Register      Login
Soil Research Soil Research Society
Soil, land care and environmental research
RESEARCH ARTICLE

Potential microbial remediation of pyrene polluted soil: the role of biochar

Lea Piscitelli https://orcid.org/0000-0002-5334-0485 A B D , Anna Daniela Malerba B , Giuseppe Natale Mezzapesa A , Stefano Dumontet C , Donato Mondelli B , Teodoro Miano B and Giovanni Luigi Bruno B
+ Author Affiliations
- Author Affiliations

A C.I.H.E.A.M. Bari, Italy.

B Dipartimento di Scienze del Suolo della Pianta e degli Alimenti (Di.S.S.P.A.), Università degli Studi di Bari Aldo Moro, Bari, Italy.

C Dipartimento di Scienze e Tecnologie, Università degli Studi di Napoli Parthenope, Napoli, Italy.

D Corresponding author. Email: piscitelli@iamb.it

Soil Research 57(8) 807-813 https://doi.org/10.1071/SR19075
Submitted: 2 April 2019  Accepted: 20 July 2019   Published: 2 October 2019

Abstract

Polycyclic aromatic hydrocarbons (PAHs) are a large group of compounds composed of two or more aromatic rings. They are extremely toxic pollutants largely produced by anthropogenic activities and characterised by high persistence in the environment. Soils contaminated by PAHs could be depolluted by bioremediation techniques, an effective in-situ procedure which provides the addition of exogenous substrates able to sustain and enhance the autochthonous soil microflora and the allochthon microbial inoculum. Our research aims to study the effects of biochar, produced by slow pyrolysis of olive pomace, as a bio-stimulant of soil microflora or support for the colonisation of the allochthon Trichoderma harzianum, on degradation of pyrene used here as model molecule for the PAH family. Biochar is considered an excellent soil conditioner because of its positive effect on soil physical and chemical properties and its positive interaction with soil microorganisms. Autochthonous microbial growth, T. harzianum growth and microbial pyrene-degradation activity were surveyed in soil samples spiked with 50 ppm of pyrene and incubated for up to 28 days. Pyrene concentration was reduced by ~70% in 28 days in both bioaugmentation and biostimulation tests. Olive mill pomace biochar did not interfere with pyrene bioavailability and did not affect microbial pyrene-degrading activity. The T. harzianum did not display a distinctive ability in degrading pyrene and partially inhibited the endogenous soil microflora.

Additional keywords: bioaugmentation, biostimulation, olive pomace biochar, pyrene, soil remediation.


References

Abdel-Shafy HI, Mansour MSM (2016) A review on polycyclic aromatic hydrocarbons: source, environmental impact, effect on human health and remediation. Egyptian Journal of Petroleum 25, 107–123.
A review on polycyclic aromatic hydrocarbons: source, environmental impact, effect on human health and remediation.Crossref | GoogleScholarGoogle Scholar |

Amellal N, Portal JM, Betthelin J (2001) Effect of soil structure on the bioavailability of polycyclic aromatic hydrocarbons within aggregates of a contaminated soil. Applied Geochemistry 16, 1611–1619.
Effect of soil structure on the bioavailability of polycyclic aromatic hydrocarbons within aggregates of a contaminated soil.Crossref | GoogleScholarGoogle Scholar |

Anawar HM, Akter F, Solaiman ZM, Strezov V (2015) Biochar: an emerging panacea for remediation of soil contaminants from mining, industry and sewage wastes. Pedosphere 25, 654–665.
Biochar: an emerging panacea for remediation of soil contaminants from mining, industry and sewage wastes.Crossref | GoogleScholarGoogle Scholar |

Argumedo-Delira R, Alarcon A, Ferrera-Cerrato R, Almaraz JJ, Pena-Cabriales JJ (2012) Tolerance and growth of 11 Trichoderma strains to crude oil, naphthalene, phenanthrene and benzo[a]pyrene. Journal of Environmental Management 95, S291–S299.
Tolerance and growth of 11 Trichoderma strains to crude oil, naphthalene, phenanthrene and benzo[a]pyrene.Crossref | GoogleScholarGoogle Scholar | 20869805PubMed |

