Abstract
Bioremediation is an environmental sustainable and cost-effective technology for the cleanup of hydrocarbon-polluted soils and coasts. In spite of that longer times are usually required compared with physicochemical strategies, complete degradation of the pollutant can be achieved, and no further confinement of polluted matrix is needed. Microbial aerobic degradation is achieved by the incorporation of molecular oxygen into the inert hydrocarbon molecule and funneling intermediates into central catabolic pathways. Several families of alkane monooxygenases and ring hydroxylating dioxygenases are distributed mainly among Proteobacteria, Actinobacteria, Firmicutes and Fungi strains. Catabolic routes, regulatory networks, and tolerance/resistance mechanisms have been characterized in model hydrocarbon-degrading bacteria to understand and optimize their metabolic capabilities, providing the basis to enhance microbial fitness in order to improve hydrocarbon removal. However, microbial communities taken as a whole play a key role in hydrocarbon pollution events. Microbial community dynamics during biodegradation is crucial for understanding how they respond and adapt to pollution and remediation. Several strategies have been applied worldwide for the recovery of sites contaminated with persistent organic pollutants, such as polycyclic aromatic hydrocarbons and petroleum derivatives. Common strategies include controlling environmental variables (e.g., oxygen availability, hydrocarbon solubility, nutrient balance) and managing hydrocarbon-degrading microorganisms, in order to overcome the rate-limiting factors that slow down hydrocarbon biodegradation.
Similar content being viewed by others
References
Abbasnezhad H, Gray M, Foght JM (2011) Influence of adhesion on aerobic biodegradation and bioremediation of liquid hydrocarbons. Appl Microbiol Biotechnol 92:653–675. doi:10.1007/s00253-011-3589-4
Agulló L, Cámara B, Martínez P, Latorre V, Seeger M (2007) Response to (chloro)biphenyls of the polychlorobiphenyl-degrader Burkholderia xenovorans LB400 involves stress proteins also induced by heat shock and oxidative stress. FEMS Microbiol Lett 267:167–175. doi:10.1111/j.1574-6968.2006.00554.x
Altimira F, Yáñez C, Bravo G, González M, Rojas L, Seeger M (2012) Characterization of copper-resistant bacteria and bacterial communities from copper-polluted agricultural soils of central Chile. BMC Microbiol 12:193. doi:10.1186/1471-2180-12-193
American Petroleum Institute, Petroleum HPV Testing Group (2010) Revised robust summary and test plan for kerosene/jet fuels. http://www.epa.gov/chemrtk/pubs/summaries/kerjetfc/c15020tc.htm. Accessed 20 Jan 2014
Atlas RM, Hazen TC (2011) Oil biodegradation and bioremediation: a tale of the two worst spills in U.S. history. Environ Sci Technol 45:6709–6715. doi:10.1021/es2013227
Atlas R, Philp J (2005) Bioremediation: applied microbial solutions for real-world environmental cleanup. ASM, Washington, DC
Baboshin MA, Golovleva LA (2012) Aerobic bacterial degradation of polycyclic aromatic hydrocarbons (PAHs) and its kinetic aspects. Microbiology 81:639–650. doi:10.1134/S0026261712060021
