Abstract
A 70 day pot experiment was conducted for the cleaning-up of a PCBs-contaminated soil (104 mg kg−1 soil DW) using bioaugmentation with Burkholderia xenovorans LB400 (LB400) assisted or not by the use of tall fescue (Festuca arundinacea). The total cultivable bacteria of the soil were higher with the presence of plants. Real-time PCR showed that LB400 (targeting 16S–23S rRNA ITS) survived with abundance related to total bacteria (targeting 16S rRNA) being higher with fescue (up to a factor of three). Bioaugmentation had a positive effect on fescue biomass and more specifically on roots (by a factor of three). PCB dissipation (sum of congeners 28, 52, 101, 118, 153, 180) averaged 13 % (bioaugmented-planted) up to 32 % (non bioaugmented-planted), without any significant difference between treatments. Basically our results demonstrated that indigenous bacteria were able to dissipate PCBs (26.2 % dissipation). PCB dissipation was not related to the abundance of LB400 or to the total bacterial counts. Bioaugmentation or fescue altered the structure of the bacterial community of the soil, not the combination of both. Principal component analysis showed that bioaugmentation tended to improve the control of the process (lower variability in PCB dissipation). Opposite to that bioaugmentation increased the variability of the structure of the bacterial community.
Similar content being viewed by others
References
AFNOR (2005) Qualité du sol: détermination du pH. Norme 10390
Baudoin E, Benizri E, Gucker A (2002) Impact of growth stage on the bacterial community structure along maize roots, as determined by metabolic and genetic fingerprinting. Appl Soil Ecol 2:135–145
Bedard DL, Quensen JF III (1995) Microbial reductive dechlorination of polychlorinated biphenyls. In: Young LY, Cerniglia CE, Cerniglia CE (eds) Microbial transformation and degradation of toxic organic chemicals. Wiley-Liss Division, New York, pp 127–216
Bedard DL, Van Dort HM, May RJ, Smullen LA (1997) Enrichment of microorganisms that sequentially meta, para-dechlorinate the residue of Aroclor 1260 in Housatonic River sediment. Environ Sci Technol 11:3308–3313
Bois P, Huguenot D, Jézéquel K, Lollier M, Cornu JY, Lebeau T (2012) Herbicide mitigation in microcosms simulating stormwater basins subject to polluted water inputs. Wat Res (in press)
Borja J, Taleon DM, Auresenia J, Gallardo S (2005) Polychlorinated biphenyls and their biodegradation. Process Biochem 40:1999–2013
Briones AM Jr, Reichardt W (1999) Estimating microbial population counts by ‘most probable number’ using Microsoft Excel®. J Microbiol Methods 2:157–161
Brüggemann N, Gessler A, Kayler Z, Keel SG, Badeck F, Barthel M, Boeckx P, Buchmann N, Brugnoli E, Esperschütz J, Gavrichkova O, Ghashghaie J, Gomez-Casanovas N, Keitel C, Knohl A, Kuptz D, Palacio S, Salmon Y, Uchida Y, Bahn M (2011) Carbon allocation and carbon isotope fluxes in the plant-soil-atmosphere continuum: a review. Biogeosciences 8:3457–3489
Caballero-Mellado J, Onofre-Lemus J, Estrada-de los Santos P, Martínez-Aguilar L (2007) The tomato rhizosphere, an environment rich in nitrogen-fixing Burkholderia species with capabilities of interest for agriculture and bioremediation. Appl Environ Microbiol 73(16):5308–5319
Campanella BF, Bock C, Schröder P (2002) Phytoremediation to increase the degradation of PCBs and PCDD/Fs, potential and limitations. Environ Sci pollut Res 1:73–85
Cébron A, Norini MP, Beguiristain T, Leyval C (2008) Real-time PCR quantification of PAH-ring hydroxylating dioxygenase (PAH-RHDα) genes from Gram positive and Gram negative bacteria in soil and sediment samples. J Microbiol Methods 73:148–159
