Abstract
Polycyclic aromatic hydrocarbon (PAH)-degrading bacteria capable of growing under electrokinetic conditions were isolated using an adjusted acclimation and enrichment procedure based on soil contaminated with heavy PAHs in the presence of an electric field. Their ability to degrade heavy PAHs under an electric field was individually investigated in artificially contaminated soils. The results showed that strains PB4 (Pseudomonas fluorescens) and FB6 (Kocuria sp.) were the most efficient heavy PAH degraders under electrokinetic conditions. They were re-inoculated into a polluted soil from an industrial site with a PAH concentration of 184.95 mg kg−1. Compared to the experiments without an electric field, the degradation capability of Pseudomonas fluorescens and Kocuria sp. was enhanced in the industrially polluted soil under electrokinetic conditions. The degradation extents of total PAHs were increased by 15.4 and 14.0 % in the electrokinetic PB4 and FB6 experiments (PB4 + EK and FB6 + EK) relative to the PB4 and FB6 experiments without electrokinetic conditions (PB4 and FB6), respectively. These results indicated that P. fluorescens and Kocuria sp. could efficiently degrade heavy PAHs under electrokinetic conditions and have the potential to be used for the electro-bioremediation of PAH-contaminated soil, especially if the soil is contaminated with heavy PAHs.
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References
Acar YB, Alshawabkeh AN (1993) Principles of electrokinetics remediation. Environ Sci Technol 27(13):2638–2647
Ahmed RZ, Ahmed N, Gadd GM (2010) Isolation of two Kocuria species capable of growing on various polycyclic aromatic hydrocarbons. Afr J Biotechnol 9:3611–3617
Al-Thani RF, Abd-Ei-Haleem DAM, Al-Shammri M (2009) Isolation and characterization of polyaromatic hydrocarbons-degrading bacteria from different Qatari soils. Afr J Microbiol Res 3(11):761–766
Andreoni V, Cavalca L, Rao MA, Nocerino G, Bernasconi S, Dell′Amico E, Colombo M, Gianfreda L (2004) Bacterial communities and enzyme activities of PAH polluted soils. Chemosphere 57:401–412
Banerjee DK, Fedorak PM, Hashimoto A, Masliyah JH, Pickard MA, Gray MR (1995) Monitoring the biological treatment of anthracene-contaminated soil in a rotating-drum bioreactor. Appl Microbiol Biotechnol 43:521–528
Bastiaens L, Springael D, Wattiau P, Harms H, deWachter R, Verachtert H, Diels L (2000) Isolation of adherent polycyclic aromatic hydrocarobon (PAH)-degrading bacteria using PAH-sorbing carriers. Appl Envrion Microbiol 66(5):1834–1843
Boonchan S, Britz ML, Stanley GA (2000) Degradation and mineralization of high-molecular-weight polycyclic aromatic hydrocarbons by defined fungal-bacterial cocultures. Appl Environ Microbiol 66:1007–1019
Bugg T, Foght JM, Pickard MA, Gray MR (2000) Uptake and active efflux of polycyclic aromatic hydrocarbons by Pseudomonas fluorescens LP6a. Appl Environ Microbiol 66(12):5387–5392
Caldini G, Cenci G, Manenti R, Morozzi G (1995) The ability of an environmental isolate of Pseudomonas fluorescens to utilize chrysene and other four-ring polynuclear aromatic hydrocarbons. Appl Microbiol Biotechnol 44:225–229
Carter DO, Yellowlees D, Tibbett M (2007) Autoclaving kills soil microbes yet soil enzymes remain active. Pedobiologia 51:295–299
Collins CH, Lyne PM (1984) Staining methods. Microbiological Methods, 5th edn. Butterworth, London
Covino S, Svobodová K, Čvančarová M, D’Annibale A, Petruccioli M, Federici F, Křesinová Z, Galli E, Cajthaml T (2010) Inoculum carrier and contaminant bioavailability affect fungal degradation performances of PAH-contaminated solid matrices from a wood preservation plant. Chemosphere 79:855–864
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 compounds. Appl Environ Micorbiol 61:711–723
Darmawan R, Nakata H, Ohta H, Niidome T, Takikawa K, Morimura S (2015) Isolation and evaluation of PAH degrading bacteria. Bioremed Biodegrad 6(3):1–7