Bragg JR, Prince RC, Harner EJ, Atlas RM (1994) Effectiveness of bioremediation for the Exxon Valdez oil spill. Nature 368:413–418. doi:10.1038/368413a0
Bučková M, Godočíková J, Zámocký M, Polek B (2010) Screening of bacterial isolates from polluted soils exhibiting catalase and peroxidase activity and diversity of their responses to oxidative stress. Curr Microbiol 61:241–247. doi:10.1007/s00284-010-9601-x
Callaghan AV, Gieg LM, Kropp KG, Suflita JM, Young LY (2006) Comparison of mechanisms of alkane metabolism under sulfate-reducing conditions among two bacterial isolates and a bacterial consortium. Appl Environ Microbiol 72:4274–4282. doi:10.1128/AEM.02896-05
Callaghan AV, Morris BEL, Pereira IAC, McInerney MJ, Austin RN, Groves JT, Kukor JJ, Suflita JM, Young LY, Zylstra GJ, Wawrik B (2012) The genome sequence of Desulfatibacillum alkenivorans AK-01: a blueprint for anaerobic alkane oxidation. Environ Microbiol 14:101–113. doi:10.1111/j.1462-2920.2011.02516.x
Cámara B, Herrera C, González M, Couve E, Hofer B, Seeger M (2004) From PCBs to highly toxic metabolites by the biphenyl pathway. Environ Microbiol 6:842–850. doi:10.1111/j.1462-2920.2004.00630.x
Cámara B, Seeger M, González M, Standfuß-Gabisch C, Kahl S, Hofer B (2007) Generation by a widely applicable approach of a hybrid dioxygenase showing improved oxidation of polychlorobiphenyls. Appl Environ Microbiol 73:2682–2689. doi:10.1128/AEM.02523-06
Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci U S A 108:4516–4522. doi:10.1073/pnas.1000080107
Chain PSG, Denef VJ, Konstantinidis KT, Vergez LM, Agulló L, Reyes VL, Hauser L, Córdova M, Gómez L, González M, Land M, Lao V, Larimer F, LiPuma JJ, Mahenthiralingam E, Malfatti SA, Marx CJ, Parnell JJ, Ramette A, Richardson P, Seeger M, Smith D, Spilker T, Sul WJ, Tsoi TV, Ulrich LE, Zhulin IB, Tiedje JM (2006) Burkholderia xenovorans LB400 harbors a multi-replicon, 9.73-Mbp genome shaped for versatility. Proc Natl Acad Sci U S A 103:15280–15287. doi:10.1073/pnas.0606924103
Chávez-Gómez B, Quintero R, Esparza-García F, Mesta-Howard AM, Zavala Díaz de la Serna F, Hernández-Rodríguez C, Gillén T, Poggi-Varaldo H, Barrera-Cortés J, Rodríguez-Vázquez R (2003) Removal of phenanthrene from soil by co-cultures of bacteria and fungi pregrown on sugarcane bagasse pith. Bioresour Technol 89:177–183. doi:10.1016/S0960-8524(03)00037-3
Copley SD (2000) Evolution of a metabolic pathway for degradation of a toxic xenobiotic: the patchwork approach. Trends Biochem Sci 25:261–265. doi:10.1016/S0968-0004(00)01562-0
Das P, Mukherjee S, Sen R (2008) Genetic regulations of the biosynthesis of microbial surfactants: an overview. Biotechnol Genet Eng Rev 25:165–185. doi:10.5661/bger-25-165
Ding G-C, Heuer H, Zühlke S, Spiteller M, Pronk GJ, Heister K, Kögel-Knabner I, Smalla K (2010) Soil type-dependent responses to phenanthrene as revealed by determining the diversity and abundance of polycyclic aromatic hydrocarbon ring-hydroxylating dioxygenase genes by using a novel PCR detection system. Appl Environ Microbiol 76:4765–4771. doi:10.1128/AEM.00047-10
