Skip to main content
SpringerLink
Log in

Effects of Apirolio Addition and Alfalfa and Compost Treatments on the Natural Microbial Community of a Historically PCB-Contaminated Soil

  • Published:
Water, Air, & Soil Pollution Aims and scope Submit manuscript

Abstract

Polychlorinated biphenyls (PCBs) are ubiquitous and persistent organic pollutants generated exclusively from human sources and found in the environment as several congeners (e.g. Apirolio, produced in Italy and used for electrical transformers). To evaluate the ability of the natural microbial community of historically PCB-contaminated soil to transform or degrade PCBs after fresh contamination through the addition of Apirolio, a microcosm experiment was conducted in a greenhouse for approximately 8 months. Compost and Medicago sativa (alfalfa) were additionally used in the microcosms to stimulate microbial PCB degradation. Chemical analyses were performed to evaluate PCB concentrations in the soil and plant tissue. Changes in the microbial community under the different experimental conditions were evaluated in terms of total abundance, viability, diversity, and activity. Interestingly, the addition of Apirolio did not negatively affect the microbial community but did stimulate the degradation of the freshly added PCBs. The plant and compost co-presence did not substantially increase PCB degradation, but it increased the microbial abundance and activity and the occurrence of α-Proteobacteria and fungi.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • 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. New Biotechnology: Part B, 38, 65–73.

    Article  CAS  Google Scholar 

  • Antolín-Rodríguez, J. M., Sánchez-Báscones, M., Martín-Ramos, P., Bravo-Sánchez, C. T., & Gil, J. M. (2016). Estimation of PCB content in agricultural soils associated with long-term fertilization with organic waste. Environmental Science and Pollution Research, 23, 12372–12383.

    Article  CAS  Google Scholar 

  • Barillot, C. D., Sarde, C. O., Bert, V., Tarnaud, E., & Cochet, N. (2013). A standardized method for the sampling of rhizosphere and rhizoplan soil bacteria associated to a herbaceous root system. Annales de Microbiologie, 63, 471–476.

    Article  CAS  Google Scholar 

  • Barra Caracciolo, A., Giuliano, G., Grenni, P., Cremisini, C., Ciccoli, R., & Ubaldi, C. (2005a). Effect of urea on degradation of terbuthylazine in soil. Environmental Toxicology and Chemistry, 24, 1035–1040.

    Article  Google Scholar 

  • Barra Caracciolo, A., Grenni, P., Cupo, C., & Rossetti, S. (2005b). In situ analysis of native microbial communities in complex samples with high particulate loads. FEMS Microbiology Letters, 253, 55–58.

    Article  CAS  Google Scholar 

  • Barra Caracciolo, A., Bottoni, P., & Grenni, P. (2010). The use of the FISH method in soil and water ecosystems: A new approach for studying the effect of xenobiotics on bacterial community structure. Environmental Toxicology and Chemistry, 92, 567–579.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Bedard, D. L., Wagner, R. E., Brennan, M. J., Haberl, M. L., & Brown, J. F. (1987). Extensive degradation of Aroclors and environmentally transformed polychlorinated biphenyls by Alcaligenes eutrophus H850. Applied and Environmental Microbiology, 53, 1094–1102.

    CAS  Google Scholar 

  • Bending, G. D., & Rodriguez-Cruz, M. S. (2007). Microbial aspects of the interaction between soil depth and biodegradation of the herbicide isoproturon. Chemosphere, 66, 664–671.

    Article  CAS  Google Scholar 

  • Bikram, B., Sagnik, C., Biswanath, B., Apurba, D. (2014). Microbial Remediation of Recalcitrant Aromatic Compounds. In: Krishna P. & Jayanta K.P. (Eds.). Industrial & Environmental Biotechnology. (pp 171–189). Studium Press (India) Pvt. Ltd.

  • Bossio, D. A., & Scow, K. M. (1998). Impacts of carbon and flooding on soil microbial communities: Phospholipid fatty acid profiles and substrate utilization patterns. Microbial Ecology, 35, 265–278.

