Environmental Science and Pollution Research

, Volume 21, Issue 3, pp 1759–1768 | Cite as

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

  • Taru Lehtinen
  • Anu Mikkonen
  • Bergur Sigfusson
  • Kristín Ólafsdóttir
  • Kristín Vala Ragnarsdóttir
  • Rannveig Guicharnaud
Research Article

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.

Keywords

PCB Aerobic bioremediation Anaerobic bioremediation Cold regions Bench study Volcanic soils Bioavailability 

References

  1. Abraham W-R, Nogales B, Golyshin PN, Pieper DH, Timmis KN (2002) Polychlorinated biphenyls-degrading microbial communities in soils and sediments. Curr Opin Microbiol 5:246–253CrossRefGoogle Scholar
  2. Aislabie J, Saul DJ, Foght JM (2006) Bioremediation of hydrocarbon-contaminated polar soils. Extremophiles 10:171–179CrossRefGoogle Scholar
  3. Alexander M (1999) Biodegradation and bioremediation, 2nd edn. Academic, California, USAGoogle Scholar
  4. Anderson MJ, Robinson J (2003) Generalized discriminant analysis based on distances. Aust New Z J Stat 45:301–318CrossRefGoogle Scholar
  5. Arnalds O (2004) Volcanic soils of Iceland. Catena 56:3–20CrossRefGoogle Scholar
  6. Arnalds O, Óskarsson H, Gísladóttir FO, Grétarsson E (2009) Soil map of Iceland. The Agricultural University of Iceland, Reykajvik, IcelandGoogle Scholar
  7. 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 CouncilGoogle Scholar
  8. 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]Google Scholar
  9. 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 ZealandGoogle Scholar
  10. Borja J, Taleon DM, Auresenia J, Gallardo S (2005) Polychlorinated biphenyls and their biodegradation. Process Biochem 40:1999–2013CrossRefGoogle Scholar
  11. Crawford RL, Crawford DL (eds) (2005) Bioremediation: Principles and Applications. Cambridge University Press, New York, USAGoogle Scholar
  12. Donnelly PK, Hedge RS, Fletcher JS (1994) Growth of PCB-degrading bacteria on compounds from photosynthetic plants. Chemosphere 28(5):981–988CrossRefGoogle Scholar
  13. Erickson MD (1997) Analytical chemistry of PCBs, 2nd edn. CRC Press LLC, Florida, USAGoogle Scholar
  14. 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):3009–3018CrossRefGoogle Scholar
  15. 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 81:381–390Google Scholar
  16. 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 445–446:237–260CrossRefGoogle Scholar
  17. Guicharnaud R, Paton GI (2006) An evaluation of acid deposition on cation leaching weathering rates of an Andosol and Cambisol. J Geochem Explor 88:279–283CrossRefGoogle Scholar
  18. Guicharnaud R, Arnalds O, Paton GI (2010) Short term changes of microbial processes of Icelandic soils to increasing temperatures. Biogeosciences 7:671–682CrossRefGoogle Scholar
  19. 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 63:1532–1538CrossRefGoogle Scholar
  20. 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 8:153–158CrossRefGoogle Scholar
  21. 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], ReykjavíkGoogle Scholar
  22. 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 212:21–33Google Scholar
  23. 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 51:5607–5611CrossRefGoogle Scholar
  24. 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 ppGoogle Scholar
  25. Jörundsdóttir H (2009) Temporal and spatial trends of organohalogens in guillemot (Uria aalge) from North Western Europe. Dissertation, Stockholm University, SwedenGoogle Scholar
  26. Jota MA, Hassett JP (1991) Effects of environmental variables on binding of a PCB congener by dissolved humic substances. Environ Toxicol Chem 10:483–491CrossRefGoogle Scholar
  27. 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 101:124–133CrossRefGoogle Scholar
  28. 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 ChemistryGoogle Scholar
  29. 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 46:423–437CrossRefGoogle Scholar
  30. Kuipers B, Cullen WR, Mohn WW (2003) Reductive dechlorination of weathered Aroclor 1260 during anaerobic biotreatment of Arctic soils. Can J Microbiol 49:9–14CrossRefGoogle Scholar
  31. 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 102:1318–1329CrossRefGoogle Scholar
  32. Margesin R (2007) Alpine microorganisms: useful tools for low-temperature bioremediation. J Microbiol 4:281–285Google Scholar
  33. Master ER, Mohn WW (1998) Psychrotolerant bacteria isolated from Arctic soil that degrade polychlorinated biphenyls at low temperatures. Appl Environ Microbiol 64:4823–4829Google Scholar
  34. 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, IcelandGoogle Scholar
  35. Michel Jr FC, Quensen J, Reddy CA (2001) Bioremediation of a PCB-contaminated soil via composting. Compost Science & Utilization 9:274–284Google Scholar
  36. Mohn WW, Westerberg K, Cullen WR, Reimer KJ (1997) Aerobic biodegradation of biphenyl and polychlorinated biphenyls by Arctic soil microorganisms. Appl Environ Microbiol 63:3378–3384Google Scholar