Domínguez-Cuevas P, González-Pastor J-E, Marqués S, Ramos J-L, de Lorenzo V (2006) Transcriptional tradeoff between metabolic and stress-response programs in Pseudomonas putida KT2440 cells exposed to toluene. J Biol Chem 281:11981–11991. doi:10.1074/jbc.M509848200
Grace Liu P-W, Chang TC, Whang L-M, Kao C-H, Pan P-T, Cheng S-S (2011) Bioremediation of petroleum hydrocarbon contaminated soil: effects of strategies and microbial community shift. Int Biodeterior Biodegrad 65:1119–1127. doi:10.1016/j.ibiod.2011.09.002
Hearn EM, Patel DR, Lepore BW, Indic M, van den Berg B (2009) Transmembrane passage of hydrophobic compounds through a protein channel wall. Nature 458:367–370. doi:10.1038/nature07678
Hernández M, Jia Z, Conrad R, Seeger M (2011) Simazine application inhibits nitrification and changes the ammonia-oxidizing bacterial communities in a fertilized agricultural soil. FEMS Microbiol Ecol 78:511–519. doi:10.1111/j.1574-6941.2011.01180.x
Iwai S, Johnson T, Chai B, Hashsham S, Tiedje JM (2011) Comparison of the specificities and efficacies of primers for aromatic dioxygenase gene analysis of environmental samples. Appl Environ Microbiol 77:3551–3557. doi:10.1128/AEM.00331-11
Jørgensen KS, Puustinen J, Suortti AM (2000) Bioremediation of petroleum hydrocarbon-contaminated soil by composting in biopiles. Environ Pollut 107:245–254. doi:10.1016/S0269-7491(99)00144-X
Kim SJ, Kweon O, Jones RC, Freeman JP, Edmondson RD, Cerniglia CE (2007) Complete and integrated pyrene degradation pathway in Mycobacterium vanbaalenii PYR-1 based on systems biology. J Bacteriol 189:464–472. doi:10.1128/JB.01310-06
Kweon O, Kim S, Freeman JP, Song J, Baek S, Cerniglia CE (2010) Substrate specificity and structural characteristics of the novel Rieske nonheme iron aromatic ring-hydroxylating oxygenases NidAB and NidA3B3 from Mycobacterium vanbaalenii PYR-1. mBio 1(2). doi:10.1128/mBio.00135-10
Labbé D, Margesin R, Schinner F, Whyte LG, Greer CW (2007) Comparative phylogenetic analysis of microbial communities in pristine and hydrocarbon-contaminated Alpine soils. FEMS Microbiol Ecol 59:466–475. doi:10.1111/j.1574-6941.2006.00250.x
Li L, Liu X, Yang W, Xu F, Wang W, Feng L, Bartlam M, Wang L, Rao Z (2008) Crystal structure of long-chain alkane monooxygenase (LadA) in complex with coenzyme FMN: unveiling the long-chain alkane hydroxylase. J Mol Biol 376:453–465. doi:10.1016/j.jmb.2007.11.069
Loman NJ, Misra RV, Dallman TJ, Constantinidou C, Gharbia SE, Wain J, Pallen MJ (2012) Performance comparison of benchtop high-throughput sequencing platforms. Nat Biotechnol 30:434–439. doi:10.1038/nbt.2198
Mackay D, Shiu WY, Ma KC, Lee SC (2006) Handbook of physical–chemical properties and environmental fate for organic chemicals. CRC, Boca Raton
Margesin R, Schinner F (2001) Bioremediation (natural attenuation and biostimulation) of diesel-oil-contaminated soil in an alpine glacier skiing area. Appl Environ Microbiol 67:3127–3133. doi:10.1128/AEM.67.7.3127
Margesin R, Labbe D, Schinner F, Greer CW, Whyte LG (2003) Characterization of hydrocarbon-degrading microbial populations in contaminated and pristine alpine soils. Appl Environ Microbiol 69:3085–3092. doi:10.1128/AEM.69.6.3085
