-Lei S. Microbial PAH degradation in soil: degradation pathways and contributing factors. Pedosphere. 2006;16:555–565. doi: 10.1016/S1002-0160(06)60088-X. [DOI] [Google Scholar]
  • 39.Kim S.-J., Kweon O., Freeman J.P., Jones R.C., Adjei M.D., Jhoo J.-W., Edmondson R.D., Cerniglia C.E. Molecular cloning and expression of genes encoding a novel dioxygenase involved in low-and high-molecular-weight polycyclic aromatic hydrocarbon degradation in Mycobacterium vanbaalenii PYR-1. Appl Environ Microbiol. 2006;72:1045–1054. doi: 10.1128/AEM.72.2.1045-1054.2006. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 40.Samanta S.K., Ckakraborti A.K., Jain R.K. Degradation of phenanthrene by different bacteria: evidence for novel transformation sequences involving the formation of 1-naphthol. Appl Environ Microbiol. 1999;53:98–107. doi: 10.1007/s002530051621. [DOI] [PubMed] [Google Scholar]
  • 41.Bosch R., Garcia-Valdés E., Moore E.R.B. Genetic characterization and evolutionary implications of a chromosomally encoded naphthalene-degradation upper pathway from Pseudomonas stutzeri AN10. Gene. 1999;236:149–157. doi: 10.1016/S0378-1119(99)00241-3. [DOI] [PubMed] [Google Scholar]
  • 42.Sanseverino J., Applegate B.M., King J.M., Sayler G.S. Plasmid-mediated mineralization of naphthalene, phenanthrene, and anthracene. Appl Environ Microbiol. 1993;59:1931–1937. doi: 10.1128/aem.59.6.1931-1937.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 43.Takizawa N., Iida T., Sawada T., Yamauchi K., Wang Y.-W., Fukuda M., Kiyohara H. Nucleotide sequences and characterization of genes encoding naphthalene upper pathway of Pseudomonas aeruginosa PaK1 and Pseudomonas putida OUS82. J Biosci Bioeng. 1999;87:723–731. doi: 10.1016/S1389-1723(99)80144-3. [DOI] [PubMed] [Google Scholar]
  • 44.Habe H., Omori T. Genetics of polycyclic aromatic hydrocarbon degradation by diverse aerobic baceria. Biosci Biotechnol Biochem. 2003;67:225–243. doi: 10.1271/bbb.67.225. [DOI] [PubMed] [Google Scholar]
  • 45.Juhasz A.L. Microbial degradation and detoxification of high molecular weight polycyclic aromatic hydrocarbons by Stenotrophomonas maltophilia strain VUN 10003. Lett Appl Microbiol. 2000;30:396–401. doi: 10.1046/j.1472-765x.2000.00733.x. [DOI] [PubMed] [Google Scholar]
  • 46.Kanaly R.A., Harayama S. Biodegradation of high-molecular-weight polycyclic aromatic hydrocarbons by bacteria. J Bacteriol. 2000;182:2059–2067. doi: 10.1128/JB.182.8.2059-2067.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 47.Watanabe K. Microorganisms relevant to bioremediation. Curr Opin Biotechnol. 2001;12:237–241. doi: 10.1016/S0958-1669(00)00205-6. [DOI] [PubMed] [Google Scholar]
  • 48.Hatfull G.F., Jacobs W.R. Molecular genetics of Mycobacteria. Washington, DC: ASM Press; 2000. [Google Scholar]
  • 49.Khan A.A., Wang R.-F., Cao W.-W., Doerge D.R., Wennerstrom D., Cerniglia C.E. Molecular cloning, nucleotide sequence, and expression of genes encoding a polycyclic aromatic ring dioxygenase from Mycobacterium sp. strain PYR-1. Appl Environ Microbiol. 2001;67:3577–3585. doi: 10.1128/AEM.67.8.3577-3585.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 50.Krivobok S., Kuony S., Meyer C., Louwagie M., Willison J.C., Jouanneau Y. Identification of pyrene-induced proteins in Mycobacterium sp. strain 6PY1: evidence for two ring-hydroxylating dioxygenases. J Bacteriol. 2003;185:3828–3841. doi: 10.1128/JB.185.13.3828-3841.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 51.Sho M., Hamel C., Greer C.W. Two distinct gene clusters encode pyrene degradation in Mycobacterium sp. strain S65. FEMS Microbiol Ecol. 2004;48:209–220. doi: 10.1016/j.femsec.2004.01.011. [DOI] [PubMed] [Google Scholar]