Beesley L, Moreno-Jiménez E, Gomez-Eyles JL (2010) Effects of biochar and greenwaste compost amendments on mobility, bioavailability and toxicity of inorganic and organic contaminants in a multi-element polluted soil. Environmental Pollution 158, 2282–2287.
Effects of biochar and greenwaste compost amendments on mobility, bioavailability and toxicity of inorganic and organic contaminants in a multi-element polluted soil.Crossref | GoogleScholarGoogle Scholar | 20219274PubMed |

Cerqueira VS, Peralba MCR, Camargo FAO, Bento FM (2014) Comparison of bioremediation strategies for soil impacted with petrochemical oily sludge. International Biodeterioration & Biodegradation 95, 338–345.
Comparison of bioremediation strategies for soil impacted with petrochemical oily sludge.Crossref | GoogleScholarGoogle Scholar |

Czapek, F (1902) Untersuchungen über die stickstoffgewinnung und eiweifsbildung der pflanzen. In ‘Beiträge zur chemischen Physiologie und Pathologie.’ pp. 538–560. (Druck und Verlag von Friedrich Vieweg und Sohn: Braunschweig)

de la Rosa JM, Paneque M, Miller AZ, Knicker H (2014) Relating physical and chemical properties of four different biochars and their application rate to biomass production of Lolium perenne on a Calcic Cambisol during a pot experiment of 79 days. The Science of the Total Environment 499, 175–184.
Relating physical and chemical properties of four different biochars and their application rate to biomass production of Lolium perenne on a Calcic Cambisol during a pot experiment of 79 days.Crossref | GoogleScholarGoogle Scholar | 25181049PubMed |

Fernández-Luqueño F, Valenzuela-Encinas C, Marsch R, Martínez-Suárez C, Vázquez-Núñez E, Dendooven L (2011) Microbial communities to mitigate contamination of PAHs in soil—possibilities and challenges: a review. Environmental Science and Pollution Research 18, 12–30.
Microbial communities to mitigate contamination of PAHs in soil—possibilities and challenges: a review.Crossref | GoogleScholarGoogle Scholar | 20623198PubMed |

García-Delgado C, Alfaro-Barta I, Eymar E (2015) Combination of biochar amendment and myco-remediation for polycyclic aromatic hydrocarbons immobilization and biodegradation in creosote-contaminated soil. Journal of Hazardous Materials 285, 259–266.
Combination of biochar amendment and myco-remediation for polycyclic aromatic hydrocarbons immobilization and biodegradation in creosote-contaminated soil.Crossref | GoogleScholarGoogle Scholar | 25506817PubMed |

Gomez-Eyles JL, Sizmur T, Collins CD, Hodson ME (2011) Effects of biochar and the earthworm Eisenia fetida on the bioavailability of polycyclic aromatic hydrocarbons and potentially toxic elements. Environmental Pollution 159, 616–622.
Effects of biochar and the earthworm Eisenia fetida on the bioavailability of polycyclic aromatic hydrocarbons and potentially toxic elements.Crossref | GoogleScholarGoogle Scholar | 21035930PubMed |

Gong P, Guan X, Witter E (2001) A rapid method to extract ergosterol from soil by physical disruption. Applied Soil Ecology 17, 285–289.
A rapid method to extract ergosterol from soil by physical disruption.Crossref | GoogleScholarGoogle Scholar |

Graber ER, Meller Harel Y, Kolton M, Cytryn E, Silber A, Rav David D, Tsechansky L, Borenshtein M, Elad Y (2010) Biochar impact on development and productivity of pepper and tomato grown in fertigated soilless media. Plant and Soil 337, 481–496.
Biochar impact on development and productivity of pepper and tomato grown in fertigated soilless media.Crossref | GoogleScholarGoogle Scholar |