Chekol T, Vough LR (2002) Assessing the phytoremediation potential of tall fescue and Sericea Lespedeza for organic contaminants in soil. Remed J 3:117–128
Chekol T, Vough LR, Chaney RL (2004) Phytoremediation of polychlorinated biphenyl–contaminated soils: the rhizosphere effect. Environ Int 6:799–804
Cook KL, Garland JL, Layton AC, Dionisi HM, Levine LH, Sayler GS (2006) Effect of microbial species richness on community stability and community function in a model plant-based wastewater processing system. Microb Ecol 52:725–737
Cravo-Laureau C, Hernandez-Raquet G, Vitte I, Jézéquel R, Bellet V, Godon JJ, Caumette P, Balaguer P, Duran R (2011) Role of environmental fluctuations and microbial diversity in degradation of hydrocarbons in contaminated sludge. Res Microb 162:888–895
Dejonghe W, Boon N, Seghers D, Top EM, Verstraete W (2001) Bioaugmentation of soils by increasing microbial richness: missing links. Environ Microbiol 3:649–657
Dercová K, Čičmanová J, Lovecká P, Demnerová K, Macková M, Hucko P, Kušnír P (2008) Isolation and identification of PCB-degrading microorganisms from contaminated sediments. Int Biodeter Biodegr 3:219–225
Duchaufour P (2001) Introduction à la science du sol: sol, végétation, environnement, 6th edn. Dunot, Paris, p 331
Fagervold SK, May HD, Sowers KR (2007) Microbial reductive dechlorination of Aroclor 1260 in Baltimore harbor sediment microcosms is catalyzed by three phylotypes within the phylum Chloroflexi. Appl Environ Microbiol 9:3009–3018
Furukawa K, Fujihara H (2008) Microbial degradation of polychlorinated biphenyls: biochemical and molecular features. J Biosci Bioeng 5:433–449
Habe H, Omori T (2003) Genetics of polycyclic aromatic hydrocarbon metabolism in diverse aerobic bacteria. Biosci Biotechnol Biochem 2:225–243
He Y, Zhao Y, Zhou G, Huang M (2009) Evaluation of extraction and purification 282 methods for obtaining PCR-amplifiable DNA from aged refuse for microbial community 283 analysis. World J Microbiol Biot 25:2043–2051
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 1:251–259
INERIS (2005) Fiche de données toxicologiques et environnementales des substances chimiques, Polychlorobiphényles
Juhanson J, Truu J, Heinaru E, Heinaru A (2009) Survival and catabolic performance of introduced Pseudomonas strains during phytoremediation and bioaugmentation field experiment. FEMS Microbiol Ecol 3:446–455
Khan FI, Husain T, Hejazi R (2004) An overview and analysis of site remediation technologies. J Environ Manage 71:95–122
Kirk JL, Beaudette LA, Hart M, Moutoglis P, Klironomos JN, Lee H, Trevors JT (2004) Methods of studying soil microbial diversity. J Microbiol Methods 58:169–188
Kuiper I, Bloemberg GV, Lugtenberg BJJ (2001) Selection of a plant-bacterium pair as a novel tool for rhizostimulation of polycyclic aromatic hydrocarbon-degrading bacteria. Mol Plant Microbe Interact 14:1197–1205
Kuiper I, Lagnedijk EL, Bloemberg GV, Lugtenberg BJJ (2004) Rhizoremediation: a beneficial plant-microbe interaction. Mol Plant Microbe Interact 17:6–15
Lebeau T (2011) Bioaugmentation, biostimulation and biocontrol, chapter 7. In: Singh A, Parmar N, Kuhad RC (eds) Soil Biology, 28th edn., Bioaugmentation for in situ soil remediation: how to ensure the success of such a processSpringer, Berlin, pp 129–186
Li Z, Kong S, Chen L, Bai Z, Ji Y, Liu J, Lu B, Han B, Wang Q (2011) Concentrations, spatial distributions and congener profiles of polychlorinated biphenyls in soils from a coastal city—Tianjin, China. Chemosphere 85:494–501