McDonald IR, Miguez CB, Rogge G, Bourque D, Wendlandt KD, Groleau D, Murrell JC (2006) Diversity of soluble methane monooxygenase-containing methanotrophs isolated from polluted environments. FEMS Microbiol Lett 255:225–232. doi:10.1111/j.1574-6968.2005.00090.x
Méndez V, Fuentes S, Hernández M, Morgante V, González M, Moore E, Seeger M (2010) Isolation of hydrocarbon-degrading heavy-metal-resistant bacteria from crude oil-contaminated soil in central Chile. J Biotechnol 150:S287
Méndez V, Agulló L, González M, Seeger M (2011) The homogentisate and homoprotocatechuate central pathways are involved in 3- and 4-hydroxyphenylacetate degradation by Burkholderia xenovorans LB400. PLoS ONE 6:e17583. doi:10.1371/journal.pone.0017583
Morgante V, López-López A, Flores C, González M, González B, Vásquez M, Rosselló-Mora R, Seeger M (2010) Bioaugmentation with Pseudomonas sp. strain MHP41 promotes simazine attenuation and bacterial community changes in agricultural soils. FEMS Microbiol Ecol 71:114–126. doi:10.1111/j.1574-6941.2009.00790.x
Namkoong W, Hwang E-Y, Park J-S, Choi J-Y (2002) Bioremediation of diesel-contaminated soil with composting. Environ Pollut 119:23–31. doi:10.1016/S0269-7491(01)00328-1
Narasingarao P, Podell S, Ugalde JA, Brochier-Armanet C, Emerson JB, Brocks JJ, Heidelberg KB, Banfield JF, Allen EE (2012) De novo metagenomic assembly reveals abundant novel major lineage of Archaea in hypersaline microbial communities. ISME J 6:81–93. doi:10.1038/ismej.2011.78
Ní Chadhain SM, Norman RS, Pesce KV, Kukor JJ, Zylstra GJ (2006) Microbial dioxygenase gene population shifts during polycyclic aromatic hydrocarbon biodegradation. Appl Environ Microbiol 72:4078–4087. doi:10.1128/AEM.02969-05
Overwin H, González M, Méndez V, Seeger M, Wray V, Hofer B (2012) Dioxygenation of the biphenyl dioxygenation product. Appl Environ Microbiol 78:4529–4532. doi:10.1128/AEM.00492-12
Pagnout C, Frache G, Poupin P, Maunit B, Muller JF, Ferard JF (2007) Isolation and characterization of a gene cluster in PAH degradation in Mycobacterium sp. strain SNP11: expression in Mycobacterium smegmatis mc2155. Res Microbiol 158:175–186. doi:10.1016/j.resmic.2006.11.002
Peng R-H, Xiong A-S, Xue Y, Fu X-Y, Gao F, Zhao W, Tian Y-S, Yao Q-H (2008) Microbial biodegradation of polyaromatic hydrocarbons. FEMS Microbiol Rev 32:927–955. doi:10.1111/j.1574-6976.2008.00127.x
Pèrez-Armendáriz B, Loera-Corral O, Fernández-Linares L, Esparza-García F, Rodríguez-Vázquez R (2004) Biostimulation of microorganisms from sugarcane bagasse pith for the removal of weathered hydrocarbon from soil. Lett Appl Microbiol 38:373–377. doi:10.1111/j.1472-765X.2004.01502.x
Pieper DH, Seeger M (2008) Bacterial metabolism of polychlorinated biphenyls. J Mol Microbiol Biotechnol 15:121–138. doi:10.1159/000121325
Ponce BL, Latorre VK, González M, Seeger M (2011) Antioxidant compounds improved PCB-degradation by Burkholderia xenovorans strain LB400. Enzym Microb Technol 49:509–516. doi:10.1016/j.enzmictec.2011.04.021
Rojo F (2009) Degradation of alkanes by bacteria. Environ Microbiol 11:2477–2490. doi:10.1111/j.1462-2920.2009.01948.x