Gul S, Whalen JK, Thomas BW, Sachdeva V, Deng H (2015) Physico-chemical properties and microbial responces in biochar amended soils: mechanisms and future directions. Agriculture, Ecosystems & Environment 206, 46–59.
Physico-chemical properties and microbial responces in biochar amended soils: mechanisms and future directions.Crossref | GoogleScholarGoogle Scholar |

Hamzah D, Zain MA, Omar O, Senafi S (2012) Optimal physical and nutrient parameters for growth of Trichoderma virens UKMP-1M for heavy crude oil degradation. Sains Malaysiana 41, 71–79.

Han G, Lan J, Chen Q, Yu C, Bie S (2017) Response of soil microbial community to application of biochar in cotton soils with different continuous cropping years. Scientific Reports 7, 10184
Response of soil microbial community to application of biochar in cotton soils with different continuous cropping years.Crossref | GoogleScholarGoogle Scholar | 28860603PubMed |

Kästner M, Breuer-Jammali M, Mahro B (1997) Impact of inoculation protocols, salinity, and pH on the degradation of polycyclic aromatic hydrocarbons (PAHs) and survival of PAH-degrading bacteria introduced into soil. Applied and Environmental Microbiology 64, 359–362.

Leelavathi MS, Vani L, Reena P (2014) Antimicrobial activity of Trichoderma harzianum against bacteria and fungi. International Journal of Current Microbiology and Applied Sciences 3, 96–103.

Lehmann J, da Silva JP, Steiner C, Nehls T, Zech W, Glaser B (2003) Nutrient availability and leaching in an archaeological Anthrosol and a Ferralsol of the Central Amazon basin: fertilizer, manure and charcoal amendments. Plants and soil 249, 343–357.
Nutrient availability and leaching in an archaeological Anthrosol and a Ferralsol of the Central Amazon basin: fertilizer, manure and charcoal amendments.Crossref | GoogleScholarGoogle Scholar |

Lehmann J, Rillig MC, Thies J, Masiello CA, Hockaday WC, Crowley D (2011) Biochar effects on soil biota–a review. Soil Biology & Biochemistry 43, 1812–1836.
Biochar effects on soil biota–a review.Crossref | GoogleScholarGoogle Scholar |

Li H, Qu R, Li C, Guo W, Han X, He F, Ma Y, Xing B (2014) Selective removal of polycyclic aromatic hydrocarbons (PAHs) from soil washing effluents using biochars produced at different pyrolytic temperatures. Bioresource Technology 163, 193–198.
Selective removal of polycyclic aromatic hydrocarbons (PAHs) from soil washing effluents using biochars produced at different pyrolytic temperatures.Crossref | GoogleScholarGoogle Scholar | 24813387PubMed |

Liu L, Chen P, Sun M, Shen G, Shang G (2015) Effect of biochar amendment on PAH dissipation and indigenous degradation bacteria in contaminated soil. Journal of Soils and Sediments 15, 313–322.
Effect of biochar amendment on PAH dissipation and indigenous degradation bacteria in contaminated soil.Crossref | GoogleScholarGoogle Scholar |

Marchal G, Smith KEC, Rein A, Winding A, Wollensen de Jonge L, Trapp S, Karlson U (2013) Impact of activated carbon, biochar and compost on the desorption and mineralization of phenanthrene in soil. Environmental Pollution 181, 200–210.
Impact of activated carbon, biochar and compost on the desorption and mineralization of phenanthrene in soil.Crossref | GoogleScholarGoogle Scholar | 23871817PubMed |

Martin JP (1949) Use of acid, rose bengal and streptomycin in the plate method for estimating soil fungi. Soil Science 69, 215–232.