Lima D, Viana P, André S, Chelinho S, Costa C, Ribeiro R, Sousa JP, Fialho AM, Viegas CA (2009) Evaluating a bioremediation tool for atrazine contaminated soils in open soil microcosms: the effectiveness of bioaugmentation and biostimulation approaches. Chemosphere 74:187–192
Mehmannavaz R, Prasher SO, Ahmad D (2002) Rhizospheric effects of alfalfa on biotransformation of polychlorinated biphenyls in a contaminated soil augmented with Sinorhizobium meliloti. Process Biochem 9:955–963
Mulligan CN, Yong RN, Gibbs BF (2001) Heavy metal removal from sediments by biosurfactants. J Hazard Mater 1–2:111–125
Narasimhan K, Basheer C, Bajic VB, Swarup S (2003) Enhancement of plant–microbe interactions using a rhizosphere metabolomics-driven approach and its application in the removal of polychlorinated biphenyls. Plant Physiol 132:146–153
Newcombe DA, Crowley DE (1999) Bioremediation of atrazine-contaminated soil by repeated applications of atrazine-degrading bacteria. Appl Microbiol Biotechnol 51:877–882
Norini MP, Secher C, Lollier M, Jézéquel K, Cornu JY, Lebeau T Quantification of the 16S-23S rRNA internal transcribed spacers of Burkholderia xenovorans strain LB400 using real-time PCR in soil samples. Lett Appl Microbiol (in press)
Nübel U, Engelen B, Felske A, Snaidr J, Wieshuber A, Amann RI, Ludwig W, Backhaus H (1996) Sequence heterogeneities of genes encoding 16S rRNAs in Paenibacillus polymyxa detected by temperature gradient gel electrophoresis. J Bacteriol 178:5636–5643
Parnell JJ, Denef VJ, Park J, Tsoi T, Tiedje JM (2010) Environmentally relevant parameters affecting PCB degradation: carbon source- and growth phase-mitigated effects of the expression of the biphenyl pathway and associated genes in Burkholderia xenovorans LB400. Biodegradation 1:47–156
Petrić I, Bru D, Udiković-Kolić N, Hršak D, Philippot L, Martin-Laurent F (2011a) Evidence for shifts in the structure and abundance of the microbial community in a long-term PCB-contaminated soil under bioremediation. J Hazard Mater 195:254–260
Petrić I, Hršak D, Fingler S, Udiković-Kolić N, Bru D, Martin-Laurent F (2011b) Insight in the PCB-degrading functional community in long-term contaminated soil under bioremediation. J Soils Sed 11:290–300
Ponce BL, Latorre VK, Gonzalez M, Seeger M (2011) Antioxidant compounds improved PCB-degradation by Burkholderia xenovorans strain LB400. Enzyme Microbial Technol 49:509–516
Rasse DP, Rumpel C, Dignac MF (2005) Is soil carbon mostly root carbon? Mechanisms for a specific stabilization. Plant Soil 269:341–356
R Development Core Team (2011). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, http://www.R-project.org/. Accessed 25 Jun 2012
Romantschuk M, Sarand I, Petanen T, Peltola R, Jonsson-Vihanne M, Koivula T, Yrjala K, Haahtela K (2000) Means to improve the effect of in situ bioremediation of contaminated soil: an overview of novel approaches. Environ Pollut 107:179–185
Ross G (2004) The public health implications of polychlorinated biphenyls (PCBs) in the environment. Rev Ecotox Environ Safety 59:275–291
Rovira AD (1969) Plant root exudates. Bot Rev 1:35–57
Schiefelbein JW (2000) Constructing a plant cell. The genetic control of root hair development. Plant Physiol 4:1525–1531
Seo JS, Keum YS, Li QX (2009) Bacterial degradation of aromatic compounds. Int J Environ Res Public Health 1:278–309
Shukla KP, Sharma S, Singh NK, Singh V, Tiwari K, Singh S (2011) Nature and role of root exudates: efficacy in bioremediation. Afr J Biotechnol 10:9717–9724