  37. Ohtsubo Y, Kudo T, Tsuda M, Nagata Y (2004) Strategies for bioremediation of polychlorinated biphenyls. Appl Microbiol Biotechnol 65:250–258Google Scholar
  38. Ólafsdóttir K, Petersen A, Thórdadóttir S, Jóhannesson T (1995) Organochlorine residues in Gyrfalcons (Falco rusticolus) in Iceland. Bull Environ Contam Toxicol 55:382–389CrossRefGoogle Scholar
  39. 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 133:509–515CrossRefGoogle Scholar
  40. Parfitt RL, (1990) Allophane in New Zealand – A review. Aust J Soil Res 28:343–360Google Scholar
  41. 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 26:121–144Google Scholar
  42. 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):804–810Google Scholar
  43. Pieper DH (2005) Aerobic degradation of polychlorinated biphenyls. Appl Microbiol Biotechnol 67:170–191CrossRefGoogle Scholar
  44. 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 35:663–668CrossRefGoogle Scholar
  45. 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 4:2476–2482CrossRefGoogle Scholar
  46. Ross G (2004) The public health implications of polychlorinated biphenyls (PCBs) in the environment. Ecotoxicol Environ Saf 59:275–291CrossRefGoogle Scholar
  47. Safe SH (1994) Polychlorinated biphenyls (PCBs): environmental impact, biochemicals and toxic responses, and implications for risk assessment. Crit Rev Toxicol 24:87–149CrossRefGoogle Scholar
  48. Shoji S, Nanzyo M, Dahlgren R (1993) Volcanic ash soils: Genesis, Properties, and Utilization. Developments in Soil Science: 21. Elsevier, The NetherlandsGoogle Scholar
  49. Sigurgeirsson MA, Arnalds O, Palsson SE, Howard BJ, Gudnason K (2005) Radioceasium fallout behaviour in volcanic soils in Iceland. J Environ Radioact 79(1):39–53CrossRefGoogle Scholar
  50. Smith KA, Mullins CE (eds) (2001) Soil and Environmental Analysis: Physical methods, 2nd edn. Marcel Dekker, New YorkGoogle Scholar
  51. Tharakan J, Tomlinson D, Addagada A, Shafagati A (2006) Biotransformation of PCBs in contaminated sludge: potential for novel biological technologies. Eng Life Sci 6:43–50CrossRefGoogle Scholar
  52. Tiedje JM, Quensen JF III, Chee-Sanford J, Schimel JP, Cole JA, Boyd SA (1993) Microbial reductive dechlorination of PCBs. Biodegradation 4:231–240CrossRefGoogle Scholar
  53. Trevors JT (1984) Dehydrogenase activity in soil: a comparison between the INT and TTC assay. Soil Biol Biochem 16:673–674CrossRefGoogle Scholar
  54. Ulbrich B, Stahlmann R (2004) Developmental toxicity of polychlorinated biphenyls (PCBs): a systematic review of experimental data. Arch Toxicol 78:252–268Google Scholar
  55. UNEP/AMAP (2011) Climate Change and POPS : Predicting the Impacts. Report of the UNEP/AMAP Expert Group. Secreteriat of the Stockholm Convention, Geneva, p 62Google Scholar
  56. Vasilyeva GK, Strijakova ER (2007) Bioremediation of soils and sediments contaminated by polychlorinated biphenyls. Microbiology 76:639–653CrossRefGoogle Scholar
  57. 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 65:217–224CrossRefGoogle Scholar
  58. Wågman N, Strandberg B, Tysklind M (2001) Dietary uptake and elimination of selected polychlorinated biphenyls congeners and hexachlorobenzene in earthworms. Environ Toxicol Chem 8:1778–1784CrossRefGoogle Scholar
  59. 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 7:1876–1884CrossRefGoogle Scholar
  60. 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 151:2039–2046CrossRefGoogle Scholar
  61. Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703Google Scholar
  62. Welander U (2005) Microbial degradation of organic pollutants in soil in a cold climate. Soil Sed Contam 14:281–291Google Scholar
  63. Wiegel J, Wu Q (2000) Microbial reductive dehalogenation of polychlorinated buphenyls. FEMS Microbiol Ecol 32:1–15CrossRefGoogle Scholar
  64. Wilke B-M, Bräutigam L (1992) Effects of polychlorinated biphenyls on soil microbial activity. Zur Pflanzenernährung och Bodenkultur 155:483–488CrossRefGoogle Scholar
  65. 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 5:3504–3514CrossRefGoogle Scholar
  66. 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 63:4818–4825Google Scholar
  67. 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 93–104CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Taru Lehtinen
    • 1
    • 2
  • Anu Mikkonen
    • 3
  • Bergur Sigfusson
    • 4
  • Kristín Ólafsdóttir
    • 5
  • Kristín Vala Ragnarsdóttir
    • 1
  • Rannveig Guicharnaud
    • 6
    • 7
  1. 1.Faculty of Earth SciencesUniversity of IcelandReykjavikIceland
  2. 2.Department of Environmental SciencesAgricultural University of IcelandBorgarnesIceland
  3. 3.Department of Food and Environmental SciencesUniversity of HelsinkiHelsinkiFinland
  4. 4.Reykjavik EnergyReykjavíkIceland
  5. 5.Department of Pharmacology and ToxicologyUniversity of IcelandReykjavíkIceland
  6. 6.Department of Land ResourcesAgricultural University of IcelandBorgarnesIceland
  7. 7.Land Resource Management Unit, Soil Action, Institute for Environment & Sustainability (IES)European Commission–DG JRCIspraItaly

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