Roldán-Martín A, Esparza-García F, Calva-Calva G, Rodríguez-Vázquez R (2006) Effects of mixing low amounts of orange peel (Citrus reticulata) with hydrocarbon-contaminated soil in solid culture to promote remediation. J Environ Sci Health A Tox Hazard Subst Environ Eng 41:2373–2385. doi:10.1080/10934520600873548
Roldán-Martín A, Calva-Calva G, Rojas-Avelizapa N, Díaz-Cervantes MD, Rodríguez-Vázquez R (2007) Solid culture amended with small amounts of raw coffee beans for the removal of petroleum hydrocarbon from weathered contaminated soil. Int Biodeterior Biodegrad 60:35–39. doi:10.1016/j.ibiod.2006.10.008
Röling WF, Milner MG, Jones DM, Lee K, Daniel F, Swannell RJ, Head IM (2002) Robust hydrocarbon degradation and dynamics of bacterial communities during nutrient-enhanced oil spill bioremediation. Appl Environ Microbiol 68:5537–5548. doi:10.1128/AEM.68.11.5537
Romero-Silva MJ, Méndez V, Agulló L, Seeger M (2013) Genomic and functional analyses of the gentisate and protocatechuate ring-cleavage pathways and related 3-hydroxybenzoate and 4-hydroxybenzoate peripheral pathways in Burkholderia xenovorans LB400. PLoS ONE 8:e56038. doi:10.1371/journal.pone.0056038
Rosenberg M, Bayer EA, Delarea J, Rosenberg E (1982) Role of thin fimbriae in adherence and growth of Acinetobacter calcoaceticus RAG-1 on hexadecane. Appl Environ Microbiol 44:929–937
Ruberto L, Vazquez SC, Mac Cormack WP (2003) Effectiveness of the natural bacterial flora, biostimulation and bioaugmentation on the bioremediation of a hydrocarbon contaminated Antarctic soil. Int Biodeterior Biodegrad 52:115–125. doi:10.1016/S0964-8305(03)00048-9
Saavedra M, Acevedo F, González M, Seeger M (2010) Mineralization of PCBs by the genetically modified strain Cupriavidus necator JMS34 and its application for bioremediation of PCB in soil. Appl Microbiol Biotechnol 87:1543–1554. doi:10.1007/s00253-010-2575-6
Salminen JM, Tuomi PM, Jørgensen KS (2008) Functional gene abundances (nahAc, alkB, xylE) in the assessment of the efficacy of bioremediation. Appl Biochem Biotechnol 151(2–3):638–652. doi:10.1007/s12010-008-8275-3
Schneiker S, Martins dos Santos VA, Bartels D, Bekel T, Brecht M, Buhrmester J, Chernikova TN, Denaro R, Ferrer M, Gertler C, Goesmann A, Golyshina OV, Kaminski F, Khachane AN, Lang S, Linke B, McHardy AC, Meyer F, Nechitaylo T, Pühler A, Regenhardt D, Rupp O, Sabirova JS, Selbitschka W, Yakimov MM, Timmis KN, Vorhölter F-J, Weidner S, Kaiser O, Golyshin PN (2006) Genome sequence of the ubiquitous hydrocarbon-degrading marine bacterium Alcanivorax borkumensis. Nat Biotechnol 24:997–1004. doi:10.1038/nbt1232
Seeger M, Pieper D (2009) Genetics of biphenyl biodegradation and co-metabolism of PCBs. In: Timmis KN (ed) Microbiology of hydrocarbons, oils, lipids, and derived compounds, vol 2. Springer, Heidelberg, pp 1179–1199
Seeger M, Timmis KN, Hofer B (1997) Bacterial pathways for the degradation of polychlorinated biphenyls. Mar Chem 58:327–333. doi:10.1016/S0304-4203(97)00059-5
Seeger M, Zielinski M, Timmis KN, Hofer B (1999) Regiospecificity of dioxygenation of di- to pentachlorobiphenyls and their degradation to chlorobenzoates by the bph-encoded catabolic pathway of Burkholderia sp. strain LB400. Appl Environ Microbiol 65:3614–3621