Singer AC, Gilbert ES, Luepromchai E, Crowley DE (2000) Bioremediation of polychlorinated biphenyl-contaminated soil using carvone and surfactant-grown bacteria. Appl Microbiol Biotechnol 6:838–843
Singer AC, Smith D, Jury WA, Hathuc K, Crowley DE (2003) Impact of the plant rhizosphere and augmentation on remediation of polychlorinated biphenyl contaminated soil. Environ Toxicol Chem 9:1998–2004
Smith KE, Schwab AP, Banks MK (2007) Phytoremediation of polychlorinated biphenyl (PCB)-contaminated sediment: a greenhouse feasibility study. J Environ Qual 36:239–244
Suárez-Moreno ZR, Caballero-Mellado J, Coutinho BG, Mendonça-Previato L, James EK, Venturi V (2012) Common features of environmental and potentially beneficial plant-associated Burkholderia. Microbial Ecol 2:249–266
Sudjarid W, Chen IM, Monkong W, Anotai J (2012) Reductive Dechlorination of 2,3,4-Chlorobiphenyl by Biostimulation and Bioaugmentation. Environment Eng Sci 29:255–261
Tam NFY, Wong YS (2008) Effectiveness of bacterial inoculum and mangrove plants on remediation of sediment contaminated with polycyclic aromatic hydrocarbons. Mar Pollut Bull 6–12:716–726
Thompson IP, van der Gast CJ, Ciric L, Singer AC (2005) Bioaugmentation for bioremediation: the challenge of strain selection. Environ Microbiol 7:909–915
Tiedje JM, Quensen JF, Chee-Sanford J, Schimel JP, Boyd SA (1993) Microbial reductive dechlorination of PCBs. Biodegradation 4:231–240
Tremaroli V, Vacchi Suzzi C, Fedi S, Ceri H, Zannoni D, Turner RJ (2010) Tolerance of Pseudomonas pseudoalcaligenes KF707 to metals, polychlorobiphenyls and chlorobenzoates: effects on chemotaxis-, biofilm-and planktonic-grown cells. FEMS Microbiol Ecol 2:291–301
Tu C, Teng Y, Luo Y, Li X, Sun X, Li Z, Liu W, Christie P (2011) Potential for biodegradation of polychlorinated biphenyls (PCBs) by Sinorhizobium meliloti. J Hazard Mater 186:1438–1444
Vogel TM, Walter MV (2001) Bioaugmentation. In: Hurst CJ, Crawford RL, Knudsen GR, McInerney MJ, Stetzenbach LD (eds) Manual of environmental microbiology. Amer Soc Microbiol, Washington, pp 952–959
Weber JB, Mrozek E Jr (1979) Polychlorinated biphenyls: phytotoxicity, absorption and translocation by plants, and inactivation by activated carbon. Bull Environ Contam Toxicol 23:412–417
Wu Q, Bedard DL, Wiegel J (1997) Effect of incubation temperature on the route of microbial reductive dechlorination of 2,3,4,6-tetrachlorobiphenyl in polychlorinated biphenyl (PCB)-contaminated and PCB-free freshwater sediments. Appl Environ Microbiol 7:2836–2843
Wu JP, Luo HJ, Zhang Y, Yu M, Chen SJ, Mai BX, Yang ZY (2009) Biomagnification of polybrominated diphenyl ethers (PBDEs) and polychlorinated biphenyls in a highly contaminated freshwater food web from south China. Environ Pollut 3:904–909
Yadav JS, Quensen JF III, Tiedje JM, Reddy CA (1995) Degradation of polychlorinated biphenyl mixtures (Aroclors 1242, 1254, and 1260) by the white rot fungus Phanerochaete chrysosporium as evidenced by congener-specific analysis. Appl Environ Microbiol 7:2560–2565
Acknowledgments
This work was supported by the Pôle de compétitivité AXELERA (Lyon, France) and the Alsace region (Strasbourg, France) for the doctoral fellowship of Camille Secher. The authors wish to thank SITA FD for providing soil used in this study.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Secher, C., Lollier, M., Jézéquel, K. et al. Decontamination of a polychlorinated biphenyls-contaminated soil by phytoremediation-assisted bioaugmentation. Biodegradation 24, 549–562 (2013). https://doi.org/10.1007/s10532-013-9625-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10532-013-9625-6