  • 52.Brezna B., Khan A.A., Cerniglia C.E. Molecular characterization of dioxygenases from polycyclic aromatic hydrocarbon-degrading Mycobacterium sp. FEMS Microbiol Lett. 2003;223:177–183. doi: 10.1016/S0378-1097(03)00328-8. [DOI] [PubMed] [Google Scholar]
  • 53.Hall K., Miller C.D., Sorensen D.L., Anderson A.J., Sims R.C. Development of a catabolically significant genetic probe for polycyclic aromatic hydrocarbon-degrading Mycobacteria in soil. Biodegradation. 2005;16:475–484. doi: 10.1007/s10532-004-5669-y. [DOI] [PubMed] [Google Scholar]
  • 54.Cruden D.L., Gibson D.T., Zylstra G.J. Sequences of genes encoding naphthalene dioxygenase in Pseudomonas putida strains G7 and NCIB 9816-4. Gene. 1993;127:31–37. doi: 10.1016/0378-1119(93)90613-8. [DOI] [PubMed] [Google Scholar]
  • 55.Brezna B., Khan A.A., Cerniglia C.E. Molecular characterization of a phenanthrene degradation pathway in Mycobacterium vanbaalenii PYR-1. Biochem Biophys Res Commun. 2004;322:133–146. doi: 10.1016/j.bbrc.2004.07.089. [DOI] [PubMed] [Google Scholar]
  • 56.Pagnout C., Frache G., Poupin P., Maunit B., Muller J.-F., Férard J.-F. Isolation and characterization of a gene cluster involved in PAH degradation in Mycobacterium sp. strain SNP11: Expression in Mycobacterium smegmatis mc 2155. Res Microbiol. 2007;158:175–186. doi: 10.1016/j.resmic.2006.11.002. [DOI] [PubMed] [Google Scholar]
  • 57.Brezna B., Kweon O., Stingley R.L., Freeman J.P., Polek B., Jones R.C., Khan A.A., Cerniglia C.E. Molecular characterization of cytochrome P450 genes in the polycyclic aromatic hydrocarbon degrading Mycobacterium vanbaalenii PYR-1. Appl Microbiol Biotechnol. 2006;71:522–532. doi: 10.1007/s00253-005-0190-8. [DOI] [PubMed] [Google Scholar]
  • 58.Liang Y., Gardner D.R., Miller C.D., Chen D., Anderson A.J., Weimer B.C., Sims R.C. Study of biochemical pathways and enzymes involved in pyrene degradation by Mycobacterium sp. strain KMS. Appl Environ Microbiol. 2006;72:7821–7828. doi: 10.1128/AEM.01274-06. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 59.Kim S.-J., Kweon O., Jones Richard C., Freeman J.P., Edmondson R.D., Cerniglia C.E. Complete and integrated pyrene degradation pathway in Mycobacterium vanbaalenii PYR-1 based on systems biology. J Bacteriol. 2007;189:464–472. doi: 10.1128/JB.01310-06. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 60.Juhasz A.L., Naidu R. Bioremediation of high molecular weight polycyclic aromatic hydrocarbons: a review of the microbial degradation of benzo[a]pyrene. Int Biodeterior Biodegradation. 2000;45:57–88. doi: 10.1016/S0964-8305(00)00052-4. [DOI] [Google Scholar]
  • 61.Kastner M., Mahro B. Microbial degradation of polycyclic aromatic hydrocarbons in soils affected by the organic matrix of compost. Appl Microbiol Biotechnol. 1996;44:668–675. doi: 10.1007/BF00172501. [DOI] [PubMed] [Google Scholar]
  • 62.Pandey G., Jain R.K. Bacterial chemotaxis toward environmental pollutants: role in bioremediation. Appl Environ Microbiol. 2002;68:5789–5795. doi: 10.1128/AEM.68.12.5789-5795.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 63.Herrenkohl M.J., Lunz J.D., Sheets R.G., Wakeman J.S. Environmental impacts of PAH and oil release as a NAPL or as contaminated pore water from the construction of a 90-cm in situ isolation cap. Environ Sci Technol. 2001;35:4927–4932. doi: 10.1021/es010758y. [DOI] [PubMed] [Google Scholar]
