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Plant-Assisted Bioremediation: An Ecological Approach for Recovering Multi-contaminated Areas

  • Valeria Ancona
  • Paola Grenni
  • Anna Barra CaraccioloEmail author
  • Claudia Campanale
  • Martina Di Lenola
  • Ida Rascio
  • Vito Felice Uricchio
  • Angelo Massacci
Conference paper
Part of the Sustainability in Plant and Crop Protection book series (SUPP)

Abstract

Plant-based clean up technologies are gaining popularity as a sustainable solution to contaminated soil remediation. In particular, plant-assisted bioremediation or phyto-assisted bioremediation exploits the synergistic action between plant root systems and natural microorganisms (bacteria and fungi) to remove, convert or contain toxic substances in soils, sediments or water. It can be applied successfully to contaminated areas. It relies on the use of a selected appropriate plant species for stimulating the biodegradation activity of natural soil microorganisms in the rhizosphere (e.g. through root exudates production or oxygen transport). Plant species can also produce extracellular enzymes that directly transform contaminants and/or make them more bioavailable. Moreover, they can also phyto-contain them. In selecting the plant species, the specific contaminant/s to be removed, and the local geopedological and climatic conditions need to be considered. Beyond the contaminant removal, there are additional benefits such as soil quality improvement, soil carbon sequestration and biomass production for energy purposes. The difficulties in remediating areas characterized by multiple pollutant occurrence (e.g. organic and inorganic toxic compounds) make the study of plant-microbial interactions important if sustainable soil recovery strategies are to be achieved. Consequently, in recent years, several plant species have been tested for stimulating natural microbial communities and supporting the remediation of contaminated soils. Among these, the poplar tree can be considered suitable for plant-assisted bioremediation purposes. In this chapter an example of the methodological approach used for its application to an area multi-contaminated (by polychlorinated biphenyls and heavy metals) is illustrated.

Keywords

Polychlorinated biphenyls (PCBs) Heavy metals Poplar 

Notes

Acknowledgements

The authors acknowledge CISA S.p.A. (Massafra, Italy), which partially funded the Research Project “Applicazione di tecniche di fitorimedio a basso costo in località ex campo Cimino-Manganecchia a Taranto”, Prot. IRSA-CNR N. 0005159, 04/12/2012.

Authors thank contribution by COST Action FP1305 “BioLink-Linking belowground biodiversity and ecosystem function in European forests”.