    Article  CAS  Google Scholar 

  • Buée, M., De Boer, W., Martin, F., van Overbeek, L., & Jurkevitch, E. (2009). The rhizosphere zoo: An overview of plant-associated communities of microorganisms, including phages, bacteria, archaea, and fungi, and of some of their structuring factors. Plant and Soil, 321, 189–212.

    Article  CAS  Google Scholar 

  • Collins, C., Fryer, M., & Grosso, A. (2006). Plant uptake of non-ionic organic chemicals. Environmental Science & Technology, 40, 45.

    Article  CAS  Google Scholar 

  • Correia-Sá, L., Fernandes, V. C., Carvalho, M., Calhau, C., Domingues, V. M. F., & Delerue-Matos, C. (2012). Optimization of QuEChERS method for the analysis of organochlorine pesticides in soils with diverse organic matter. Journal of Separation Science, 35, 1521–1530.

    Article  CAS  Google Scholar 

  • Crecchio, C., Curci, M., Pizzigallo, M. D. R., Ricciuti, P., & Ruggiero, P. (2004). Effects of municipal solid waste compost amendments on soil enzyme activities and bacterial genetic diversity. Soil Biology and Biochemistry, 36, 1595–1605.

    Article  CAS  Google Scholar 

  • Chrisofi, N., & Ivshina, I. B. (2002). A review. Microbial surfactants and their use in field studies of soil remediation. Journal of Applied Microbiology, 93, 915–929.

    Article  Google Scholar 

  • de Cárcer, D. A., Martín, M., Karlson, U., & Rivilla, R. (2007). Changes in bacterial populations and in biphenyl dioxygenase gene diversity in a polychlorinated biphenyl-polluted soil after introduction of willow trees for rhizoremediation. Applied and Environmental Microbiology, 73, 6224–6232.

    Article  CAS  Google Scholar 

  • Doty, S. L. (2008). Enhancing phytoremediation through the use of transgenics and endophytes. The New Phytologist, 179, 318–333.

    Article  CAS  Google Scholar 

  • EFSA (2005). European Food Safety Authority. Opinion of the scientific panel on contaminants in the food chain on a request from the commission related to the presence of non dioxin-like polychlorinated biphenyls (PCB) in feed and food. The EFSA Journal, 284, 1–137.

  • Fava, F., & Piccolo, A. (2002). Effect of humic substances on the bioavailability aerobic biodegradation of polychlorinated biphenils in a model soil. Biothecnol Bioeng, 77, 204–211.

    Article  CAS  Google Scholar 

  • Ficko, S. A., Rutter, A., & Zeeb, B. A. (2011). Effect of pumpkin root exudates on ex situ polychlorinated biphenyl (PCB) phytoextraction by pumpkin and weed species. Environmental Science and Pollution Research, 18, 1536–1543.

    Article  CAS  Google Scholar 

  • Field, J. A., & Sierra-Alvarez, R. (2008). Microbial transformation and degradation of polychlorinated biphenyls. Environmental Pollution, 155, 1–12.

    Article  CAS  Google Scholar 

  • Frostegård, Å., Tunlid, A., & Bååth, E. (2011). Use and misuse of PLFA measurements in soils. Soil Biology and Biochemistry, 43, 1621–1625.

    Article  CAS  Google Scholar 

  • Greuter, D., Loy, A., Horn, M., & Rattei, T. (2016). probeBase-an online resource for rRNA-targeted oligonucleotide probes and primers: New features 2016. Nucleic Acids Research. https://doi.org/10.1093/nar/gkv1232.

  • Godoi, I., Sene, L., & Barra Caracciolo, A. (2014). Assessment of the bacterial community structure in a Brazilian clay soil treated with atrazine. Annales de Microbiologie, 64, 307–311.

    Article  CAS  Google Scholar 

  • Grenni, P., Barra Caracciolo, A., Rodríguez-Cruz, M. S., & Sánchez-Martín, M. J. (2009). Changes in the microbial activity in a soil amended with oak and pine residues and treated with linuron herbicide. Applied Soil Ecology, 41, 2–7.

    Article  Google Scholar 

  • Grenni, P., Rodríguez-Cruz, M. S., Herrero-Hernández, E., Marín-Benito, J. M., & 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Hinojosa, M. B., Parra, A., Laudicina, V. A., & Moreno, J. M. (2014). Experimental drought induces short-term changes in soil functionality and microbial community structure after fire in a Mediterranean shrub land. Biogeosciences Discussions, 11, 15251–15287.