Moscoso F, Teijiz I, Deive FJ, Sanromán MA (2012) Efficient PAHs biodegradation by a bacterial consortium at flask and bioreactor scale. Bioresource Technology 119, 270–276.
Efficient PAHs biodegradation by a bacterial consortium at flask and bioreactor scale.Crossref | GoogleScholarGoogle Scholar | 22738812PubMed |

Mukherjee A, Lal R (2013) Biochar impacts on soil physical properties and greenhouse gas emissions. Agronomy (Basel) 3, 313–339.
Biochar impacts on soil physical properties and greenhouse gas emissions.Crossref | GoogleScholarGoogle Scholar |

Nadarajah N, Van Hamme J, Pannu J, Singh A, Ward O (2002) Enhanced transformation of polycyclic aromatic hydrocarbons using a combined Fenton’s reagent, microbial treatment and surfactant. Applied Microbiology and Biotechnology 59, 540–544.
Enhanced transformation of polycyclic aromatic hydrocarbons using a combined Fenton’s reagent, microbial treatment and surfactant.Crossref | GoogleScholarGoogle Scholar | 12172623PubMed |

Novak JM, Busscher WJ, Laird DJ, Ahmedna M, Watts DW, Niandou AS (2009) Impact of biochar amendment on fertility of a southeastern coastal plain soil. Soil Science 174, 105–112.
Impact of biochar amendment on fertility of a southeastern coastal plain soil.Crossref | GoogleScholarGoogle Scholar |

Petruzzelli L, Celi L, Cignetti A, Ajmone Marsan F (2002) Influence of soil organic matter on the leaching of polycyclic aromatic hydrocarbons in soil. Journal of Environmental Science and Health: Part B, pesticides, food contaminants, and agricultural wastes 37, 187–199.
Influence of soil organic matter on the leaching of polycyclic aromatic hydrocarbons in soil.Crossref | GoogleScholarGoogle Scholar |

Petter FA, Ferreira TA, Sinhorin AP, de Lima AB, de Morais LA, Pereira Pacheco L (2016) Sorption and desorption of diuron in Oxisol under biochar application. Bragantia 75, 487–496.
Sorption and desorption of diuron in Oxisol under biochar application.Crossref | GoogleScholarGoogle Scholar |

Rhodes AH, Carlin A, Semple KT (2008) Impact of black carbon in the extraction and mineralization of phenanthrene in soil. Environmental Science & Technology 42, 740–745.
Impact of black carbon in the extraction and mineralization of phenanthrene in soil.Crossref | GoogleScholarGoogle Scholar |

Rillig MC, Thies JE (2012) Characteristics of biochar: biological properties. In ‘Biochar for environmental management’. (Eds J Lehmann, S Joseph) pp. 117–138. (Routledge: London, UK)

Rosales E, Pérez-Paz A, Vázquez X, Pazos M, Sanromán MA (2012) Isolation of novel benzo[a]anthracene-degrading microorganisms and continuous bioremediation in an expanded-bed bioreactor. Bioprocess and Biosystems Engineering 35, 851–855.
Isolation of novel benzo[a]anthracene-degrading microorganisms and continuous bioremediation in an expanded-bed bioreactor.Crossref | GoogleScholarGoogle Scholar | 22170303PubMed |

Samsøe-Petersen L, Larsen EH, Larsen PB, Bruun P (2002) Uptake of trace elements and PAHs by fruit and vegetables from contaminated soils. Environmental Science & Technology 36, 3057–3063.
Uptake of trace elements and PAHs by fruit and vegetables from contaminated soils.Crossref | GoogleScholarGoogle Scholar |

Saraswathy A, Hallberg R (2002) Degradation of pyrene by indigenous fungi from a former gasworks site. FEMS Microbiology Letters 210, 227–232.
Degradation of pyrene by indigenous fungi from a former gasworks site.Crossref | GoogleScholarGoogle Scholar | 12044679PubMed |

