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Bioremediation trial on aged PCB-polluted soils—a bench study in Iceland

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Abstract

Polychlorinated biphenyls (PCBs) pose a threat to the environment due to their high adsorption capacity to soil organic matter, stability and low reactivity, low water solubility, toxicity and ability to bioaccumulate. With Icelandic soils, research on contamination issues has been very limited and no data has been reported either on PCB degradation potential or rate. The goals of this research were to assess the bioavailability of aged PCBs in the soils of the old North Atlantic Treaty Organization facility in Keflavík, Iceland and to find the best biostimulation method to decrease the pollution. The effectiveness of different biostimulation additives (N fertiliser, white clover and pine needles) at different temperatures (10 and 30 °C) and oxygen levels (aerobic and anaerobic) were tested. PCB bioavailability to soil fauna was assessed with earthworms (Eisenia foetida). PCBs were bioavailable to earthworms (bioaccumulation factor 0.89 and 0.82 for earthworms in 12.5 ppm PCB soil and in 25 ppm PCB soil, respectively), with less chlorinated congeners showing higher bioaccumulation factors than highly chlorinated congeners. Biostimulation with pine needles at 10 °C under aerobic conditions resulted in nearly 38 % degradation of total PCBs after 2 months of incubation. Detection of the aerobic PCB degrading bphA gene supports the indigenous capability of the soils to aerobically degrade PCBs. Further research on field scale biostimulation trials with pine needles in cold environments is recommended in order to optimise the method for onsite remediation.

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References

  • Abraham W-R, Nogales B, Golyshin PN, Pieper DH, Timmis KN (2002) Polychlorinated biphenyls-degrading microbial communities in soils and sediments. Curr Opin Microbiol 5:246–253

    Article  CAS  Google Scholar 

  • Aislabie J, Saul DJ, Foght JM (2006) Bioremediation of hydrocarbon-contaminated polar soils. Extremophiles 10:171–179

    Article  CAS  Google Scholar 

  • Alexander M (1999) Biodegradation and bioremediation, 2nd edn. Academic, California, USA

    Google Scholar 

  • Anderson MJ, Robinson J (2003) Generalized discriminant analysis based on distances. Aust New Z J Stat 45:301–318

    Article  Google Scholar 

  • Arnalds O (2004) Volcanic soils of Iceland. Catena 56:3–20

    Article  CAS  Google Scholar 

  • Arnalds O, Óskarsson H, Gísladóttir FO, Grétarsson E (2009) Soil map of Iceland. The Agricultural University of Iceland, Reykajvik, Iceland

    Google Scholar 

  • BEST (2001) A risk management strategy for PCB-contaminated sediments. Washington D. C., USA: Committee on Remediation of PCB-Contaminated Sediments, Board on Environmental Studies and Toxicology, National Research Council

  • Björnsson H, Sveinbjörnsdóttir AE, Danielsdóttir AK, Snorrason Á, Viggósson G, Sigurjónsson J, Baldursson S, Þorvaldsdóttir S, Jónsson T (2008) Hnattrænar loftlagsbreytingar og áhrif þeirra á Íslandi (Global climate change and its influence in Iceland). Icelandic Ministry for the Environment. 118 p. [In Icelandic]

  • Blakemore LC, Searle PL, Daly BK (1987) Methods for chemical analysis of soils: New Zealand Soil Bureau Science Report 80. New Zealand Soil Bureau, New Zealand

    Google Scholar 

  • Borja J, Taleon DM, Auresenia J, Gallardo S (2005) Polychlorinated biphenyls and their biodegradation. Process Biochem 40:1999–2013

    Article  CAS  Google Scholar 

  • Crawford RL, Crawford DL (eds) (2005) Bioremediation: Principles and Applications. Cambridge University Press, New York, USA

    Google Scholar 

  • Donnelly PK, Hedge RS, Fletcher JS (1994) Growth of PCB-degrading bacteria on compounds from photosynthetic plants. Chemosphere 28(5):981–988