  • 64.Schluep M., Imboden D.M., Galli R., Zeyer J. Mechanisms affecting the dissolution of nonaqueous phase liquids into the aqueous phase in slow stirring batch system. Environ Toxicol Chem. 2001;20:459–466. doi: 10.1897/1551-5028(2001)020<0459:MATDON>2.0.CO;2. [DOI] [PubMed] [Google Scholar]
  • 65.Wick L.Y., Colangelo T., Harms H. Kinetics of mass transfer-limited bacterial growth on solid PAHs. Environ Sci Technol. 2001;35:354–361. doi: 10.1021/es001384w. [DOI] [PubMed] [Google Scholar]
  • 66.Volkering F., Breure A.M., Andel J.G.V., Rulkens W.H. Influence of nonionic surfactants on bioavailability and biodegradation of polycyclic aromatic hydrocarbons. Appl Environ Microbiol. 1995;61:1699–1705. doi: 10.1128/aem.61.5.1699-1705.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 67.Grimberg S.J. Quantifying the biodegradation of phenanthrene by Pseudomonas stutzeri P16 in the presence of a nonionic surfactant. Appl Environ Microbiol. 1996;62:2387–2392. doi: 10.1128/aem.62.7.2387-2392.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 68.Willumsen P.A. Degradation of phenanthrene-analogue azaarenes by Mycobacterium gilvum strain LB307T under aerobic conditions. Appl Microbiol Biotechnol. 2001;56:539–544. doi: 10.1007/s002530100640. [DOI] [PubMed] [Google Scholar]
  • 69.Ron E.Z., Rosenberg E. Biosurfactants and oil bioremediation. Curr Opin Biotechnol. 2002;13:249–252. doi: 10.1016/S0958-1669(02)00316-6. [DOI] [PubMed] [Google Scholar]
  • 70.Rosenberg E., Barkay T., Navon-Venezia S., Ron E.Z. Role of Acinetobacter bioemulsans in petroleum degradation. In: Fass R., editor. Novel Approaches for Bioremediation of Organic Pollution. New York: Kluwer Academic/Plenum Publishers; 1999. pp. 171–180. [Google Scholar]
  • 71.Barkay T., Navon-Venezia S., Ron E., Rosenberg E. Enhancement of solubilization and biodegradation of polyaromatic hydrocarbons by the bioemulsifier alasan. Appl Environ Microbiol. 1999;65:2697–2702. doi: 10.1128/aem.65.6.2697-2702.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 72.Aronstein B.N., Alexander M. Surfactants at low concentrations stimulate biodegradation of sorbed hydrocarbons in samples of aquifer sands and soil slurries. Environ Toxicol Chem. 1992;11:1227–1233. doi: 10.1897/1552-8618(1992)11[1227:SALCSB]2.0.CO;2. [DOI] [Google Scholar]
  • 73.Aronstein B.N., Alexander M. Effect of a non-ionic surfactant added to the soil surface on the biodegradation of aromatic hydrocarbons within the soil. Appl Environ Microbiol. 1993;39:386–390. [Google Scholar]
  • 74.Bury S.J., Miller C.A. Effect of micellar solubilization on biodegradation rates of hydrocarbons. Environ Sci Technol. 1993;27:104–110. doi: 10.1021/es00038a010. [DOI] [Google Scholar]
  • 75.Churchill P.F., Dudley R.J., Churchill S.A. Surfactant-enhanced bioremediation. Waste Manag. 1995;15:371–377. doi: 10.1016/0956-053X(95)00038-2. [DOI] [Google Scholar]
  • 76.Tiehm A. Degradation of polycyclic aromatic hydrocarbons in the presence of synthetic surfactants. Appl Environ Microbiol. 1994;60:258–263. doi: 10.1128/aem.60.1.258-263.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 77.Straube W.L., Nestler C.C., Hansen L.D., Ringleberg D., Pritchard P.J., Jones-Meehan J. Remediation of polyaromatic hydrocarbons (PAHs) through landfarming with biostimulation and bioaugmentation. Acta Biotechnologica. 2003;2:179–196. doi: 10.1002/abio.200390025. [DOI] [Google Scholar]
  • 78.Mulligan, Gibbs . Factors influencing the economics of biosurfactants. In: Kosaric N., editor. Biosurfactants, Production, Properties, Applications. New York: Marcel Dekker; 1993. pp. 329–371. [Google Scholar]