Delgado-Balbuena L, Romero-Tepal EM, Luna-Guido ML, Marsh R, Dendooven L (2013) Removal of anthracene from recently contaminated and aged soils. Water Air Soil Pollut 224:1420–1427
El-Naas MH, Al-Muhtaseb SA, Makhlouf S (2009) Biodegradation of phenol by Pseudomonas putida immobilized in polyvinyl alcohol (PVA) gel. J Hazard Mater 164:720–725
Gallego RJS, Carcía-Martínez MJ, Llamas JF, Belloch C, Peláez AI, Sánchez J (2007) Biodegradation of oil tank bottom sludge using microbial consortia. Biodegradation 18:269–281
Gan S, Lau EV, Ng HK (2009) Remediation of soil contaminated with polycyclic aromatic hydrocarbons (PAHs). J Hazard Mater 172:532–549
González N, Simarro R, Molina MC, Bautista LF, Delgado L, Villa JA (2011) Effect of surfactants on PAH biodegradation by a bacterial consortium and on the dynamics of the bacterial community during the process. Bioresour Technol 102:9438–9446
Harbottle MJ, Lear G, Sills GC, Thompson IP (2009) Enhanced biodegradation of pentachlorophenol in unsaturated soil using reversed field electrokinecics. J Environ Manag 90:1893–1900
Haritash AK, Kaushik CP (2009) Biodegradation aspects of polycyclic aromatic hydrocarbons (PAH): a review. J Hazard Mater 169:1–15
Heitkamp MA, Cerniglia CE (1988) Mineralization of polycyclic aromatic hydrocarbons by a bacterium isolated from sediment below an oil field. Appl Environ Microbiol 54:1612–1614
Herbes SE, Schwall LR (1978) Microbial transformation of polycyclic aromatic hydrocarbons in pristine and petroleum-contaminatd sediments. Appl Envrion Microbiol 35:306–316
Hilyard EJ, Jones-Meehan JM, Spargo BJ, Hill RT (2008) Enrichment, isolation, and phylogenetic identification of polycyclic aromatic hydrocarbon-degrading bacteria from Elizabeth River sediments. Appl Environ Microbiol 74:1176–1182
Huang DN, Guo SH, Li TT, Wu B (2013) Coupling interactions between electrokinetics and bioremediation for Pyrene removal from soil under polarity reversal conditions. Clean-Soil, Air, Water 41(4):383–389
Huker GJ, Conn HJ (1923) Method of Gram staining. N Y State Agric Exp Stn Tech Bull 19:3–37
Ibekwe AM, Grieve CM (2004) Changes in developing plant microbial community structure as affected by contaminaged water. FEMS Microbiol Eol 2:239–248
International Agency for Research on Cancer (IARC) (1984). Monographs on the evaluation of the carcinogenic risk of chemicals to humans. Polycyclic aromatic hydrocarbons. Part 3. Industrial exposure in aluminum production, coal gasification, coke production, and iron and steel founding
John GH (1989) Bergey’s manual of systematic bacteriology. Williams & Wilkins, Baltimore
Juhasz AL, Naidu R (2000a) Bioremediation of high molecular weight polycyclic aromatic hydrocarbons: a review of the microbial degradation of benzo[a]pyrene. Int Biodeterior Biodegrad 45:57–88
Juhasz AL, Naidu R (2000b) Enrichment and isolation of non-specific aromatic degraders from unique uncontaminated (plant and faecal material) sources and contaminated soils. J Appl Microbiol 89:642–650
Kasai Y, Kishira H, Harayama S (2002) Bacteria belonging to the genus Cycloclasticus play a primary role in the degradation of aromatic hydrocarbons released in a marine environment. Appl Environ Microbiol 68:5625–5633
Kaushik CP, Haritash AK (2006) Polycyclic aromatic hydrocarbons (PAHs) and environmental health. Our earth 3: 1–7
Kelley I, Cerniglia CE (1995) Degradation of a mixture of high molecular-weight polycyclic aromatic hydrocarbons by a Mycobacterium strain PYR-1. J Soil Contam 4:77–91
Kim SH, Han HY, Lee YJ, Kim CW, Yang JW (2010) Effect of electrokinetic remediation on indigenous microbial activity and community within diesel contaminated soil. Sci Total Environ 408:3162–3168
Kiyohara H, Nagao K, Yana K (1982) Rapid screen for bacteria degrading water insoluble, solid hydrocarbons on agar plates. Appl Environ Microbiol 43:454–457