    Article  Google Scholar 

  • Erickson MD (1997) Analytical chemistry of PCBs, 2nd edn. CRC Press LLC, Florida, USA

    Google Scholar 

  • 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 73(9):3009–3018

    Article  CAS  Google Scholar 

  • Fava F, Bertin L, Fedi S, Zannoni D (2003) Methyl-beta-cyclodextrin-enhanced solubilization and aerobic biodegradation of polychlorinated biphenyls in two aged-contaminated soils. Biotech Bioeng 81:381–390

    Google Scholar 

  • Gomes HI, Dias-Ferreira C, Ribeiro AB (2013) Overview of in situ and ex situ remediation technologies for PCB-contaminated soils and sediments and obstacles for full-scale application. Sci Total Environ 445–446:237–260

    Article  Google Scholar 

  • Guicharnaud R, Paton GI (2006) An evaluation of acid deposition on cation leaching weathering rates of an Andosol and Cambisol. J Geochem Explor 88:279–283

    Article  CAS  Google Scholar 

  • Guicharnaud R, Arnalds O, Paton GI (2010) Short term changes of microbial processes of Icelandic soils to increasing temperatures. Biogeosciences 7:671–682

    Article  CAS  Google Scholar 

  • Hallgren P, Westbom R, Nilsson T, Sporring S, Björklund E (2006) Measuring bioavailability of polychlorinated biphenyls in soil to earthworms using selective supercritical fluid extraction. Chemosphere 63:1532–1538

    Article  CAS  Google Scholar 

  • Hernandez BS, Koh S-C, Chial M, Focht DD (1997) Terpene-utilizing isolates and their relevance to enhanced biotransformation of polychlorinated biphenyls in soil. Biodegradation 8:153–158

    Article  CAS  Google Scholar 

  • ÍSOR – Iceland Geosurvey (2008) Sýnataka og efnagreiningar á grunnvatni úr fjórum holum á Keflavíkurflugvelli (sampling and analyses of groundwater from four holes at the Kaflavik airport). ÍSOR [In Icelandic], Reykjavík

    Google Scholar 

  • Jensen S, Reutergårdh L, Janson B (1983) Analytical methods for measuring organochlorines and methyl mercury by gas-chromatography. FAO/SIDA Manual of methods in aquatic environment research. Part 9. Analysis of metals and organochlorines in fish. FAO Fish Tech Paper 212:21–33

    Google Scholar 

  • Jensen S, Häggberg L, Jörundsdóttir H, Odham G (2003) A quantitative lipid extraction method for residue analysis of fish involving nonhalogenated solvents. J Agric Food Chem 51:5607–5611

    Article  CAS  Google Scholar 

  • Jones A, Stolbovoy V, Tarnocai C, Broll G, Spaargaren O, Montanarella L (eds) (2010) Soil Atlas of the Northern Circumpolar Region. European Commission, Publications Office of the European Union, Luxemburg. 144 pp

  • Jörundsdóttir H (2009) Temporal and spatial trends of organohalogens in guillemot (Uria aalge) from North Western Europe. Dissertation, Stockholm University, Sweden

  • Jota MA, Hassett JP (1991) Effects of environmental variables on binding of a PCB congener by dissolved humic substances. Environ Toxicol Chem 10:483–491

    Article  CAS  Google Scholar 

  • Kalinovich IK, Rutter A, Rowe RK, Poland JS (2012) Design and application of surface PRBs for PCB remediation in the Canadian Arctic. J Environ Manag 101:124–133

    Article  CAS  Google Scholar 

  • Karstensen KH, Ringstad O, Rustad I, Kalevi K, Jörgensen K, Nylund K, Alsberg T, Ólafsdóttir K, Heidenstam O, Solberg H (1997) Nordic Guidelines for Chemical Analysis of Contaminated Soil Samples. NORDTEST Technical Report 329. Oslo, Norway: SINTEF Applied Chemistry