  • 79.Deschênes L., Lafrance P., Villeneuve J.-P., Samson R. The effect of an anionic surfactant on the mobilization and biodegradation of PAHs in a creosote-contaminated soil. Hydrol Sci J. 1995;40:471–484. doi: 10.1080/02626669509491433. [DOI] [Google Scholar]
  • 80.Grimberg S.J., Aitken M.D. Biodegradation kinetics of phenanthrene solubilized in surfactant micelles. In: Hinchee R. E., Brockman F. J., Vogel C. M., editors. Microbial processes for bioremediation. Columbus, Ohio: Battelle Press; 1995. pp. 59–66. [Google Scholar]
  • 81.Laha S., Luthy R.G. Effects of nonionic surfactants on the solubilization and mineralization of phenanthrene in soil-water systems. Biotechnol Bioeng. 1992;40:1367–1380. doi: 10.1002/bit.260401111. [DOI] [PubMed] [Google Scholar]
  • 82.Bruheim P. Bacterial degradation of emulsified crude oil and the effect of various surfactants. Can J Microbiol. 1997;43:17–22. doi: 10.1139/m97-003. [DOI] [PubMed] [Google Scholar]
  • 83.Bruheim P. Chemically emulsified crude oil as substrate for bacterial oxidation: differences in species response. Can J Microbiol. 1998;44:195–199. doi: 10.1139/cjm-44-2-195. [DOI] [PubMed] [Google Scholar]
  • 84.García-Junco M.E., Olmedo, Ortega-Calvo J.J. Bioavailability of solid and non-aqueous phase liquid (NAPL)-dissolved phenanthrene to the biosurfactant-producing bacterium Pseudomonas aeruginosa 19SJ. Environ Microbiol. 2001;3:561–569. doi: 10.1046/j.1462-2920.2001.00223.x. [DOI] [PubMed] [Google Scholar]
  • 85.Guerin W.F., Boyd S.A. Differential bioavailability of soil-sorbed naphthalene to two bacterial species. Appl Environ Microbiol. 1992;58:1142–1152. doi: 10.1128/aem.58.4.1142-1152.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 86.Tang W.C., White J.C., Alexander M. Utilization of sorbed compounds by microorganisms specifically isolated for that purpose. Appl Microbiol Biotechnol. 1998;49:117–121. doi: 10.1007/s002530051147. [DOI] [PubMed] [Google Scholar]
  • 87.Miyata N., Iwahori K., Foght J.M., Gray M.R. Saturable, energy-dependent uptake of phenanthrene in aqueous phase by Mycobacterium sp. strain RJGII-135. Appl Environ Microbiol. 2004;70:363–369. doi: 10.1128/AEM.70.1.363-369.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 88.Sikkema J., Bont J.A.M., Poolman B. Mechanisms of membrane toxicity of hydrocarbons. Microbiol Rev. 1995;59:201–222. doi: 10.1128/mr.59.2.201-222.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 89.Tongpim S., Pickard M.A. Growth of Rhodococcus S1 on anthracene. Can J Microbiol. 1996;42:289–294. doi: 10.1139/m96-042. [DOI] [PubMed] [Google Scholar]
  • 90.Bastiaens L., Springael D., Wattiau P., Harms H., Wachter R., Verachtert H., Diels L. isolation of adherent polycyclic aromatic hydrocarbon (PAH)-degrading bacteria using PAH-sorbing carriers. Appl Environ Microbiol. 2000;66:1834–1843. doi: 10.1128/AEM.66.5.1834-1843.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 91.Wick L.Y., Ruiz de Munain A., Springael D. Responses of Mycobacterium sp. LB501T to the low bioavailability of solid anthracene. Appl Microbiol Biotechnol. 2002;58:378–385. doi: 10.1007/s00253-001-0898-z. [DOI] [PubMed] [Google Scholar]
  • 92.Dean-Ross D., Moody J., Cerniglia C.E. Utilization of mixtures of polycyclic aromatic hydrocarbons by bacteria isolated from contaminated sediment. FEMS Microbiol Ecol. 2002;41:1–7. doi: 10.1111/j.1574-6941.2002.tb00960.x. [DOI] [PubMed] [Google Scholar]
  • 93.McLellan S.L., Warshawsky D., Shann J.R. The effect of polycyclic aromatic hydrocarbons on the degradation of benzo[aa]pyrene by Mycobacterium sp. strain RJGII-135. Environ Toxicol Chem. 2002;21:253–259. doi: 10.1897/1551-5028(2002)021<0253:TEOPAH>2.0.CO;2. [DOI] [PubMed] [Google Scholar]