Lear G, Harbottle MJ, van der Gast CJ, Jack SA, Knowles CJ, Sills G, Thompson IP (2004) The effect of electrokinetics on soil microbial communities. Soil Biol Biochem 11:1751–1760
Li JL, Chen BH (2009) Effect of nonionic surfactants on biodegradation of phenanthrene by a marine bacteria of Neptunomonas naphthovorans. J Hazard Mater 162:66–73
Li FM, Guo SH, Wu B, Ye HF (2011) Concentrations and sources of polycyclic aromatic hydrocarbons in topsoil of Benxi city, Northeast China. Chinese Geogr Sci 21:185–194
Li FM, Guo SH, Hartog N (2012) Electrokinetics-enhanced biodegradation of heavy polycycylic aromatic hydrocarbons in soil around iron and steel industries. Electrochim Acta 85:228–234
Liu WK, Brown RW, Elliott TSJ (1997) Mechanisms of the bacteriacidal activity of low amperage current (DC). Antimicrob Chemother 39:687–695
Luo QS, Zhang XH, Wang H, Qian Y (2005) The use of non-uniform electrokinetics to enhance in-situ bioremediation of phenol-contaminated soil. J Hazard Mater 121:187–194
Macnab RM (1977) Bacterial flagella rotating in bundles: a study in helical geometry. Proc Natl Acad Sci USA 74:221–225
Miguel VS, Peinado C, Catalina F, Abrusci C (2009) Bioremediation of naphthalene in water by Sphingomonas paucimobilis using new biodegradable surfactants based on poly (ε-caprolactone). Int Biodeterior Biodegrad 63:217–223
Niqui-Arroyo JL, Ortega-Calvo JJ (2007) Integrating biodegradation and electroosmosis for the enhanced removal of polycyclic aromatic hydrocarbons from creosote-polluted soils. J Environ Qual 36:1444–1451
Ohtomo R, Satio M (2001) Increase in the culturable cell number of Escherchia coli during recovery from saline stress: possible implication for resuscitation from the VBNC state. Microb Ecol 2:208–214
Pagnout C, Frache G, Poupin P, Maunit B, Muller JF (2007) Isolation and characterization of a gene cluster involved in PAH degradation in Mycobacterium sp. Strain SNP11: expression in Mycobacterium smegmatis mc(2)155. Res Microbiol 158:175–186
Patel V, Cheturvedula S, Madamwar D (2012) Phenanthrene degradation by Pseudoxanthomonas sp. DMVP2 isolated from hydrocarbon contaminated sediment of Amlakhadi canal, Gujarat. India J Hazard Mater 201–202:43–51
Pinyakong O, Tiangda K, Iwata K, Omori T (2012) Isolation of novel phenanthrene-degrading bacteria from seawater and the influence of its physical factors on the degradation of phenanthrene. Sci Asia 38:36–43
Rahner D, Ludwig G, Röhrs J (2002) Electrochemically induced reactions in soils-a new approach to the in situ remeidation of contaminated soils? Part 1: the microconductor principle. Electrochim Acta 47:1395–1403
Reid BJ, Jones KC, Semple KT (2000) Bioavailability of persistent organic pollutants in soils and sediments-a perspective on mechanisms, consequences and assessment. Environ Pollut 108:103–112
Rentza JA, Alvrezb PJJ, Schnoor JL (2008) Benzo[a]pyrene degradation by Sphingomonas yanoikuyae JAR02. Environ Pollut 151:669–677
Röhrs J, Ludwig G, Rahner D (2002) Electrochemically induced reactions in soils-a new approach to the in situ remeidation of contaminated soils? Part 2: remediation experiments with a natural soil containing highly chlorinated hydrocabons. Electrochim Acta 47:1405–1414
Saichek R, Reddy K (2003) Effect of pH control at the anode for the electrokinetic removal of phenanthrene from kaolin soil. Chemosphere 51:273–287
Samanta SK, Singh OV, Jain RK (2002) Polycyclic aromatic hydrocarbons: environmental pollution and bioremediation. Trends Biotechnol 20:243–248
Sanromán MA, Pazos M, Ricart MT, Cameselle C (2005) Decolourisation of textile indigo dye by DC electric current. Eng Geol 77:253–261
She P, Bo S, Xing XH, van Loosdrecht M, Liu Z (2006) Electrolytic stimulation of bacteria Enterobacter dissolvens by a direct current. Biochem Eng J 1:23–29