    Article  Google Scholar 

  • Ionescu, M., Beranova, K., Dudkova, V., Kochankova, L., Demnerova, K., Macek, T., et al. (2009). Isolation and characterization of different plant associated bacteria and their potential to degrade polychlorinated biphenyls. International Biodeterioration and Biodegradation, 63, 667–672.

    Article  CAS  Google Scholar 

  • Jha, P., Panwar, G., & Jha, P. N. (2015). Secondary plant metabolites and root exudates: Guiding tools for polychlorinated biphenyl biodegradation. International journal of Environmental Science and Technology, 12, 789–802.

    Article  CAS  Google Scholar 

  • Kirk, J. L., Beaudette, L. A., Hart, M., Moutoglis, P., Klironomos, J. N., Lee, H., et al. (2004). Methods of studying soil microbial diversity. Journal of Microbiological Methods, 58, 169–188.

    Article  CAS  Google Scholar 

  • Komancová, M., Jurčová, I., Kochánková, L., & Burkhard, J. (2003). Metabolic pathways of polychlorinated biphenyls degradation by Pseudomonas sp. 2. Chemosphere, 50, 537–543.

    Article  Google Scholar 

  • Laudicina, V.A., Dennis, P.G., Palazzolo, E., Badalucco, L. (2012). Key biochemical attributes to assess soil ecosystem sustainability. In Environmental Protection Strategies for Sustainable Development (pp. 193–227). Springer Netherlands, Netherlands.

  • Leigh, M. B., Fletcher, J. S., Fu, X. O., & Schmit, F. J. (2002). Root turnover: An important source of microbial substrates in rhizosphere remediation of recalcitrant contaminants. Environmental Science & Technology, 36, 1579–1583.

    Article  CAS  Google Scholar 

  • Li, H., Liu, L., Lin, C., Wang, S. (2011) Plant uptake and in-soil degradation of PCB-5 under varying cropping conditions. Chemosphere, 84, 943–949.

  • Li, Y., Liang, F., Zhu, Y., & Wang, F. (2013). Phytoremediation of a PCB-contaminated soil by alfalfa and tall fescue single and mixed plants cultivation. Journal of Soils and Sediments, 13, 925–931.

    Article  CAS  Google Scholar 

  • Lugtenberg, B., & Kamilova, F. (2009). Plant-growth-promoting rhizobacteria. Annual Review of Microbiology, 63, 541–556.

    Article  CAS  Google Scholar 

  • McFarlane, J.C. (1995). Plant transport of organic chemicals. In: Trapp S. McFarlane J.C. Eds. Plant contamination-modelling and simulation of organic chemicals processes. Lewis Publisher: Boca Raton., FL.

  • Meggo, R. E., & Schnoor, J. L. (2013). Cleaning polychlorinated biphenyl (PCB) contaminated garden soil by phytoremediation. Environmental Science, 1, 33–52.

    Article  Google Scholar 

  • Meharg, A. A., & Cairney, J. W. G. (2000). Ectomycorrhizas - extending the capabilities of rhizosphere remediation? Soil Biology and Biochemistry, 32, 1475–1484.

    Article  CAS  Google Scholar 

  • Mocali, S., Galeffi, C., Perrin, E., Florio, A., Migliore, M., Canganella, F., et al. (2013). Alteration of bacterial communities and organic matter in microbial fuel cells (MFCs) supplied with soil and organic fertilizer. Applied Microbiology and Biotechnology, 97(3), 1299–1315.

    Article  CAS  Google Scholar 

  • Muir, D., & Sverko, E. (2006). Analytical methods for PCBs and organochlorine pesticides in environmental monitoring and surveillance: A critical appraisal. Analytical and Bioanalytical Chemistry, 386, 769–789.

    Article  CAS  Google Scholar 

  • Nannipieri, P., Ascher, J., Ceccherini, M., Landi, L., Pietramellara, G., & Renella, G. (2003). Microbial diversity and soil functions. European Journal of Soil Science, 54, 655–670.