  • Karstensen KH, Ringstad O, Rustad I, Kalevi K, Jörgensen K, Nylund K, Alsberg T, Ólafsdóttir K, Heidenstam O, Solberg H (1998) Methods for chemical analysis of contaminated soil samples - tests of their reproducibility between Nordic laboratories. Talanta 46:423–437

    Article  CAS  Google Scholar 

  • Kuipers B, Cullen WR, Mohn WW (2003) Reductive dechlorination of weathered Aroclor 1260 during anaerobic biotreatment of Arctic soils. Can J Microbiol 49:9–14

    Article  CAS  Google Scholar 

  • Lambo AJ, Patel TR (2007) Biodegradation of polychlorinated biphenyls in Aroclor 1232 and production of metabolites from 2,4,4′-trichlorobiphenyl at low temperature by psychrotolerant Hydrogenophaga sp strain IA3-A. J Appl Microbiol 102:1318–1329

    Article  CAS  Google Scholar 

  • Margesin R (2007) Alpine microorganisms: useful tools for low-temperature bioremediation. J Microbiol 4:281–285

    Google Scholar 

  • Master ER, Mohn WW (1998) Psychrotolerant bacteria isolated from Arctic soil that degrade polychlorinated biphenyls at low temperatures. Appl Environ Microbiol 64:4823–4829

    CAS  Google Scholar 

  • Meyles CA, Schmidt B (2005) Report on Soil Protection and Remediation of Contaminated Sites in Iceland: A preliminary study. Environment and Food Agency of Iceland (UST), Reykjavik, Iceland

    Google Scholar 

  • Michel Jr FC, Quensen J, Reddy CA (2001) Bioremediation of a PCB-contaminated soil via composting. Compost Science & Utilization 9:274–284

  • Mohn WW, Westerberg K, Cullen WR, Reimer KJ (1997) Aerobic biodegradation of biphenyl and polychlorinated biphenyls by Arctic soil microorganisms. Appl Environ Microbiol 63:3378–3384

    CAS  Google Scholar 

  • Ohtsubo Y, Kudo T, Tsuda M, Nagata Y (2004) Strategies for bioremediation of polychlorinated biphenyls. Appl Microbiol Biotechnol 65:250–258

    CAS  Google Scholar 

  • Ólafsdóttir K, Petersen A, Thórdadóttir S, Jóhannesson T (1995) Organochlorine residues in Gyrfalcons (Falco rusticolus) in Iceland. Bull Environ Contam Toxicol 55:382–389

    Article  Google Scholar 

  • Ólafsdóttir K, Petersen A, Magnusdóttir EV, Björnsson T, Jóhannesson T (2005) Temporal trends of organochlorine contamination in Black Guillemots in Iceland from 1976 to 1996. Environ Pollut 133:509–515

    Article  Google Scholar 

  • Parfitt RL, (1990) Allophane in New Zealand – A review. Aust J Soil Res 28:343–360

    Google Scholar 

  • Parfitt RL, Childs CW, (1988) Estimation of forms of Fe and Al: A review, and analysis of contrasting soils by dissolution and moessbauer methods. Aust J Soil Res 26:121–144

    Google Scholar 

  • Park Y-I, So J-S, Koh S-C (1999) Induction by carvone of the polychlorinated biphenyl (PCB)-degradative pathway in Alcaligenes eutrophus H850 and its molecular monitoring. J Microbiol Biotechnol 9(6):804–810

    CAS  Google Scholar 

  • Pieper DH (2005) Aerobic degradation of polychlorinated biphenyls. Appl Microbiol Biotechnol 67:170–191

    Article  CAS  Google Scholar 

  • Rodriques JLM, Maltseva OV, Tsoi TV, Helton RR, Quensen JF III, Fukuda M, Tiedje JM (2001) Development of a Rhodococcus recombinant strain for degradation of products from anaerobic dechlorination of PCBs. Environ Sci Technol 35:663–668

