Phytoremediation of pyrene-contaminated soils: A critical review of the key factors affecting the fate of pyrene

https://doi.org/10.1016/j.jenvman.2021.112805Get rights and content

Highlights

  • The main parameters affecting pyrene removal through phytoremediation are reviewed.

  • Soil organic matter and pyrene bioavailability strongly govern pyrene fate in soils.

  • Higher aging times reduce pyrene bioavailability and hinder pyrene biodegradation.

  • Multiple plant species result in a higher number of pyrene degraders in rhizosphere.

  • Additives can affect pyrene uptake by plants as well as biodegradation.

Abstract

Soil contamination by pyrene has increased over the years due to human-related activities, urgently demanding for remediation approaches to ensure human and environment safety. Within this frame, phytoremediation has been successfully applied over the years due to its green and cost-effectiveness features. The scope of this review includes the main phytoremediation mechanisms correlated with the removal of pyrene from contaminated soils and sediments to highlight the impact of different parameters and the supplement of additives on the efficiency of the treatment. Soil organic matter (SOM), plant species, aging time, environmental parameters (pH, soil oxygenation, and temperature) and bioavailability are among the main parameters affecting pyrene removal through phytoremediation. Phytoextraction only accounts for a small part of the entire phytoremediation process, but the addition of surfactants and chelating agents in planted soils could increase pyrene accumulation in plant tissues by 20% as a consequence of the increased pyrene bioavailability. Rhizodegradation is the main phytoremediation mechanism involved due to the activity of bacteria capable of degrading pyrene in the root area. Inoculated-planted soil treatments have the potential to decrease pyrene accumulation in shoots and roots by approximately 30 and 40%, respectively, further stimulating the proliferation of pyrene-degrading bacteria in the rhizosphere. Plant-fungi symbiotic association results in an enhanced accumulation of pyrene in shoots and roots of plants as well as a higher biodegradation. Finally, pyrene removal from soil can be improved in the presence of amendments, such as natural non-ionic surfactants, biochar, and bacterial mixtures.

Introduction

Polycyclic aromatic hydrocarbons (PAHs) are widespread as the result of human-related and natural activities, having both pyrogenic (combustion) or petrogenic (originating from petroleum) origins (Hamid et al., 2018). Gas expelled from volcanoes and wildfires represent the main natural sources of PAHs, while fossil fuel combustion in vehicles, coking plants and industrial productive activities are the anthropogenic sources that mostly increase the quantity of PAHs in the environmental matrices. PAHs can be additionally formed during the slow transformation of complex organic molecules in soil (Cachada et al., 2016), or during industrial thermal processes and, as a consequence, petroleum, natural gas, and bio-gas are rich in these compounds (Hu et al., 2020).

PAHs belong to the group of persistent organics pollutants (POPs) and consist of two or more fused aromatic rings organized in a linear, angular or a cluster structure. In general, low-molecular-weight PAHs with less than 4 rings are easier to degrade than high-molecular-weight PAHs, which are particularly recalcitrant to chemical and biological degradation (Bianco et al., 2020; Gupta et al., 2020b; Sun et al., 2010). Humans can be exposed to PAHs contamination through different ways such as ingestion, inhalation, or skin adsorption, with the ingestion of contaminated food being the predominant path of exposure (Polachova et al., 2020). Although more than a hundred PAHs exists, the United States Environmental Protection Agency (USEPA) listed sixteen compounds of priority concern, based upon their toxicity, easier exposure, and persistency in the contaminated sites (USEPA, 1993). In the last decades, this list of the 16 PAHs has played a significant role mainly for environmental science and policy issues, but questions are recently opened on the update of the environmental regulatory system based on recent toxicology studies, possibly extending the classification to additional PAHs in the future (Andersson and Achten, 2015; Keith, 2015).