References

  1. Ancona, V., Barra Caracciolo, A., Grenni, P., Di Lenola, M., Campanale, C., Calabrese, A., Uricchio, V. F., Mascolo, G., & Massacci, A. (2017). Plant-assisted bioremediation of a historically PCB and heavy metal-contaminated area in Southern Italy. New Biotechnology: Part B, 38, 65–73.CrossRefGoogle Scholar
  2. Artigas, J., Arts, G., Babut, B., Barra Caracciolo, A., Charles, S., Chaumot, A., Combourieu, B., Dahllöf, I., Despréaux, D., Ferrari, B., Friberg, N., Garric, J., Geffard, O., Gourlay-Francé, C., Hein, M., Hjorth, M., Krauss, M., De Lange, H. J., Lahr, J., Lehtonen, K. K., Lettieri, T., Liess, M., Lofts, S., Mayer, P., Morin, S., Paschke, A., Svendsen, C., Usseglio-Polatera, P., van den Brink, N., Vindimian, E., & Williams, R. (2012). Towards a renewed research agenda in eco toxicology. Environmental Pollution, 160, 201–206.CrossRefPubMedGoogle Scholar
  3. Bais, H., Weir, T., Perry, L., Gilroy, S., & Vivanco, J. (2006). The role of root exudates in rhizosphere interactions with plants and other organisms. Annual Review of Plant Biology, 57, 233–266.CrossRefPubMedGoogle Scholar
  4. Barra Caracciolo, A., Bottoni, P., & Grenni, P. (2013). Microcosm studies to evaluate microbial potential to degrade pollutants in soil and water ecosystems. Microchemical Journal, 107, 126–130.CrossRefGoogle Scholar
  5. Barra Caracciolo, A., Bustamante, M. A., Nogues, I., Di Lenola, M., Luprano, M. L., & Grenni, P. (2015). Changes in microbial community structure and functioning of a semiarid soil due to the use of anaerobic digestate derived composts and rosemary plants. Geoderma, 245–246, 89–97.CrossRefGoogle Scholar
  6. Baldantoni, D., Bellino, A., Cicatelli, A., & Castiglione, S. (2011). Artificial mycorrhization does not influence the effects of iron availability on Fe, Zn, Cu, Pb and Cd accumulation in leaves of a heavy metal tolerant white poplar clone. Plant Biosystems, 145, 236–240.CrossRefGoogle Scholar
  7. Bert, V., Allemon, J., Sajet, P., Dieu, S., Papin, A., Collet, S., Gaucher, R., Chalot, M., Michiels, B., & Raventos, C. (2017). Torrefaction and pyrolysis of metal-enriched poplars from phytotechnologies: Effect of temperature and biomass chlorine content on metal distribution in endproducts and valorization options. Biomass and Bioenergy, 96, 1–11.CrossRefGoogle Scholar
  8. Bianconi, D., De Paolis, M. R., Agnello, M. C., Lippi, D., Pietrini, F., Zacchini, M., Polcaro, C., Donati, E., Paris, P., Spina, S., & Massacci, A. (2010). Field-scale rhyzoremediation of a contaminated soil with hexachlorocyclohexane (HCH) isomers: The potential of poplars for environmental restoration. In I. A. Golubev (Ed.), Phytoremediation: Processes, characteristics, and applications (pp. 783–794). Hauppauge: Nova Science Publisher.Google Scholar
  9. Bru, D., Ramette, A., Saby, N. P., Dequiedt, S., Ranjard, L., Jolivet, C., Arrouays, D., & Philippot, L. (2011). Determinants of the distribution of nitrogen-cycling microbial communities at the landscape scale. The ISME Journal, 5, 532–542.CrossRefPubMedGoogle Scholar
  10. Chekol, T., Vough, L. R., & Chaney, R. L. (2004). Phytoremediation of polychlorinated biphenyl-contaminated soils: The rhizosphere effect. Environment International Journal, 30, 799–804.CrossRefGoogle Scholar
  11. Di Baccio, D., Tognetti, R., Sebastiani, L., & Vitagliano, C. (2003). Responses of Populus deltoides x Populus nigra (Populus x euramericana) clone I-214 to high zinc concentrations. New Phytologist, 159, 443–452.CrossRefGoogle Scholar
  12. Ding, N., Hayat, T., Wang, J. E., Wang, H. Z., Liu, X. M., & Xu, J. M. (2011). Responses of microbial community in rhizosphere soils when ryegrass was subjected to stress from PCBs. Journal of Soils Sediments, 11, 1355–1362.CrossRefGoogle Scholar
  13. Dzantor, E. K., Chekol, T., & Vough, L. R. (2000). Feasibility of using forage grasses and legumes for phytoremediation of organic pollutants. Journal of Environmental Science and Health, 35, 1645–1661.CrossRefGoogle Scholar
  14. EC (European Commission). (2009). Directive 2009/28/EC of the European Parliament and of the Council of 23 April 2009 on the promotion of the use of energy from renewable sources and amending and subsequently repealing Directives 2001/77/EC and 2003/30/EC. Official Journal of the European Union L, 140, 16–62.Google Scholar
  15. Field, J. A., & Sierra-Alvarez, R. (2008). Microbial transformation and degradation of polychlorinated biphenyls. Environmental Pollution, 155, 1–12.CrossRefPubMedGoogle Scholar
  16. Fierer, N., & Jackson, R. B. (2006). The diversity and biogeography of soil bacterial communities. Proceedings of the National Academy of Sciences, USA, 103, 626–631.CrossRefGoogle Scholar