    Article  Google Scholar 

  • Rodriques JLM, Kachel CA, Aiello MR, Quensen JF, Maltseva OV, Tsoi TV, Tiedje JM (2006) Degradation of Aroclor 1242 dechlorination products in sediments by Burkholderia xenovarans LB400(ohc) and Rhococcus sp. Strain RHA1(fcb). Appl Environ Microbiol 4:2476–2482

    Article  Google Scholar 

  • Ross G (2004) The public health implications of polychlorinated biphenyls (PCBs) in the environment. Ecotoxicol Environ Saf 59:275–291

    Article  CAS  Google Scholar 

  • Safe SH (1994) Polychlorinated biphenyls (PCBs): environmental impact, biochemicals and toxic responses, and implications for risk assessment. Crit Rev Toxicol 24:87–149

    Article  CAS  Google Scholar 

  • Shoji S, Nanzyo M, Dahlgren R (1993) Volcanic ash soils: Genesis, Properties, and Utilization. Developments in Soil Science: 21. Elsevier, The Netherlands

    Google Scholar 

  • Sigurgeirsson MA, Arnalds O, Palsson SE, Howard BJ, Gudnason K (2005) Radioceasium fallout behaviour in volcanic soils in Iceland. J Environ Radioact 79(1):39–53

    Article  CAS  Google Scholar 

  • Smith KA, Mullins CE (eds) (2001) Soil and Environmental Analysis: Physical methods, 2nd edn. Marcel Dekker, New York

  • Tharakan J, Tomlinson D, Addagada A, Shafagati A (2006) Biotransformation of PCBs in contaminated sludge: potential for novel biological technologies. Eng Life Sci 6:43–50

    Article  CAS  Google Scholar 

  • Tiedje JM, Quensen JF III, Chee-Sanford J, Schimel JP, Cole JA, Boyd SA (1993) Microbial reductive dechlorination of PCBs. Biodegradation 4:231–240

    Article  CAS  Google Scholar 

  • Trevors JT (1984) Dehydrogenase activity in soil: a comparison between the INT and TTC assay. Soil Biol Biochem 16:673–674

    Article  CAS  Google Scholar 

  • Ulbrich B, Stahlmann R (2004) Developmental toxicity of polychlorinated biphenyls (PCBs): a systematic review of experimental data. Arch Toxicol 78:252–268

    CAS  Google Scholar 

  • UNEP/AMAP (2011) Climate Change and POPS : Predicting the Impacts. Report of the UNEP/AMAP Expert Group. Secreteriat of the Stockholm Convention, Geneva, p 62

    Google Scholar 

  • Vasilyeva GK, Strijakova ER (2007) Bioremediation of soils and sediments contaminated by polychlorinated biphenyls. Microbiology 76:639–653

    Article  CAS  Google Scholar 

  • Ville P, Roch P, Cooper EL, Masson P, Narbonne J-F (1995) PCBs increase molecular-related activities (Lysozyme, Antibacterial, Hemolysis, Proteases) but inhibit macrophage-related functions (Phagocytosis, Wound Healing) in earthworms. J Invertebr Pathol 65:217–224

    Article  CAS  Google Scholar 

  • Wågman N, Strandberg B, Tysklind M (2001) Dietary uptake and elimination of selected polychlorinated biphenyls congeners and hexachlorobenzene in earthworms. Environ Toxicol Chem 8:1778–1784

    Article  Google Scholar 

  • Wagner A, Adrian L, Kleinsteuber S, Andreesen JR, Lechner U (2009) Transcription analysis of genes encoding homologues of reductive dehalogenases in “Dehaloccoides” sp. Strain CBDB1 by using terminal restriction fragment length polymorphism and quantitative PRC. Appl Environ Microbiol 7:1876–1884

    Article  Google Scholar 

  • Watts JEM, Fagervold SK, May HD, Sowers KR (2005) A PCR-based specific assay reveals a population of bacteria within the Chloroflexi associated with the reductive dehalogenation of polychlorinated biphenyls. Microbiology 151:2039–2046