  • 94.Bugg T., Foght J.M., Pickard M.A., Gray M.R. Uptake and active efflux of polycyclic aromatic hydrocarbons by Pseudomonas fluorescens LP6a. Appl Microbiol Biotechnol. 2000;66:5387–5392. doi: 10.1128/aem.66.12.5387-5392.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 95.Whitman B.E., Lueking D.R., Mihelcic J.R. Naphthalene uptake by a Pseudomonas fluorescens isolate. Can J Microbiol. 1998;44:1086–1093. doi: 10.1139/cjm-44-11-1086. [DOI] [PubMed] [Google Scholar]
  • 96.Kahng H.Y., Byrne A.M., Olsen R.H., Kukor J.J. Characterization and role of tbuXtbuX in utilization of toluene by Ralstonia PKO1. J Bacteriol. 2000;182:1232–1242. doi: 10.1128/JB.182.5.1232-1242.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 97.Kasai Y., Inoue J., Harayama S. The TOL plasmid pWW0 xylNxylN gene product from Pseudomonas putida is involved in mm-xylene uptake. J Bacteriol. 2001;183:6662–6666. doi: 10.1128/JB.183.22.6662-6666.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 98.Beal R., Betts Role of rhamnolipid biosurfactants in the uptake and mineralization of hexadecane in Pseudomonas aeruginosa. J Appl Microbiol. 2000;89:158–168. doi: 10.1046/j.1365-2672.2000.01104.x. [DOI] [PubMed] [Google Scholar]
  • 99.Kim I.S., Foght J.M., Gray M.R. Selective transport and accumulation of alkanes by Rhodococcus erythropolis. Biotechnol Bioeng. 2002;80:650–659. doi: 10.1002/bit.10421. [DOI] [PubMed] [Google Scholar]
  • 100.Noordman W.H., Janssen D.B. Rhamnolipid stimulates uptake of hydrophobic compounds by Pseudomonas aeruginosa. Appl Environ Microbiol. 2002;68:4502–4508. doi: 10.1128/AEM.68.9.4502-4508.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 101.Noda K.I., Watanabe K., Maruhashi K. Isolation of the Pseudomonas aeruginosa gene affecting uptake of dibenzothiophene in nn-tetradecane. J Biosci Bioeng. 2003;95:504–511. [PubMed] [Google Scholar]
  • 102.Black P.N., DiRusso C.C. Molecular and biochemical analyses of fatty acid transport, metabolism, and gene regulation in Escherichia coli. Biochim Biophys Acta. 1994;1210:123–145. doi: 10.1016/0005-2760(94)90113-9. [DOI] [PubMed] [Google Scholar]
  • 103.Hirsch D., Stahl A., Lodish H.F. A family of fatty acid transporters conserved from Mycobacterium to man. Proc Natl Acad Sci USA. 1998;95:8625–8629. doi: 10.1073/pnas.95.15.8625. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 104.Diaz E., Prieto M.A. Bacterial promoters triggering biodegradation of aromatic pollutants. Curr Opin Biotechnol. 2000;11:467–475. doi: 10.1016/S0958-1669(00)00126-9. [DOI] [PubMed] [Google Scholar]
  • 105.Cases, Lorenzo V. Expression systems and physiological control of promoter activity in bacteria. Curr Opin Microbiol. 1998;1:303–310. doi: 10.1016/S1369-5274(98)80034-9. [DOI] [PubMed] [Google Scholar]
  • 106.Platt A., Shingler V., Taylor S.C., Williams P.A. The 4-hydroxy-2-oxovalerate aldolase and acetaldehyde dehydrogenase (acylating) encodedby the nahM and nahO genes of the naphthalene catabolic plasmid pWW60-22 provide further evidence of conservation of meta-cleavage pathway gene sequences. Microbiology. 1995;141:2223–2233. doi: 10.1099/13500872-141-9-2223. [DOI] [PubMed] [Google Scholar]
  • 107.Simon M.J., Osslund T.D., Saunders R., Ensley B.D., Suggs S., Harcourt W.-C., Cruden S.L., Gibson D.T., Zylstra G.J. Sequence of genes encoding naphthalene dioxygenase in Pseudomonas putida strains G7 and NCIB 9816-4. Gene. 1993;127:31–37. doi: 10.1016/0378-1119(93)90613-8. [DOI] [PubMed] [Google Scholar]