    Article  Google Scholar 

  • Passatore, L., Rossetti, S., Juwarkar, A. A., & Massacci, A. (2014). Phytoremediation and bioremediation of polychlorinated biphenyls (PCBs): State of knowledge and research perspectives. Journal of Hazardous Materials, 278, 189–202.

    Article  CAS  Google Scholar 

  • Pernthaler, J., Glöckner, F. O., Schönhuber, W., & Amann, R. (2001). Fluorescence in situ hybridization (FISH) with rRNA-targeted oligonucleotide probes. Method Microbiol, 30, 207–226.

    Article  CAS  Google Scholar 

  • Philippot, L., Raaijmakers, J. M., Lemanceau, P., & van der Putten, W. H. (2013). Going back to the roots: The microbial ecology of the rhizosphere. Nature Reviews Microbiology, 11, 789–799.

    Article  CAS  Google Scholar 

  • Pieper, D. H., & Seeger, M. (2008). Bacterial metabolism of polychlorinated biphenyls. Journal of Molecular Microbiology and Biotechnology, 15, 121–138.

    Article  CAS  Google Scholar 

  • Praveckova, M., Brennerova, M. V., Holliger, C., DeAlencastro, F., & Rossi, P. (2016). Indirect evidence link PCB dehalogenation with Geobacteraceae in anaerobic sediment-free microcosms. Frontiers in Microbiology, 7, 933.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Rashid, A., Nawaz, S., Barker, H., Ahmad, I., & Ashraf, M. (2010). Development of a simple extraction and clean-up procedure for determination of organochlorine pesticides in soil using gas chromatography-tandem mass spectrometry. Journal of Chromatography, 1217, 2933–2939.

    Article  CAS  Google Scholar 

  • Salemi, A., Shafiei, E., & Vosough, M. (2012). Optimization of matrix solid phase dispersion coupled with gas chromatography electron capture detection for determination of chlorinated pesticides in soil. Talanta, 101, 1–550.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Semple, K. T., Reid, B. J., & Fermor, T. R. (2001). Impact of composting strategies on the treatment of soils contaminated with organic pollutants. Environmental Pollution, 112, 269–283.

    Article  CAS  Google Scholar 

  • Singer, A. C., Smith, D., Jury, W. A., Hathuc, K., & Crowley, D. E. (2003). Impact of the plant rhizosphere and augmentation on remediation of polychlorinated biphenyl contaminated soil. Environmental Toxicology and Chemistry, 22, 1998–2004.

    Article  CAS  Google Scholar 

  • Singh, B. K., Munro, S., Potts, J. M., & Millard, P. (2007). Influence of grass species and soil type on rhizosphere microbial community structure in grassland soils. Applied Soil Ecology, 36, 147–155.

    Article  Google Scholar 

  • Slater, H., Gouin, T., & Leigh, M. B. (2011). Assessing the potential for rhizoremediation of PCB contaminated soils in northern regions using native tree species. Chemosphere, 84, 199–206.

    Article  CAS  Google Scholar 

  • Song, M., Luoa, C., Li, F., Jiang, L., Wang, Y., Zhangd, D., et al. (2015). Anaerobic degradation of polychlorinated biphenyls (PCBs) and polychlorinated biphenyls ethers (PBDEs), and microbial community dynamics of electronic waste-contaminated soil. Science of the Total Environment, 502, 426–433.

    Article  CAS  Google Scholar 

  • Stella, T., Covino, S., Burianová, E., Filipová, A., Křesinová, Z., Voříšková, J., et al. (2015). Chemical and microbiological characterization of an aged PCB-contaminated soil. Science of the Total Environment, 533, 177–186.

    Article  CAS  Google Scholar 

  • Sylvestre, M., Toussaint, J.P. (2011). Engineering microbial enzymes and plants to promote PCB degradation in soil: Current State of Knowledge. In: Koukkou A.I. (Ed.). Microbial bioremediation of Nonmetals - Current Research. (pp 177–96). Norfolk (UK), Caister Academic.

  • Sylvestre, M. (2013). Prospects for using combined engineered bacterial enzymes and plant systems to rhizoremediate polychlorinated biphenyls. Environmental Microbiology, 15, 907–915.