    Article  CAS  Google Scholar 

  • Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703

    CAS  Google Scholar 

  • Welander U (2005) Microbial degradation of organic pollutants in soil in a cold climate. Soil Sed Contam 14:281–291

    CAS  Google Scholar 

  • Wiegel J, Wu Q (2000) Microbial reductive dehalogenation of polychlorinated buphenyls. FEMS Microbiol Ecol 32:1–15

    Article  CAS  Google Scholar 

  • Wilke B-M, Bräutigam L (1992) Effects of polychlorinated biphenyls on soil microbial activity. Zur Pflanzenernährung och Bodenkultur 155:483–488

    Article  CAS  Google Scholar 

  • Witzig R, Junca H, Hecht H-J, Pieper DH (2006) Assessment of toluene/biphenyl dioxygenase gene diversity in benzene-polluted soils: link between benzene biodegradation and genes similar to those encoding isopropylbenzene dioxygenases. Appl Environ Microbiol 5:3504–3514

    Article  Google Scholar 

  • Wu Q, Bedard DL, Wiegel J (1997) Temperature determines the pattern of anaerobic microbial dechlorination of Aroclor 1260 primed by 2,3,4,6-tetrachlorobiphenyl in Woods Pond sediment. Appl Environ Microbiol 63:4818–4825

    CAS  Google Scholar 

  • Zharikov GA, Borovick RV, Kapranov VV, Kiseleva NI, Krainova OA, Dyadishcheva VP, Shalanda AV, Zharikov MG (2007) Study of contamination and Migration Polychlorinated biphenyls in the environment. Bioremediation of contaminated soils and assessment of their impact on the Serpukhov population health. In: Heipieper HJ (ed) Bioremediation of Soils Contaminated with Aromatic Compounds. Springer, Amsterdam, The Netherlands, pp 93–104

    Chapter  Google Scholar 

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Acknowledgments

The authors are grateful for Kadeco, Rio Tinto Alcan, Nordplus Express Mobility Grant, University of Iceland Graduate Travel Grant and SoilSoc–Nordic Network on Soils and Society for financial support for the project. Elin V. Magnusdóttir at the University of Iceland and Sunna Áskelsdóttir at the Agricultural University of Iceland are acknowledged for assistance and guidance in the laboratory work. Kristina Lindström at the University of Helsinki is thanked for senior advice and microbiological laboratory facilities.

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Authors and Affiliations

  1. Faculty of Earth Sciences, University of Iceland, Askja, Sturlugata 7, 101, Reykjavik, Iceland

    Taru Lehtinen & Kristín Vala Ragnarsdóttir

  2. Department of Environmental Sciences, Agricultural University of Iceland, Hvanneyri, 311, Borgarnes, Iceland

    Taru Lehtinen

  3. Department of Food and Environmental Sciences, University of Helsinki, P.O. Box 56, 00014, Helsinki, Finland

    Anu Mikkonen

  4. Reykjavik Energy, Bæjarhálsi 1, 110, Reykjavík, Iceland

    Bergur Sigfusson

  5. Department of Pharmacology and Toxicology, University of Iceland, Hofsvallagata 53, 107, Reykjavík, Iceland

    Kristín Ólafsdóttir

  6. Department of Land Resources, Agricultural University of Iceland, Hvanneyri, 311, Borgarnes, Iceland

    Rannveig Guicharnaud

  7. Land Resource Management Unit, Soil Action, Institute for Environment & Sustainability (IES), European Commission–DG JRC, Via E. Fermi, 2749, 21027, Ispra, VA, Italy

    Rannveig Guicharnaud

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  1. Taru Lehtinen
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  5. Kristín Vala Ragnarsdóttir
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Correspondence to Taru Lehtinen.

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Lehtinen, T., Mikkonen, A., Sigfusson, B. et al. Bioremediation trial on aged PCB-polluted soils—a bench study in Iceland. Environ Sci Pollut Res 21, 1759–1768 (2014). https://doi.org/10.1007/s11356-013-2069-z

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