Abstract
Polycyclic aromatic hydrocarbons (PAHs) are ubiquitous in the natural environment and easily accumulate in soil and sediment due to their low solubility and high hydrophobicity, rendering them less available for biological degradation. However, microbial degradation is a promising mechanism which is responsible for the ecological recovery of PAH-contaminated soil and sediment for removing these recalcitrant compounds compared with chemical degradation of PAHs. The goal of this review is to provide an outline of the current knowledge of biodegradation of PAHs in related aspects. Over 102 publications related to PAH biodegradation in soil and sediment are compiled, discussed, and analyzed. This review aims to discuss PAH degradation under various redox potential conditions, the factors affecting the biodegradation rates, degrading bacteria, the relevant genes in molecular monitoring methods, and some recent-year bioremediation field studies. The comprehensive understanding of the bioremediation kinetics and molecular means will be helpful for optimizing and monitoring the process, and overcoming its limitations in practical projects.
Similar content being viewed by others
References
Allen CCR, Boyd DR, Hempenstall F, Larkin MJ, Sharma ND (1999) Contrasting effects of a nonionic surfactant on the biotransformation of polycyclic aromatic hydrocarbons to cis-dihydrodiols by soil bacteria. Appl Environ Microbiol 65:1335–1339
Ambrosoli R, Petruzzelli L, Minati JL, Marsan FA (2005) Anaerobic PAH degradation in soil by a mixed bacterial consortium under denitrifying conditions. Chemosphere 60:1231–1236
Leeson A, Alleman BC (eds) (1999) Bioremediation technologies for polycyclic aromatic hydrocarbon compounds. Battelle, Columbus
Annweiler E, Richnow HH, Antranikian G, Hebenbrock S, Garms C, Franke S, Francke W, Michaelis W (2000) Naphthalene degradation and incorporation of naphthalene-derived carbon into biomass by the thermophile Bacillus thermoleovorans. Appl Environ Microbiol 66:518–523
Arzayus KM, Dickhut RM, Canuel EA (2002) Effects of physical mixing on the attenuation of polycyclic aromatic hydrocarbons in estuarine sediments. Org Geochem 33:1759–1769
Avramova T, Sotirova A, Galabova D, Karpenko E (2008) Effect of Triton X-100 and rhamnolipid PS-17 on the mineralization of phenanthrene by Pseudomonas sp cells. Int Biodeter Biodegr 62:415–420
Bach QD, Kim SJ, Choi SC, Oh YS (2005) Enhancing the intrinsic bioremediation of PAH-contaminated anoxic estuarine sediments with biostimulating agents. J Microbiol 43(4):319–324
Bamforth SM, Singleton I (2005) Bioremediation of polycyclic aromatic hydrocarbons: current knowledge and future directions. J Chem Technol Biot 80:723–736
Bautista LF, Sanz R, Molina MC, Gonzalez N, Sanchez D (2009) Effect of different non-ionic surfactants on the biodegradation of PAHs by diverse aerobic bacteria. Int Biodeter Biodegr 63:913–922
Betancur-Galvis LA, Alvarez-Bernal D, Ramos-Valdivia AC, Dendooven L (2006) Bioremediation of polycyclic aromatic hydrocarbon-contaminated saline–alkaline soils of the former Lake Texcoco. Chemosphere 62:1749–1760
Bewley RJF, Webb G (2001) In situ bioremediation of groundwater contaminated with phenols, BTEX and PAHs using nitrate as electron acceptor. Land Contam Reclamat 9(4):335–347