  17. Furukawa, K. (2000). Biochemical and genetic bases of microbial degradation of polychlorinated biphenyls (PCBs). Journal of General and Applied Microbiology, 46, 283–296.CrossRefPubMedGoogle Scholar
  18. Gamalero, E., Cesaro, P., Cicatelli, A., Todeschini, V., Musso, C., et al. (2012). Poplar clones of different sizes, grown on a heavy metal polluted site, are associated with microbial populations of varying composition. Science of Total Environment, 425, 262–270.CrossRefGoogle Scholar
  19. Grenni, P., Rodriguez-Cruz, M. S., Herrero-Hernandez, E., Marin-Benito, J. M., Sanchez-Martin, M. J., & Barra Caracciolo, A. (2012). Effects of wood amendments on the degradation of terbuthylazine and on soil microbial community activity in a clay loam soil. Water, Air and Soil Pollution, 223, 5401–5412.CrossRefGoogle Scholar
  20. Hinojosa, M. B., Carreira, J. A., García-Ruíz, R., & Dick, R. P. (2005). Microbial response to heavy metal-polluted soils: Community analysis from phospholipid-linked fatty acids and ester-linked fatty acids extracts. Journal of Environmental Quality, 34, 1789–1800.CrossRefPubMedGoogle Scholar
  21. Hinojosa, M. B., Parra, A., Laudicina, V. A., & Moreno, J. M. (2016). Post-fire soil functionality and microbial community structure in a Mediterranean shrubland subjected to experimental drought. Science of the Total Environment, 573, 1178–1189.CrossRefPubMedGoogle Scholar
  22. Hinsinger, P., Bengough, A. G., Vetterlein, D., & Young, I. M. (2009). Rhizosphere: Biophysics, biogeochemistry and ecological relevance. Plant and Soil, 321, 117–152.CrossRefGoogle Scholar
  23. ITRC. (2009). Phytotechnology. Technical and regulatory guidance and decision trees, revised. Available at http://www.scribd.com/doc/67998102/Phytotechnology-Technical-and-Regulatory-Guidance-and-Decision-Trees-Revised
  24. Laudicina, V. A., Dennis, P. G., Palazzolo, E., & Badalucco, L. (2012). Key biochemical attributes to assess soil ecosystem sustainability. In A. Malik & E. Grohmann (Eds.), Environmental protection strategies for sustainable development (pp. 193–227). Cham: Springer.Google Scholar
  25. Liu, J., & Schnoor, J. L. (2008). Uptake and translocation of lesser chlorinated polychlorinated biphenyls (PCBs) in whole hybrid of poplar plants after hydroponic exposure. Chemosphere, 73, 1608–1616.CrossRefPubMedPubMedCentralGoogle Scholar
  26. Madejón, P., Marañón, T., Murillo, J. M., & Robinson, B. (2004). White poplar (Populus alba) as a biomonitor of trace elements in contaminated riparian forests. Environmental Pollution, 132, 145–155.CrossRefPubMedGoogle Scholar
  27. Matturro, B., Ubaldi, C., Grenni, P., Barra Caracciolo, A., & Rossetti, S. (2016). Polychlorinated biphenyl (PCB) anaerobic degradation in marine sediments: Microcosm study and role of autochtonous microbial communities. Environmental Science and Pollution Research, 23, 12613–12623.CrossRefPubMedGoogle Scholar
  28. Massacci, A., Bianconi, D., & Paris, P. (2012). Pioppicoltura a turno di taglio breve per bioenergia e fitorimedio. SILVÆ, 7, 125–144.Google Scholar
  29. Meggo, R. E., & Schnoor, J. L. (2013). Rhizosphere redox cycling and implications for rhizosphere biotransformation of selected polychlorinated biphenyl (PCB) congeners. Ecological Engineering, 57, 285–292.CrossRefPubMedPubMedCentralGoogle Scholar
  30. Meggo, R. E., Schnoor, J. L., & Hu, D. (2013). Dechlorination of PCBs in the rhizosphere of switchgrass and poplar. Environmental Pollution, 178, 312–321.CrossRefPubMedPubMedCentralGoogle Scholar
  31. Musilova, L., Ridl, J., Polivkova, M., Macek, T., & Uhlik, O. (2016). Effects of secondary plant metabolites on microbial populations: Changes in community structure and metabolic activity in contaminated environments. International Journal of Molecular Science, 17, E1205.CrossRefGoogle Scholar
  32. Ohtsubo, Y., Kudo, T., Tsuda, M., & Nagata, Y. (2004). Strategies for bioremediation of polychlorinated biphenyls. Applied Microbiology and Biotechnology, 65, 250–258.CrossRefPubMedGoogle Scholar
  33. Pham, T. T., Pino Rodriguez, N. J., Hijri, M., & Sylvestre, M. (2015). Optimizing polychlorinated biphenyl degradation by flavonoid-induced cells of the rhizobacterium Rhodococcus erythropolis U23A. PLoS One, 10, e0126033.CrossRefPubMedPubMedCentralGoogle Scholar
  34. Philippot, L., Raaijmakers, J. M., Lemanceau, P., & van der Putten, W. M. (2013). Going back to the roots: the microbial ecology of the rhizosphere. Nature Review Microbiology, 11, 789–799.CrossRefPubMedGoogle Scholar
  35. Pieper, D. H. (2005). Aerobic degradation of polychlorinated biphenyls. Applied Microbiology and Biotechnology, 67, 170–191.CrossRefPubMedGoogle Scholar
  36. Pieper, D., & Seeger, M. (2008). Bacterial metabolism of polychlorinated biphenyls. Journal of Molecular Microbiology and Biotechnology, 15, 121–133.CrossRefPubMedGoogle Scholar