Among PAHs, pyrene (4 fused rings) has gained attention as a result of its high toxicity, mutability, ubiquitous presence in all environmental matrices, high persistence and recalcitrance to biodegradation (IARC Working Group on the Evaluation of Carcinogenic Risks to Humans, 2010). Particularly related to the subject of this article, recent research has shown a negative influence of pyrene on plant life cycle in function of the global increased temperature, posing the problem of a possible future aggravation of the risk caused by pyrene in the environment due to climate change (Zhang et al., 2018). Pyrene is repeatedly found in lands intended for agriculture as the predominant PAH due to the industrial practices described above, urgently demanding for the implementation of remediation technologies (Lu et al., 2019; Yakovleva et al., 2020). The success of these technologies is intimately correlated to some factors (e.g. pH, site temperature, bioavailability), thus knowing the environmental behavior of pyrene is crucial to assess the efficiency and select the most suited remediation technique. Apart from the pyrene concentration in soil and the additional variables cited above, the environmental and ecotoxicological properties of pyrene strongly depend on the content of natural organic matter in soil (Cachada et al., 2016). Indeed, hydrophobicity and bioaccumulating characteristics make pyrene highly prone to be adsorbed onto suspended particulates and biota, and accumulated in soil and sediments (Dong et al., 2010; Umeh et al., 2020).

Despite the existence of different thermal and chemical methods to remediate pyrene-polluted soils, such as incineration, solvent extraction and oxidation by chemical agents, green biological technologies offer several advantages (Sakshi et al., 2019). For instance, phytoremediation has been successfully applied due to its cost-effectiveness, the possibility to remediate pollutants from different environmental compartments (Truu et al., 2015) and the eco-friendly interaction with the surrounding environment (Lama et al., 2020). Although phytoremediation is a consolidate technology, current knowledge needs a review that includes a critical approach about the emerging phytoremediation results for the removal of pyrene from contaminated sites (Bao et al., 2018; Kim et al., 2019) and the main mechanisms occurring between the contaminant and the plant. Also, the use of soil amendments requires an in-depth analysis as a strategy to enhance the phytoremediation of pyrene-contaminated sites in terms of both removal percentage and rate. Hence, this study aims to provide a guidance for future research on pyrene removal from soils through phytoremediation and to boost the development of new methods capable to improve the efficiency of the process.

Section snippets

Pyrene: properties, distribution, and removal

Pyrene, C16H10, is composed of 4 fused rings assembled in a flat aromatic structure (IUPAC, 1998). Pyrene belongs to group 4 in the classification for carcinogenicity provided by International Agency Research on Cancer (IARC), meaning that the agent (mixture or circumstances) does not show evidence for carcinogenic induced effects to humans. In contrast, studies report that pyrene can meet transformation processes and be transformed into more hazardous compounds such as benzo(a)pyrene, which

Phytoremediation of pyrene contaminated soils

Phytoremediation offers different advantages against the conventional physico-chemical methods, as the latter may cause serious chemical modification of the site and interference with ongoing activities (Vasavi et al., 2010). Overall, the most considerable advantages of phytoremediation deal with the possibility to concomitantly remove different contaminants, the non-interference with the ecosystem and the site, and the low operating costs. Indeed, the estimated costs for phytoremediation are

Pyrene bioavailability

During phytoremediation of pyrene-contaminated soils, bioavailability of pyrene is an essential key factor to consider as it represents the relevant exposure dose available for degradation by living organisms (Fernández-López et al., 2020), but also a possible toxicity exposure for plants and associated microorganisms in soil (Ortega-Calvo et al., 2015). The accessible quantity of pyrene for biodegradation is the portion available to cross the cellular membrane of organisms (Wei et al., 2017)

Additives used to strengthen phytoremediation of pyrene-contaminated soils

The performance of phytoremediation of pyrene-contaminated soils can be improved by adding compounds (e.g. nutrients, chelating agents, bacterial growth stimulators) or seeding rhizospheric and endophytic bacteria to soil (Salehi et al., 2020; Zhang et al., 2017). As illustrated in Fig. 3, the aim is to improve the quality of the soil treated by increasing the bioaccessibility of the contaminant, the biomass growth and the biological degradation, thus the success of the treatment (Kumar et al.,

Conclusions and potential future investigations

Phytoremediation is an effective, sustainable, and reliable technique for the remediation of pyrene-contaminated soils, involving only simple equipment, resulting in low operating costs, and having no-interference with the ecosystem. The present review pointed out that pyrene is mostly removed through rhizodegradation (i.e. the action of microorganisms in the rhizosphere region), significantly promoted by the specific plant species involved. The phytoremediation efficiency strongly depends on

Credit author statement

Ilaria Gabriele: Conceptualization, Data curation, Investigation, Writing – original draft, Writing – review & editing. Marco Race: Conceptualization, Supervision, Writing – review & editing. Stefano Papirio: Conceptualization, Supervision, Writing – review & editing. Giovanni Esposito: Supervision, Writing – review & editing, Administration, Funding acquisition.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

References (225)

  • Y. Abbas et al.