Boonchan S, Britz ML, Stanley GA (1998) Surfactant-enhanced biodegradation of high molecular weight polycyclic aromatic hydrocarbons by Stenotrophomonas maltophilia. Biotechnol Bioeng 59:482–494
Breedveld GD, Sparrevik M (2000) Nutrient-limited biodegradation of PAH in various soil strata at a creosote contaminated site. Biodegradation 11:391–399
Bregnard TPA, Hohener P, Haner A, Zeyer J (1996) Degradation of weathered diesel fuel by microorganisms from a contaminated aquifer in aerobic and anaerobic microcosms. Environ Toxicol Chem 15:299–307
Carriere PPE, Mesania FA (1995) Enhanced biodegradation of creosote-contaminated soil. Waste Manage 15:579–583
Cebron A, Norini MP, Beguiristain T, Leyval C (2008) Real-time PCR quantification of PAH-ring hydroxylating dioxygenase (PAH-RHD alpha) genes from Gram positive and Gram negative bacteria in soil and sediment samples. J Microbiol Meth 73:148–159
Chang BV, Chang IT, Yuan SY (2008) Anaerobic degradation of phenanthrene and pyrene in mangrove sediment. B Environ Contam Tox 80:145–149
Chang BV, Chang SW, Yuan SY (2003) Anaerobic degradation of polycyclic aromatic hydrocarbons in sludge. Adv Environ Res 7:623–628
Chen JF, Wong MH, Wong YS, Tam NFY (2008) Multi-factors on biodegradation kinetics of polycyclic aromatic hydrocarbons (PAHs) by Sphingomonas sp a bacterial strain isolated from mangrove sediment. Mar Pollut Bull 57:695–702
Coates JD, Anderson RT, Lovley DR (1996) Oxidation of polycyclic aromatic hydrocarbons under sulfate-reducing conditions. Appl Environ Microbiol 62:1099–1101
Dandie CE, Thomas SM, Bentham RH, McClure NC (2004) Physiological characterization of Mycobacterium sp strain 1B isolated from a bacterial culture able to degrade high-molecular-weight polycyclic aromatic hydrocarbons. J Appl Microbiol 97:246–255
DeBruyn JM, Mead TJ, Wilhelm SW, Sayler GS (2009) PAH biodegradative genotypes in Lake Erie sediments: evidence for broad geographical distribution of pyrene-degrading mycobacteria. Environ Sci Technol 43:3467–3473
Desai AM, Autenrieth RL, Dimitriou-Christidis P, McDonald TJ (2008) Biodegradation kinetics of select polycyclic aromatic hydrocarbon (PAH) mixtures by Sphingomonas paucimobilis EPA505. Biodegradation 19:223–233
Di Gennaro P, Rescalli E, Galli E, Sello G, Bestetti G (2001) Characterization of Rhodococcus opacus R7, a strain able to degrade naphthalene and o-xylene isolated from a polycyclic aromatic hydrocarbon-contaminated soil. Res Microbiol 152:641–651
Dou JF, Liu X, Ding AZ (2009) Anaerobic degradation of naphthalene by the mixed bacteria under nitrate reducing conditions. J Hazard Mater 165:325–331
Eriksson M, Sodersten E, Yu ZT, Dalhammar G, Mohn WW (2003) Degradation of polycyclic aromatic hydrocarbons at low temperature under aerobic and nitrate-reducing conditions in enrichment cultures from northern soils. Appl Environ Microbiol 69:275–284
Franzetti A, Caredda P, Ruggeri C, Colla PL, Tamburini E, Papacchini M, Bestetti G (2009) Potential applications of surface active compounds by Gordonia sp. strain BS29 in soil remediation technologies. Chemosphere 75:801–807
Fuenmayor SL, Wild M, Boyes AL, Williams PA (1998) A gene cluster encoding steps in conversion of naphthalene to gentisate in Pseudomonas sp. strain U2. J Bacteriol 180:2522–2530
Geiselbrecht AD, Hedlund BP, Tichi MA, Staley JT (1998) Isolation of marine polycyclic aromatic hydrocarbon (PAH)-degrading Cycloclasticus strains from the Gulf of Mexico and comparison of their PAH degradation ability with that of Puget Sound Cycloclasticus strains. Appl Environ Microbiol 64:4703–4710