Sigmund G, Poyntner C, Piñar G, Kah M, Hofmann T (2018) Influence of compost and biochar on microbial communities and the sorption/degradation of PAHs and NSO-substituted PAHs in contaminated soils. Journal of Hazardous Materials 345, 107–113.
Influence of compost and biochar on microbial communities and the sorption/degradation of PAHs and NSO-substituted PAHs in contaminated soils.Crossref | GoogleScholarGoogle Scholar | 29136576PubMed |

Spokas KA (2010) Review of the stability of biochar in soils: predictability of O:C molar ratios. Carbon Management 1, 289–303.
Review of the stability of biochar in soils: predictability of O:C molar ratios.Crossref | GoogleScholarGoogle Scholar |

Tripathi P, Singh PC, Mishra A, Chauhan PS, Dwivedi S, Bais RT, Tripathi RD (2013) Trichoderma: a potential bioremediator for environmental cleanup. Clean Technologies and Environmental Policy 15, 541–550.
Trichoderma: a potential bioremediator for environmental cleanup.Crossref | GoogleScholarGoogle Scholar |

Tyagi M, da Fonseca MMR, Carvalho CCCR (2011) Bioaugmentation and biostimulation strategies to improve the effectiveness of bioremediation processes. Biodegradation 22, 231–241.
Bioaugmentation and biostimulation strategies to improve the effectiveness of bioremediation processes.Crossref | GoogleScholarGoogle Scholar | 20680666PubMed |

Wang X, Gong ZQ, Li PJ, Zhang LH, Hu XM (2008) Degradation of pyrene and benzo(a)pyrene in contaminated soil by immobilized fungi. Environmental Engineering Science 25, 677–684.
Degradation of pyrene and benzo(a)pyrene in contaminated soil by immobilized fungi.Crossref | GoogleScholarGoogle Scholar |

Weete JD (1989) Structure and function of sterols in fungi. Advances in Lipid Research 23, 115–167.
Structure and function of sterols in fungi.Crossref | GoogleScholarGoogle Scholar |

Wei R, Ni J, Guo L, Yang L, Yang Y (2014) The effect of aging time on the distribution of pyrene in soil particle-size fractions. Geoderma 232–234, 19–23.
The effect of aging time on the distribution of pyrene in soil particle-size fractions.Crossref | GoogleScholarGoogle Scholar |

Wu M, Dick WA, Li W, Wang X, Yang Q, Wang T, Xu L, Zhang M, Chen L (2016) Bioaugmentation and biostimulation of hydrocarbon degradation and the microbial community in a petroleum-contaminated soil. International Biodeterioration & Biodegradation 107, 158–164.
Bioaugmentation and biostimulation of hydrocarbon degradation and the microbial community in a petroleum-contaminated soil.Crossref | GoogleScholarGoogle Scholar |

Wu M, Li W, Dick WA, Ye X, Chen K, Kost D, Chen L (2017) Bioremediation of hydrocarbon degradation in a petroleum-contaminated soil and microbial population and activity determination. Chemosphere 169, 124–130.
Bioremediation of hydrocarbon degradation in a petroleum-contaminated soil and microbial population and activity determination.Crossref | GoogleScholarGoogle Scholar | 27870933PubMed |

Zafra G, Moreno-Montano A, Absalon AE, Cortes-Espinosa DV (2015) Degradation of polycyclic aromatic hydrocarbons in soil by a tolerant strain of Trichoderma asperellum. Environmental Science and Pollution Research 22, 1034–1042.
Degradation of polycyclic aromatic hydrocarbons in soil by a tolerant strain of Trichoderma asperellum.Crossref | GoogleScholarGoogle Scholar | 25106516PubMed |

Zhang Q, Dijkstra FA, Liu X, Wang Y, Huang J, Lu N (2014) Effects of biochar on soil microbial biomass after four years of consecutive application in the North China Plain. PLoS One 9, 1–8.
Effects of biochar on soil microbial biomass after four years of consecutive application in the North China Plain.Crossref | GoogleScholarGoogle Scholar |