  • 108.Yen K.-M., Serdar C.M. Genetics of naphthalene catabolism in Pseudomonads. CRC Crit Rev Microbiol. 1988;15:247–268. doi: 10.3109/10408418809104459. [DOI] [PubMed] [Google Scholar]
  • 109.QLau P.C.K., Wang Y., Patel A., Labbe D., Bergeron H., Brousseau R., Konishi Y., Rawlings A bacterial basic region leucine zipper histidine kinase regulating toluene degradation. Proc Natl Acad Sci. 1997;95:1453–1458. doi: 10.1073/pnas.94.4.1453. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 110.Goldstein R.M., Mallory L.M., Alexander M. Reasons for possible failure of inoculation to enhance biodegradation. Curr Opin Biotechnol. 1985;50:977–983. doi: 10.1128/aem.50.4.977-983.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 111.Bouchez M., Blanchet D., Vandecasteele V.-P. Degradation of polycyclic aromatic hydrocarbons by pure strains and by defined strain associations: inhibition phenomena and cometabolism. Appl Microbiol Biotechnol. 1995;43:156–164. doi: 10.1007/BF00170638. [DOI] [PubMed] [Google Scholar]
  • 112.Wagner-Döbler I. Pilot plant for bioremediation of mercury-containing industrial wastewater. Appl Microbiol Biotechnol. 2003;62:124–133. doi: 10.1007/s00253-003-1322-7. [DOI] [PubMed] [Google Scholar]
  • 113.Providenti M.A., Lee H., Trevors J.T. Selected factors limiting the microbial degradation of recalcitrant compounds. J Ind Microbiol. 1993;12:379–395. doi: 10.1007/BF01569669. [DOI] [Google Scholar]
  • 114.Molina M., Araujo R., Hodson R.E. Cross-induction of pyrene and phenanthrene in a Mycobacterium sp. isolated from polycyclic aromatic hydrocarbon contaminated river sediments. Can J Microbiol. 1999;45:520–529. doi: 10.1139/cjm-45-6-520. [DOI] [PubMed] [Google Scholar]
  • 115.Mohan S., Takuro K., Takeru O., Robert K., Yoshihisa S. Bioremediation technologies for treatment of PAH-contaminated soil and strategies to enhance process efficiency. Rev Environ Sci Biotechnol. 2006;5:347–374. doi: 10.1007/s11157-006-0004-1. [DOI] [Google Scholar]
  • 116.Demane che S., Meyer C., Micoud J., Louwagie M., Willison J.C., Jouanneaul Y. Identification and functional analysis of two aromatic-ring-hydroxylating dioxygenases from a Sphingomonas strain that degrades various polycyclic aromatic hydrocarbons. Appl Environ Microbiol. 2004;70:6714–6725. doi: 10.1128/AEM.70.11.6714-6725.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 117.Gilbert E.S., Crowley D.E. Plant compounds that induce polychlorinated biphenyl biodegradation by Arthrobacter sp. strain B1B. Appl Environ Microbiol. 1997;63:1933–1938. doi: 10.1128/aem.63.5.1933-1938.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 118.Ohtsubo Y., Shimura M., Delawary M., Kimbara K., Takagi M., Kudo T., Ohta A., Nagata Y. Novel approach to the improvement of biphenyl and polychlorinated biphenyl degradation activity: promoter implantation by homologous recombination. Appl Environ Microbiol. 2003;69:146–153. doi: 10.1128/AEM.69.1.146-153.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 119.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]
  • 120.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]
  • 121.Kauppi B., Lee K., Carredano E., Parales R.E., Gibson D.T., Eklund H., Ramaswamy S. Structure of an aromatic-ring-hydroxylating dioxygenase-naphthalene 1,2-dioxygenase. Structure. 1998;6:571–586. doi: 10.1016/S0969-2126(98)00059-8. [DOI] [PubMed] [Google Scholar]