Gopishetty SR, Heinemann J, Deshpande M, Rosazza JPN (2007) Aromatic oxidations by Streptomyces griseus: biotransformations of naphthalene to 4-hydroxy-1-tetralone. Enzyme Microb Tech 40:1622–1626
Guha S, Jaffe PR, Peters CA (1998) Bioavailability of mixtures of PAHs partitioned into the micellar phase of a nonionic surfactant. Environ Sci Technol 32:2317–2324
Habe H, Omori T (2003) Genetics of polycyclic aromatic hydrocarbon metabolism in diverse aerobic bacteria. Biosci Biotechnol Biochem 67:225–243
Haritash AK, Kaushik CP (2009) Biodegradation aspects of polycyclic aromatic hydrocarbons (PAHs): a review. J Hazard Mater 169:1–15
Hedlund BP, Geiselbrecht AD, Bair TJ, Staley JT (1999) Polycyclic aromatic hydrocarbon degradation by a new marine bacterium, Neptunomonas naphthovorans gen. nov., sp. nov. Appl Environ Microbiol 65:251–259
Hickey AM, Gordon L, Dobson ADW, Kelly CT, Doyle EM (2007) Effect of surfactants on fluoranthene degradation by Pseudomonas alcaligenes PA-10. Appl Microbiol Biotechnol 74:851–856
Jakoncic J, Jouanneau Y, Meyer C, Stojanoff V (2007) The catalytic pocket of the ring-hydroxylating dioxygenase from Sphingomonas CHY-1. Biochem Biophys Res Commun 352:861–866
Jang SA, Lee DS, Lee MW, Woo SH (2007) Toxicity of phenanthrene dissolved in nonionic surfactant solutions to Pseudomonas putida P2. FEMS Microbiol Lett 267:194–199
Jin DY, Jiang X, Jing X, Ou ZQ (2007) Effects of concentration, head group, and structure of surfactants on the degradation of phenanthrene. J Hazard Mater 144:215–221
Johnson K, Ghosh S (1998) Feasibility of anaerobic biodegradation of PAHs in dredged river sediments. Water Sci Technol 38:41–48
Kastner M, Breuer-Jammali M, Mahro B (1998) Impact of inoculation protocols, salinity, and pH on the degradation of polycyclic aromatic hydrocarbons (PAHs) and survival of PAH-degrading bacteria introduced into soil. Appl Environ Microbiol 64:359–362
Kim HS, Lindsay KS, Pfaender FK (2008) Enhanced mobilization of field contaminated soil-bound PAHs to the aqueous phase under anaerobic conditions. Water Air Soil Poll 189:135–147
Kim HS, Weber WJ (2003) Preferential surfactant utilization by a PAH-degrading strain: effects on micellar solubilization phenomena. Environ Sci Technol 37:3574–3580
Kim HS, Weber WJ (2005) Polycyclic aromatic hydrocarbon behavior in bioactive soil slurry reactors amended with a nonionic surfactant. Environ Toxicol Chem 24:268–276
Kim IS, Park JS, Kim KW (2001) Enhanced biodegradation of polycyclic aromatic hydrocarbons using nonionic surfactants in soil slurry. Appl Geochem 16:1419–1428
Kim TJ, Lee EY, Kim YJ, Cho KS, Ryu HW (2003) Degradation of polyaromatic hydrocarbons by Burkholderia cepacia 2A-12. World J Microb Biot 19:411–417
Kim YH, Freeman JP, Moody JD, Engesser KH, Cerniglia CE (2005) Effects of pH on the degradation of phenanthrene and pyrene by Mycobacterium vanbaalenii PYR-1. Appl Microbiol Biotechnol 67:275–285
Kimura N, Kitagawa W, Mori T, Nakashima N, Tamura T, Kamagata Y (2006) Genetic and biochemical characterization of the dioxygenase involved in lateral dioxygenation of dibenzofuran from Rhodococcus opacus strain SAO101. Appl Microbiol Biotechnol 73:474–484
Lei L, Khodadoust AP, Suidan MT, Tabak HH (2005) Biodegradation of sediment-bound PAHs in field contaminated sediment. Water Res 39:349–361