Shi L, Müller S, Loffhagen N, Harms H, Wick LY (2008) Activity and viability of polycyclic aromatic hydrocarbon-degrading Sphingomonas sp. LB126 in a DC-electrical field typical for electrobioremediation measures. Microb Biotechnol 1:53–61
Song X, Xu Y, Li G, Zhang Y, Huang T, Hu Z (2011) Isolation, characterization of Rhodococcus sp. P14 capable of degrading high-molecular-weight polycyclic aromatic hydrocarbons and aliphatic hydrocarbons. Mar Pollut Bull 62:2122–2128
Straube WL, Nestler CC, Harsen LD, Ringleberg D, Pritchard PH, Jones-Meehan J (2003) Remediation of polyaromatic hydrocarbons (PAHs) through landfarming with biostimulation and bioaugmentation. Acta Biotechnol 23(2–3):179–196
Suni S, Romantschuk M (2004) Mobilisation of bacteria in soils by electro-osmosis. FEMS Microbiol Ecol 49:51–57
Thrash JC, Coates JD (2008) Review: direct and indirect electrical stimulation of microbial metabolism. Environ Sci Technol 11:3921–3931
Tian Y, Liu HJ, Zheng TL, Kwon KK, Kim SJ, Yan CL (2008) PAHs contamination and bacterial communities in mangrove surface sediments of the Jiulong River Estuary, China. Mar Pollut Bull 57:707–715
Tiehm A, Lohner ST, Augenstein T (2009) Effects of direct electric current and electrode reactions on vinyl chloride degrading microorganisms. Electrochim Acta 54:3453–3459
Trzesicka-Mlynarz D, Ward OP (1995) Degradation of polycyclic aromatic hydrocarbons (PAHs) by a mixed culture and its components pure cultures, obtained from PAH-contaminated soil. Can J Microbiol 41:470–476
USEPA Method 3550C (1996) Ultrasonic extraction. United State Environmental Protection Agency, Washington, DC
Virkutyte J, Sillanpää M, Latostenmaa P (2002) Electrokinetic soil remediation-critical overview. Sci Total Environ 189:97–121
Wick LY, Buchholz F, Fetzer I, Kleinsteuber S, Härtig C, Shi L, Miltner A, Harms H, Pucci GN (2010) Responses of soil microbial communities to weak electric fields. Sci Total Environ 408:4886–4893
Wick LY, Shi L, Harms H (2007). Electro-bioremediation of hydrophobic organic soil contaminants: A review of fundamental interactions. Electrochim Acta 52: 3441-3448
Willison JC (2004) Isolation and characterization of a novel sphingomonad capable of growth with chrysene as sole carbon and energy source. FEMS Microbial Lett 241:143–150
Wolf DC, Dao TH, Scott HD, Lavy TL (1989) Influence of sterilization methods on selected soil microbiological, physical and chemical properties. J Environ Qual 18:39–44
Yu JW, Neretnieks I (1997) Theoretical evaluation of a technique for electrokinetic decontamination of soils. J Contam Hydrol 26:291–299
Yuan SY, Su LM, Chang BV (2009) Biodegradation of phenanthrene and pyrene in compost-amended soil. J Environ Sci Health, Part A 44:648–653
Zhang GY, Ling JY, Sun HB, Luo J, Fan YY, Cui ZJ (2009) Isolation and characterization of a newly isolated polycyclic aromatic hydrocarbons-degrading Janibacter anopheles strain JY11. J Hazard Mater 172:580–586
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
Acknowledgments
This research was supported by the National Natural Science Foundation of China (21047006), Major Science and Technology Program for Water Pollution Control and Treatment (No. 2013ZX07202-007) and the National High Technology Research and Development Program of China (No. 2013AA06A210). We thank Kerusha Lutchmiah of KWR Watercycle Research Institute for proof reading the final manuscript. We thank two anonymous reviewers for their constructive comments that helped improve this manuscript.
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Li, F., Guo, S., Hartog, N. et al. Isolation and characterization of heavy polycyclic aromatic hydrocarbon-degrading bacteria adapted to electrokinetic conditions. Biodegradation 27, 1–13 (2016). https://doi.org/10.1007/s10532-015-9750-5
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DOI: https://doi.org/10.1007/s10532-015-9750-5