  37. Pietrini, F., Zacchini, M., Iori, V., Pietrosanti, L., Bianconi, D., & Massacci, A. (2010). Screening of poplar clones for cadmium phytoremediation using photosynthesis, biomass and cadmium content analyses. International Journal of Phytoremediation, 12, 1–16.Google Scholar
  38. Pilon-Smits, E. (2005). Phytoremediation. Annual Review of Plant Biology, 56, 15–39.CrossRefPubMedGoogle Scholar
  39. Qin, H., Brookes, P. C., & Xu, J. (2014). Cucurbita spp. and Cucumis sativus enhance the dissipation of polychlorinated biphenyl congeners by stimulating soil microbial community development. Environmental Pollution, 184, 306–312.CrossRefPubMedGoogle Scholar
  40. Schutter, M. E., & Dick, R. P. (2000). Comparison of fatty acid methyl ester (FAME) methods for characterizing microbial communities. Soil Science Society of America Journal, 64, 1659–1668.CrossRefGoogle Scholar
  41. Sebastiani, L., Scebba, F., & Tognetti, R. (2004). Heavy metal accumulation and growth responses in poplar clones Eridano (Populus deltoides × maximowiczii) and I-214 (P. × euramericana) exposed to industrial waste. Environmental and Experimental Botany, 52, 79–88.CrossRefGoogle Scholar
  42. Soudek, P., Tykva, R., & Vanek, T. (2004). Laboratory analyses of 137Cs uptake by sunflower, reed and poplar. Chemosphere, 55, 1081–1087.CrossRefPubMedGoogle Scholar
  43. Sylvestre, M., & Toussaint, J. P. (2011). Engineering microbial enzymes and plants to promote PCB degradation in soil: Current state of knowledge. In A. I. Koukkou (Ed.), Microbial bioremediation of nonmetals – Current research (pp. 177–196). Norfolk: Caister Academic.Google Scholar
  44. Teng, Y., Luo, Y., Sun, X., Tu, C., Xu, L., Liu, W., Li, Z., & Christie, P. (2010). Influence of arbuscular mycorrhiza and Rhizobium on phytoremediation by alfalfa of an agricultural soil contaminated with weathered PCBs: A field study. International Journal of Phytoremediation, 12, 516–533.CrossRefPubMedGoogle Scholar
  45. Thijs, S., Sillen, W., Rineau, F., Weyens, N., & Vangronsveld, J. (2016). Towards an enhanced understanding of plant-microbiome interactions to improve phytoremediation: Engineering the metaorganism. Frontiers in Microbiology, 7, 341.CrossRefPubMedPubMedCentralGoogle Scholar
  46. Tsednee, M., Mak, Y. W., Chen, Y. R., & Yeh, K. C. (2012). A sensitive LC-ESI-Q-TOF-MS method reveals novel phytosiderophores and phytosiderophore–iron complexes in barley. New Phytologist, 195, 951–961.CrossRefPubMedGoogle Scholar
  47. Toussaint, J. P., Pham, T. T., Barriault, D., & Sylvestre, M. (2012). Plant exudates promote PCB degradation by a rhodococcal rhizobacteria. Applied Microbiology and Biotechnology, 95, 1589–1603.CrossRefPubMedGoogle Scholar
  48. US EPA. (2010). Superfund green remediation strategy. U.S. Environmental Protection Agency, Office of Solid Waste and Emergency Response, Office of Superfund Remediation and Technology Innovation. Available at https://www.epa.gov/sites/production/files/2016-01/documents/175857.pdf
  49. Wenzel, W. W. (2009). Rhizosphere processes and management in plant-assisted bioremediation (phytoremediation) of soils. Plant and Soil, 321, 385–408.CrossRefGoogle Scholar
  50. Wiegel, J., & Wu, Q. (2000). Microbial reductive dehalogenation of polychlorinated biphenyls. FEMS Microbiology and Ecology, 32, 1–15.CrossRefGoogle Scholar
  51. Xu, L., Teng, Y., Li, Z. G., Norton, J. M., & Luo, Y. M. (2010). Enhanced removal of polychlorinated biphenyls from alfalfa rhizosphere soil in a field study: The impact of a rhizobial inoculum. Science of Total Environment, 408, 1007–1013.CrossRefGoogle Scholar
  52. Zanaroli, G., Balloi, A., Negroni, A., Borruso, L., Daffonchio, D., & Fava, F. (2012). Chloroflexi bacterium dechlorinates polychlorinated biphenyls in marine sediments under in sit-like biogeochemical conditions. Journal of Hazardous Materials, 209, 449–457.CrossRefPubMedGoogle Scholar
  53. Zhai, G., Hu, D., Lehmler, H. J., & Schnoor, J. L. (2011). Enantioselective biotransformation on chiral PCBs in whole poplar plants. Environmental Science and Technology, 45, 2308–2316.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Valeria Ancona
    • 1
  • Paola Grenni
    • 2
  • Anna Barra Caracciolo
    • 2
    Email author
  • Claudia Campanale
    • 1
  • Martina Di Lenola
    • 2
  • Ida Rascio
    • 1
  • Vito Felice Uricchio
    • 1
  • Angelo Massacci
    • 3
  1. 1.CNR-IRSA, National Research CouncilWater Research InstituteBariItaly
  2. 2.National Research Council, Water Research InstituteCNR-IRSAMonterotondoItaly
  3. 3.CNR-IBAF, National Research CouncilInstitute of Agroenvironmental and Forestry BiologyRomeItaly

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