Li JL, Bai RB (2005) Effect of a commercial alcohol ethoxylate surfactant (C11-15E7) on biodegradation of phenanthrene in a saline water medium by Neptunomonas naphthovorans. Biodegradation 16:57–65
Lu XY, Zhang T, Fang HHP, Leung KMY, Zhang G (2010) Biodegradation of naphthalene by enriched marine denitrifying bacteria. Int Biodeter Biodegr. doi:10.1016/j.ibiod.2010.11.004
Liang YN, Britt DW, McLean JE, Sorensen DL, Sims RC (2007) Humic acid effect on pyrene degradation: finding an optimal range for pyrene solubility and mineralization enhancement. Appl Microbiol Biotechnol 74:1368–1375
Lloyd-Jones G, Laurie AD, Hunter DWF, Fraser R (1999) Analysis of catabolic genes for naphthalene and phenanthrene degradation in contaminated New Zealand soils. FEMS Microbiol Ecol 29:69–79
Ma YF, Wang L, Shao ZZ (2006) Pseudomonas, the dominant polycyclic aromatic hydrocarbon-degrading bacteria isolated from Antarctic soils and the role of large plasmids in horizontal gene transfer. Environ Microbiol 8:455–465
MacRae JD, Hall KJ (1998) Biodegradation of polycyclic aromatic hydrocarbons (PAH) in marine sediment under denitrifying conditions. Water Sci Technol 38:177–185
Maletic S, Dalmacija B, Roncevic S, Agbaba J, Petrovic O (2009) Degradation kinetics of an aged hydrocarbon-contaminated soil. Water Air Soil Pollut 202(1-4):149–159
McNally DL, Mihelcic JR, Lueking DR (1998) Biodegradation of three- and four-ring polycyclic aromatic hydrocarbons under aerobic and denitrifying conditions. Environ Sci Technol 32:2633–2639
Meckenstock RU, Safinowski M, Griebler C (2004) Anaerobic degradation of polycyclic aromatic hydrocarbons. FEMS Microbiol Ecol 49:27–36
Mihelcic JR, Luthy RG (1988) Degradation of polycyclic aromatic hydrocarbon compounds under various redox conditions in soil–water systems. Appl Environ Microbiol 54:1182–1187
Moody JD, Freeman JP, Doerge DR, Cerniglia CE (2001) Degradation of phenanthrene and anthracene by cell suspensions of Mycobacterium sp strain PYR-1. Appl Environ Microbiol 67:1476–1483
Mrozik A, Piotrowska-Seget Z, Labuzek S (2003) Bacterial degradation and bioremediation of polycyclic aromatic hydrocarbons. Pol J Environ Stud 12:15–25
Mulligan CN, Yong RN, Gibbs BF (2001) Surfactant-enhanced remediation of contaminated soil: a review. Eng Geol 60:371–380
Musat F, Galushko A, Jacob J, Widdel F, Kube M, Reinhardt R, Wilkes H, Schink B, Rabus R (2009) Anaerobic degradation of naphthalene and 2-methylnaphthalene by strains of marine sulfate-reducing bacteria. Environ Microbiol 11:209–219
Nestler C, Hansen LD, Ringelberg D, Talley JW (2001) Remediation of soil PAH: comparison of biostimulation and bioaugmentation. In: Magar VS, VonFahnestock FM, Leeson A (eds) Ex situ biological treatment technologies, vol 6. Bioremediation series, vol 6. Battelle, Columbus, pp 43–50
Ortiz I, Auria R, Sigoillot JC, Revah S (2003) Enhancing phenanthrene biomineralization in a polluted soil using gaseous toluene as a cosubstrate. Environ Sci Technol 37(4):805–810
Park JW, Crowley DE (2006) Dynamic changes in nahAc gene copy numbers during degradation of naphthalene in PAH-contaminated soils. Appl Microbiol Biotechnol 72:1322–1329
Penfold J, Staples E, Tucker I, Thompson L, Thomas RK (2002) Adsorption of nonionic mixtures at the air–water interface: effects of temperature and electrolyte. J Colloid Interf Sci 247:404–411