  • 122.Parales R.E., Lee K., Resnick S.M., Jiang H.Y., Lessner D.J., Gibson D.T. Substrate specificity of naphthalene dioxygenase: effect of specific amino acids at the active site of the enzyme. J BacterioL. 2000;182:1641–1649. doi: 10.1128/JB.182.6.1641-1649.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 123.Furusawa Y., Nagarajan V., Tanokura M., Masai E., Fukuda M., Senda T. Crystal structure of the terminal oxygenase component of biphenyl dioxygenase derived from Rhodococcus sp. strain RHA1. J Mol Biol. 2004;342:1041–1052. doi: 10.1016/j.jmb.2004.07.062. [DOI] [PubMed] [Google Scholar]
  • 124.Jouanneau Y., Meyer C., Jakoncic J., Stojanoff V., Gaillard J. Characterization of a naphthalene dioxygenase endowed with an exceptionally broad substrate specificity toward polycyclic aromatic hydrocarbons. Biochemistry. 2006;45:12380–12391. doi: 10.1021/bi0611311. [DOI] [PubMed] [Google Scholar]
  • 125.Hammel K.E., Kalyanaraman B., Kirk T.K. Oxidation of polycyclic aromatic-hydrocarbons and dibenzo P-dioxins by phanerochaete-chrysosporium ligninase. J Biol Chem. 1986;261:6948–6952. [PubMed] [Google Scholar]
  • 126.Ang E.L., Zhao H., Obbard J.P. Recent advances in the bioremediation of persistent organic pollutants via biomolecular engineering. Enz Microbial Technol. 2005;37:487–496. doi: 10.1016/j.enzmictec.2004.07.024. [DOI] [Google Scholar]
  • 127.Bulter T., Alcalde T., Sieber V., Meinhold P., Schlachtbauer C., Arnold F.H. Functional expression of a fungal laccase in Saccharomyces cerevisiae by directed evolution. Appl Environ Microbiol. 2003;69:987–995. doi: 10.1128/AEM.69.2.987-995.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 128.Alcalde M., Ferrer M., Plou F.J., Ballesteros A. Environmental biocatalysis: from remediation with enzymes to novel green processes. Trends Biotechnol. 2006;24:281–287. doi: 10.1016/j.tibtech.2006.04.002. [DOI] [PubMed] [Google Scholar]
  • 129.Harford-Cross C.F., Carmichael A.B., Allan A.K., England P.A., Rouch D.A., Wong L.L. Protein engineering of cytochrome P450(cam) (CYP101) for the oxidation of polycyclic aromatic hydrocarbons. Prot Eng. 2000;13:121–128. doi: 10.1093/protein/13.2.121. [DOI] [PubMed] [Google Scholar]
  • 130.Carmichael A.B., Wong L.L. Protein engineering of Bacillus megaterium CYP102-the oxidation of polycyclic aromatic hydrocarbons. Eur J Biochem. 2001;268:3117–3125. doi: 10.1046/j.1432-1327.2001.02212.x. [DOI] [PubMed] [Google Scholar]
  • 131.Li Q.S., Ogawa J., Schmid R.D., Shimizu S. Engineering cytochrome P450BM-3 for oxidation of polycyclic aromatic hydrocarbons. Appl Environ Microbiol. 2001;67:5735–5739. doi: 10.1128/AEM.67.12.5735-5739.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 132.Joo Z.L., Lin, Arnold F.H. Laboratory evolution of peroxide-mediated cytochrome P450 hydroxylation. Nature. 1999;399:670–673. doi: 10.1038/21395. [DOI] [PubMed] [Google Scholar]
  • 133.Salazar O., Cirino P.C., Arnold F.H. Thermostabilization of a cytochrome p450 peroxygenase. Chembiochem. 2003;4:891–893. doi: 10.1002/cbic.200300660. [DOI] [PubMed] [Google Scholar]
  • 134.Belotte D., Curien J.B., Maclean R.C., Bell G. An experimental test of local adaptation in soil bacteria. Evolution. 2003;57:27–36. doi: 10.1111/j.0014-3820.2003.tb00213.x. [DOI] [PubMed] [Google Scholar]
  • 135.Law A.M., Aitken M.D. Bacterial chemotaxis to naphthalene desorbing from a nonaqueous liquid. Appl Environ Microbiol. 2003;69:5968–5973. doi: 10.1128/AEM.69.10.5968-5973.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 136.Bhushan B. Chemotaxis and biodegradation of 3-methyl-4-nitrophenol by Ralstonia sp. SJ98. Biochem Biophy Res Commun. 2000;275:129–133. doi: 10.1006/bbrc.2000.3216. [DOI] [PubMed] [Google Scholar]