    Article  CAS  Google Scholar 

  • Tehrani, R., & Van Aken, B. (2014). Hydroxylated polychlorinated biphenyls in the environment: Sources, fate, and toxicities. Environmental Science and Pollution Research, 21, 6334–6345.

    Article  CAS  Google Scholar 

  • Teng, Y., Shen, Y., Luo, Y., Sun, X., Sun, M., Fu, D., et al. (2011). Influence of Rhizobium meliloti on phytoremediation of polycyclic aromatic hydrocarbons by alfalfa in an aged contaminated soil. Journal of Hazardous Materials, 186, 1271–1276.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • US EPA (2005). Polychlorinated biphenyls (PCBs). Available on line at: http://www3.epa.gov/epawaste/hazard/tsd/pcbs/about.html.

  • US EPA. (2008). Method 1668, revision a: Chlorinated biphenyl congeners in water, soil, sediment and tissue by HRGC/HRMS. Washington DC: US Environmental Protection Agency 133 pp.

    Google Scholar 

  • Visoottiviseth, P., Francesconi, K., & Sridokchan, W. (2002). The potential of Thai indigenous plant species for the phytoremediation of arsenic contaminated land. Environmental Pollution, 118, 453–461.

    Article  CAS  Google Scholar 

  • White, J. C., Ross, D. D. W., Gent, M. P. N., Eitzer, B. D., & Mattina, M. I. (2006). Effect of mycorrhizal fungi on the phytoextraction of weathered p, p-DDE by Cucurbita pepo. Journal of Hazardous Materials, 137, 1750–1757.

    Article  CAS  Google Scholar 

  • Wiegel, J., & Wu, Q. Z. (2000). Microbial reductive dehalogenation of polychlorinated biphenyls. FEMS Microbiology Letters, 32, 1–15.

    Article  CAS  Google Scholar 

  • 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 the Total Environment, 408, 1007–1013.

    Article  CAS  Google Scholar 

  • Zelles, L. (1999). Fatty acid patterns of phospholipids and lipopolysaccharides in the characterization of microbial communities in soil: A review. Biology and Fertility of Soils, 29, 111–129.

    Article  CAS  Google Scholar 

  • Zhang, C., Du, Y., Tao, X. Q., Zhang, K., Shen, D. S., & Long, Y. Y. (2013). Dechlorination of polychlorinated biphenyl-contaminated soil via anaerobic composting with pig manure. Journal of Hazardous Materials, 261, 826–832.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Francesca Falconi for assisting in the microbiological analysis and Giuseppe Mascolo, Giuseppe Bagnuolo, Angelantonio Calabrese, and Claudia Campanale for their help in the chemical analyses.

Author information

Authors and Affiliations

  1. Istituto di Ricerca Sulle Acque-Consiglio Nazionale delle Ricerche, (CNR-IRSA), Rome, Italy

    Martina Di Lenola, Anna Barra Caracciolo, Paola Grenni & Jasmin Rauseo

  2. Istituto di Ricerca Sulle Acque-Consiglio Nazionale delle Ricerche, (CNR-IRSA), Bari, Italy

    Valeria Ancona & Vito Felice Uricchio

  3. Dipartimento Scienze Agrarie e Forestali, Università degli Studi di Palermo, Palermo, Italy

    Vito A. Laudicina

  4. Istituto di Biologia Agroambientale e Forestale-Consiglio Nazionale delle Ricerche, (CNR-IBAF), Rome, Italy

    Angelo Massacci

Authors
  1. Martina Di Lenola
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anna Barra Caracciolo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Paola Grenni
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Valeria Ancona
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jasmin Rauseo
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Vito A. Laudicina
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Vito Felice Uricchio
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Angelo Massacci
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Anna Barra Caracciolo.

Electronic supplementary material

ESM 1

(DOCX 20 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Di Lenola, M., Barra Caracciolo, A., Grenni, P. et al. Effects of Apirolio Addition and Alfalfa and Compost Treatments on the Natural Microbial Community of a Historically PCB-Contaminated Soil. Water Air Soil Pollut 229, 143 (2018). https://doi.org/10.1007/s11270-018-3803-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11270-018-3803-4

Keywords

Search

Navigation