Peng RH, Xiong AS, Xue Y, Fu XY, Gao F, Zhao W, Tian YS, Yao QH (2008) Microbial biodegradation of polyaromatic hydrocarbons. FEMS Microbiol Rev 32:927–955
Pumphrey GM, Madsen EL (2007) Naphthalene metabolism and growth inhibition by naphthalene in Polaromonas naphthalenivorans strain CJ2. Microbiology 153:3730–3738
Quantin C, Joner EJ, Portal JM, Berthelin J (2005) PAH dissipation in a contaminated river sediment under oxic and anoxic conditions. Environ Pollut 134:315–322
Ramsay JA, Li H, Brown RS, Ramsay BA (2003) Naphthalene and anthracene mineralization linked to oxygen, nitrate, Fe(III) and sulphate reduction in a mixed microbial population. Biodegradation 14:321–329
Hinchee RE, Wilson JT, Downey DC (eds) (1995) Intrinsic bioremediation. Battelle, Columbus
Rockne KJ, Chee-Sanford JC, Sanford RA, Hedlund BP, Staley JT, Strand SE (2000) Anaerobic naphthalene degradation by microbial pure cultures under nitrate-reducing conditions. Appl Environ Microbiol 66:1595–1601
Rockne KJ, Strand SE (1998) Biodegradation of bicyclic and polycyclic aromatic hydrocarbons in anaerobic enrichments. Environ Sci Technol 32:3962–3967
Rockne KJ, Strand SE (2001) Anaerobic biodegradation of naphthalene, phenanthrene, and biphenyl by a denitrifying enrichment culture. Water Res 35:291–299
Saito A, Iwabuchi T, Harayama S (2000) A novel phenanthrene dioxygenase from Nocardioides sp strain KP7: expression in Escherichia coli. J Bacteriol 182:2134–2141
Santos EC, Jacques RJS, Bento FM, Peralba MDR, Selbach PA, Sa ELS, Camargo FAO (2008) Anthracene biodegradation and surface activity by an iron-stimulated Pseudomonas sp. Bioresour Technol 99:2644–2649
Sartoros C, Yerushalmi L, Beron P, Guiot SR (2005) Effects of surfactant and temperature on biotransformation kinetics of anthracene and pyrene. Chemosphere 61:1042–1050
Seeliger S, Cord-Ruwisch R, Schink B (1998) A periplasmic and extracellular c-type cytochrome of Geobacter sulfurreducens acts as a ferric iron reductase and as an electron carrier to other acceptors or to partner bacteria. J Bacteriol 180:3686–3691
Seo Y, Bishop PL (2007) Influence of nonionic surfactant on attached biofilm formation and phenanthrene bioavailability during simulated surfactant enhanced bioremediation. Environ Sci Technol 41:7107–7113
Šepič E, Bricelj M, Leskovsek H (1998) Degradation of fluoranthene by Pasteurella sp IFA and Mycobacterium sp PYR-1: isolation and identification of metabolites. J Appl Microbiol 85:746–754
Shao MF, Zhang T, Fang HHP (2009) Autotrophic denitrification and its effect on metal speciation during marine sediment remediation. Water Res 43:2961–2968
Smith KE, Schwab AP, Banks MK (2008) Dissipation of PAHs in saturated, dredged sediments: a field trial. Chemosphere 72(10):1614–1619
Stach JEM, Burns RG (2002) Enrichment versus biofilm culture: a functional and phylogenetic comparison of polycyclic aromatic hydrocarbon-degrading microbial communities. Environ Microbiol 4:169–182
Su D, Li PJ, Stagnitti F, Xiong XZ (2006) Biodegradation of benzo a pyrene in soil by Mucor sp SF06 and Bacillus sp SB02 co-immobilized on vermiculite. J Environ Sci China 18:1204–1209
Teng Y, Luo YM, Ping LF, Zou DX, Li ZA, Christie P (2010) Effects of soil amendment with different carbon sources and other factors on the bioremediation of an aged PAH-contaminated soil. Biodegradation 21(2):167–178