Seeger M, Cámara B, Hofer B (2001) Dehalogenation, denitration, dehydroxylation, and angular attack on substituted biphenyls and related compounds by a biphenyl dioxygenase. J Bacteriol 183:3548–3555. doi:10.1128/JB.183.12.3548
Seeger M, González M, Cámara B, Muñoz L, Ponce E, Mejías L, Mascayano C, Vásquez Y, Sepúlveda-Boza S (2003) Biotransformation of natural and synthetic isoflavonoids by two recombinant microbial enzymes. Appl Environ Microbiol 69:5045–5050
Segura A, Molina L, Fillet S, Krell T, Bernal P, Muñoz-Rojas J, Ramos J-L (2012) Solvent tolerance in Gram-negative bacteria. Curr Opin Biotechnol 23:415–421. doi:10.1016/j.copbio.2011.11.015
Sei K, Sugimoto Y, Mori K, Maki H, Kohno T (2003) Monitoring of alkane-degrading bacteria in a sea-water microcosm during crude oil degradation by polymerase chain reaction based on alkane-catabolic genes. Environ Microbiol 5:517–522. doi:10.1046/j.1462-2920.2003.00447.x
Seo JS, Keum YS, Li QX (2012) Mycobacterium aromativorans JS19b1T degrades phenanthrene through C-1,2, C-3,4 and C-9,10 dioxygenation pathways. Int Biodeterior Biodegrad 70:96–103. doi:10.1016/j.ibiod.2012.02.005
Shinoda Y, Sakai Y, Uenishi H, Uchihashi Y, Hiraishi A, Yukawa H, Yurimoto H, Kato N (2004) Aerobic and anaerobic toluene degradation by a newly isolated denitrifying bacterium, Thauera sp. strain DNT-1. Appl Environ Microbiol 70:1385–1392. doi:10.1128/AEM.70.3.1385-1392.2004
Smalla K, Oros-Sichler M, Milling A, Heuer H, Baumgarte S, Becker R, Neuber G, Kropf S, Ulrich A, Tebbe C (2007) Bacterial diversity of soils assessed by DGGE, T-RFLP and SSCP fingerprints of PCR-amplified 16S rRNA gene fragments: do the different methods provide similar results? J Microbiol Methods 69:470–479. doi:10.1016/j.mimet.2007.02.014
So CM, Phelps CD, Young LY (2003) Anaerobic transformation of alkanes to fatty acids by a sulfate-reducing bacterium, strain Hxd3. Appl Environ Microbiol 69:3892–3900. doi:10.1128/AEM.69.7.3892
Speight JG (2001) Handbook of petroleum analysis. Wiley-Interscience, New York
Throne-Holst M, Wentzel A, Ellingsen TE, Kotlar H-K, Zotchev SB (2007) Identification of novel genes involved in long-chain n-alkane degradation by Acinetobacter sp. strain DSM 17874. Appl Environ Microbiol 73:3327–3332. doi:10.1128/AEM.00064-07
Uhlik O, Wald J, Strejcek M, Musilova L, Ridl J, Hroudova M, Vlcek C, Cardenas E, Mackova M, Macek T (2012) Identification of bacteria utilizing biphenyl, benzoate, and naphthalene in long-term contaminated soil. PLoS ONE 7:e40653. doi:10.1371/journal.pone.0040653
US Federal Remediation Technologies Roundtable (2014) http://www.frtr.gov/matrix2/top_page.html. Accessed 20 Jan 2014
van Beilen JB, Funhoff EG (2007) Alkane hydroxylases involved in microbial alkane degradation. Appl Microbiol Biotechnol 74:13–21. doi:10.1007/s00253-006-0748-0
van Beilen JB, Funhoff EG, van Loon A, Just A, Kaysser L, Bouza M, Holtackers R, Röthlisberger M, Li Z, Witholt B (2006) Cytochrome P450 alkane hydroxylases of the CYP153 family are common in alkane-degrading eubacteria lacking integral membrane alkane hydroxylases. Appl Environ Microbiol 72:59–65. doi:10.1128/AEM.72.1.59