  • 137.Bhushan B. Chemotaxis and biodegradation of 3-methyl-4-nitrophenol by Ralstonia sp. SJ98. Biochem Biophy Res Commun. 2000;275:129–133. doi: 10.1006/bbrc.2000.3216. [DOI] [PubMed] [Google Scholar]
  • 138.Gentry T.J., Rensing C., Pepper I.L. New approaches for bioaugmentation as a remediation technology. Cri Rev Environ Sci Technol. 2004;34:447–494. doi: 10.1080/10643380490452362. [DOI] [Google Scholar]
  • 139.Kuiper I., Lagendijk E.L., Bloemberg G.V., Lugtenberg B.J.J. Rhizoremediation: a beneficial plant-microbe interaction. Mol Plant Microbe Interact. 2004;17:6–15. doi: 10.1094/MPMI.2004.17.1.6. [DOI] [PubMed] [Google Scholar]
  • 140.Wu C.H., Wood T.K., Mulchandani A., Chen W. Engineering plant-microbe symbiosis for rhizoremediation of heavy metals. Appl Environ Microbiol. 2006;72:1129–1134. doi: 10.1128/AEM.72.2.1129-1134.2006. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 141.Barac T., Taghavi S., Borremans B., Provoost A., Oeyen L., Colpaert J.V. Engineered endophytic bacteria improve phytoremediation of water-soluble, volatile, organic pollutants. Nat Biotechnol. 2004;22:583–588. doi: 10.1038/nbt960. [DOI] [PubMed] [Google Scholar]
  • 142.Villacieros M., Whelan C., Mackova M., Molgaard J., Sánchez-Contreras M., Lloret J. Polychlorinated biphenyl rhizoremediation by Pseudomonas fluorescens F113 derivatives, using a Sinorhizobium meliloti nod system to drive bph gene expression. Appl Environ Microbiol. 2005;71:2687–2694. doi: 10.1128/AEM.71.5.2687-2694.2005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 143.Kuiper I., Kravchenko L.V., Bloemberg G.V., Lugtenberg B.J.J. Pseudomonas putida strain PCL1444, selected for efficient root colonization and naphthalene degradation, effectively utilizes root exudate components. Mol Plant Microbe Interact. 2002;15:734–741. doi: 10.1094/MPMI.2002.15.7.734. [DOI] [PubMed] [Google Scholar]
  • 144.Monti M.R., Smania A.M., Fabro G., Alvarez M.E., Argaraña C.E. Engineering Pseudomonas fluorescens for biodegradation of 2,4-dinitrotoluene. Appl Environ Microbiol. 2005;71:8864–8872. doi: 10.1128/AEM.71.12.8864-8872.2005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 145.Crowley D.E., Brennerova M.V., Irwin C., Brenner V., Focht D.D. Rhizosphere effects on biodegradation of 2,5-dichlorobenzoate by a bioluminescent strain of root-colonizing Pseudomonas fluorescens. FEMS Microbiol Ecol. 1996;20:79–89. doi: 10.1111/j.1574-6941.1996.tb00307.x. [DOI] [Google Scholar]
  • 146.Kuiper I., Bloemberg G.V., Lugtenberg B.J. Selection of a plant-bacterium pair as a novel tool for rhizostimulation of polycyclic aromatic hydrocarbon-degrading bacteria. Mol Plant Microbe Interact. 2001;14:1197–1205. doi: 10.1094/MPMI.2001.14.10.1197. [DOI] [PubMed] [Google Scholar]
  • 147.Liu L., Jiang C.-Y., Liu X.-Y., Wu J.-F., Ha J.-G., Liu S.-J. Plant-microbe association for rhizoremediation of chloronitroaromatic pollutants with Comamonas sp. strain CNB-1. Environ Microbiol. 2007;9:465–473. doi: 10.1111/j.1462-2920.2006.01163.x. [DOI] [PubMed] [Google Scholar]
  • 148.Child R., Miller C., Liang Y., Narasimham G., Chatterton J., Harrison P., Sims R., Britt D., Anderson A. Polycyclic aromatic hydrocarbon-degrading Mycobacterium isolates: their association with plant roots. Appl Microbiol Biotechnol. 2007;75:655–663. doi: 10.1007/s00253-007-0840-0. [DOI] [PubMed] [Google Scholar]
  • 149.Hamme J.D., Singh A., Ward O.P. Recent advances in petroleum microbiology. Microbiol Mol Biol Rev. 2003;67:503–549. doi: 10.1128/MMBR.67.4.503-549.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]

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