Uribe-Jongbloed A, Bishop PL (2007) Comparative study of PAH removal efficiency under absence of molecular oxygen: effect of electron acceptor and hydrodynamic conditions. J Environ Eng Sci 6:367–376
Valentin L, Feijoo G, Moreira MT, Lema JM (2006) Biodegradation of polycyclic aromatic hydrocarbons in forest and salt marsh soils by white-rot fungi. Int Biodeter Biodegr 58:15–21
Weissenfels WD, Beyer M, Klein J (1990) Degradation of phenanthrene, fluorene and fluoranthene by pure bacterial cultures. Appl Microbiol Biotechnol 32:479–484
Wong JWC, Fang M, Zhao ZY, Xing BS (2004) Effect of surfactants on solubilization and degradation of phenanthrene under thermophilic conditions. J Environ Qual 33:2015–2025
Xia X, Wang R (2008) Effect of sediment particle size on polycyclic aromatic hydrocarbon biodegradation: importance of the sediment–water interface. Environ Toxicol Chem 27:119–125
Xia XH, Yu H, Yang ZF, Huang GH (2006) Biodegradation of polycyclic aromatic hydrocarbons in the natural waters of the Yellow River: effects of high sediment content on biodegradation. Chemosphere 65:457–466
Yuan SY, Chang BV (2007) Anaerobic degradation of five polycyclic aromatic hydrocarbons from river sediment in Taiwan. J Environ Sci Heal B 42:63–69
Yuan SY, Chang JS, Yen JH, Chang BV (2001) Biodegradation of phenanthrene in river sediment. Chemosphere 43:273–278
Zeinali M, Vossoughi M, Ardestani SK (2008) Naphthalene metabolism in Nocardia otitidiscaviarum strain TSH1, a moderately thermophilic microorganism. Chemosphere 72:905–909
Zhang GY, Ling JY, Sun HB, Luo J, Fan YY, Cui ZJ (2009a) Isolation and characterization of a newly isolated polycyclic aromatic hydrocarbons-degrading Janibacter anophelis strain JY11. J Hazard Mater 172:580–586
Zhang M, Zhang T, Shao MF, Fang HHP (2009b) Autotrophic denitrification in nitrate-induced marine sediment remediation and Sulfurimonas denitrificans-like bacteria. Chemosphere 76:677–682
Zhang WX, Bouwer EJ (1997) Biodegradation of benzene, toluene and naphthalene in soil–water slurry microcosms. Biodegradation 8:167–175
Zhang XM, Young LY (1997) Carboxylation as an initial reaction in the anaerobic metabolism of naphthalene and phenanthrene by sulfidogenic consortia. Appl Environ Microbiol 63:4759–4764
Zhao BW, Zhu LZ, Li W, Chen BL (2005) Solubilization and biodegradation of phenanthrene in mixed anionic-nonionic surfactant solutions. Chemosphere 58:33–40
Zheng XJ, Blais JF, Mercier G, Bergeron M, Drogui P (2007) PAH removal from spiked municipal wastewater sewage sludge using biological, chemical and electrochemical treatments. Chemosphere 68:1143–1152
Zhou HW, Guo CL, Wong YS, Tam NFY (2006) Genetic diversity of dioxygenase genes in polycyclic aromatic hydrocarbon-degrading bacteria isolated from mangrove sediments. FEMS Microbiol Lett 262:148–157
Zhou QX, Hua T (2004) Bioremediation: a review of applications and problems to be resolved. Prog Nat Sci 14:937–944
Acknowledgments
The authors wish to thank the Hong Kong Research Grants Council for the financial support of this study (HKU7122/10E). Xiao-Ying Lu wishes to thank HKU for the postgraduate studentship.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Lu, XY., Zhang, T. & Fang, H.HP. Bacteria-mediated PAH degradation in soil and sediment. Appl Microbiol Biotechnol 89, 1357–1371 (2011). https://doi.org/10.1007/s00253-010-3072-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-010-3072-7