Van Gestel K, Mergaert J, Swings J, Coosemans J, Ryckeboer J (2003) Bioremediation of diesel oil-contaminated soil by composting with biowaste. Environ Pollut 125:361–368. doi:10.1016/S0269-7491(03)00109-X
Wang W, Shao Z (2012) Genes involved in alkane degradation in the Alcanivorax hongdengensis strain A-11-3. Appl Microbiol Biotechnol 94:437–448. doi:10.1007/s00253-011-3818-x
Wang L, Wang W, Lai Q, Shao Z (2010) Gene diversity of CYP153A and AlkB alkane hydroxylases in oil-degrading bacteria isolated from the Atlantic Ocean. Environ Microbiol 12:1230–1242. doi:10.1111/j.1462-2920.2010.02165.x
Wentzel A, Ellingsen TE, Kotlar H-K, Zotchev SB, Throne-Holst M (2007) Bacterial metabolism of long-chain n-alkanes. Appl Microbiol Biotechnol 76:1209–1221. doi:10.1007/s00253-007-1119-1
Whyte LG, Schultz A, van Beilen JB, Luz AP, Pellizari V, Labbé D, Greer CW (2002) Prevalence of alkane monooxygenase genes in Arctic and Antarctic hydrocarbon-contaminated and pristine soils. FEMS Microbiol Ecol 41:141–150. doi:10.1111/j.1574-6941.2002.tb00975.x
Yakimov MM, Gentile G, Bruni V, Cappello S, D’Auria G, Golyshin PN, Giuliano L (2004) Crude oil-induced structural shift of coastal bacterial communities of rod bay (Terra Nova Bay, Ross Sea, Antarctica) and characterization of cultured cold-adapted hydrocarbonoclastic bacteria. FEMS Microbiol Ecol 49:419–432. doi:10.1016/j.femsec.2004.04.018
Yakimov MM, Timmis KN, Golyshin PN (2007) Obligate oil-degrading marine bacteria. Curr Opin Biotechnol 18:257–266. doi:10.1016/j.copbio.2007.04.006
Yergeau E, Arbour M, Brousseau R, Juck D, Lawrence JR, Masson L, Whyte LG, Greer CW (2009) Microarray and real-time PCR analyses of the responses of high-arctic soil bacteria to hydrocarbon pollution and bioremediation treatments. Appl Environ Microbiol 75:6258–6267. doi:10.1128/AEM.01029-09
Yergeau E, Sanschagrin S, Beaumier D, Greer CW (2012) Metagenomic analysis of the bioremediation of diesel-contaminated Canadian high arctic soils. PLoS ONE 7:e30058. doi:10.1371/journal.pone.0030058
Zielinski M, Kahl S, Standfuß-Gabisch C, Cámara B, Seeger M, Hofer B (2006) Generation of novel-substrate-accepting biphenyl dioxygenases through segmental random mutagenesis and identification of residues involved in enzyme specificity. Appl Environ Microbiol 72:2191–2199. doi:10.1128/AEM.72.3.2191-2199.2006
Acknowledgments
The authors gratefully acknowledge Conicyt PhD (SF, VM), Mecesup FMS0710 PhD (PA, SF), and Fulbright (SF) fellowships. MS acknowledges financial support of FONDECYT (1110992 and 1070507) (http://www.fondecyt.cl), Conicyt-BMBF, Center for Nanotechnology and Systems Biology (http://www.usm.cl), and USM (131342, 131109, 130948) (http://www.usm.cl) grants. The funders had no role in study design, data collection and analyses, decision to publish, or preparation of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Fuentes, S., Méndez, V., Aguila, P. et al. Bioremediation of petroleum hydrocarbons: catabolic genes, microbial communities, and applications. Appl Microbiol Biotechnol 98, 4781–4794 (2014). https://doi.org/10.1007/s00253-014-5684-9
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-014-5684-9