    Remediation of pyrene contaminated soil by double dielectric barrier discharge plasma technology: performance optimization and evaluation

    Environ. Pollut.

    (2020)
  • I.K.U. Adam et al.

    Microbial communities in pyrene amended soil–compost mixture and fertilized soil

  • P. Agarwal et al.

    Unravelling the role of rhizospheric plant-microbe synergy in phytoremediation: a genomic perspective

    Curr. Genom.

    (2020)
  • A.C. Agnello et al.

    Citric acid- and Tween® 80-assisted phytoremediation of a co-contaminated soil: alfalfa (Medicago sativa L.) performance and remediation potential

    Environ. Sci. Pollut. Control Ser.

    (2016)
  • S. Ahn et al.

    Physicochemical characterization of coke-plant soil for the assessment of polycyclic aromatic hydrocarbon availability and the feasibility of phytoremediation

    Environmental Toxicology and Chemistry

    (2005)
  • N.H. AL Sbani et al.

    PAH-degrading rhizobacteria of Lepironia articulata for phytoremediation enhancement

    Journal of Water Process Engineering

    (2020)
  • S. Alagić et al.

    How can plants manage polycyclic aromatic hydrocarbons? May these effects represent a useful tool for an effective soil remediation?

    A Review. Clean Technologies And Environmental Policy

    (2015)
  • M. Alexander

    Aging, bioavailability, and overestimation of risk from environmental pollutants

    Environmental Science and Technology

    (2000)
  • X. An et al.

    Research progress on aging of organic pollutants in geosorbents: a review

    Acta Geochimica

    (2017)
  • J.T. Andersson et al.

    Time to say goodbye to the 16 EPA PAHs? Toward an up-to-date use of PACs for environmental purposes

    (2015)
  • A. Balasubramaniyam

    The influence of plants in the remediation of petroleum hydrocarbon- contaminated sites

    Pharmaceutical Analytical Chemistry: Open Access

    (2015)
  • M.M. Baneshi et al.

    Effect of bioaugmentation to enhance phytoremediation for removal of phenanthrene and pyrene from soil with Sorghum and Onobrychis sativa

    Journal of Environmental Health Science and Engineering

    (2014)
  • K. Banger et al.

    Polycyclic aromatic hydrocarbons in urban soils of different land uses in Miami, Florida

    Soil and Sediment Contamination

    (2010)
  • H. Bao et al.

    Status, sources, and risk assessment of polycyclic aromatic hydrocarbons in urban soils of Xi’an, China

    Environmental Science and Pollution Research

    (2018)
  • P. Bardos et al.

    Status of Nanoremediation and its Potential for Future Deployment: Risk-Benefit and Benchmarking Appraisals

    (2018)
  • F. Bianco et al.

    Removal of polycyclic aromatic hydrocarbons during anaerobic biostimulation of marine sediments

    Sci. Total Environ.

    (2020)
  • Francesco Bianco et al.

    Comparing performances, costs and energy balance of ex situ remediation processes for PAH-contaminated marine sediments

    Environ. Sci. Pollut. Control Ser.

    (2020)
  • Francesco Bianco et al.

    The addition of biochar as a sustainable strategy for the remediation of PAH–contaminated sediments

    Chemosphere

    (2021)
  • N.S. Bolan et al.

    Phytostabilization. A green approach to contaminant containment

    Advances in Agronomy

    (2011)
  • A. Cachada et al.

    Risk assessment of urban soils contamination: the particular case of polycyclic aromatic hydrocarbons

    Science of the Total Environment

    (2016)
  • M.C. Chang et al.

    Remediation of pyrene-contaminated soil by synthesized nanoscale zero-valent iron particles

    Journal of Environmental Science and Health - Part A Toxic/Hazardous Substances and Environmental Engineering

    (2009)
  • S.A. Cheema et al.

    Degradation of phenanthrene and pyrene in spiked soils by single and combined plants cultivation

    J. Hazard Mater.

    (2010)
  • S.A. Cheema et al.

    Surfactant enhanced pyrene degradation in the rhizosphere of tall fescue (Festuca arundinacea)

    Environmental Science and Pollution Research

    (2016)
  • S.A. Cheema et al.

    Enhancement of phenanthrene and pyrene degradation in rhizosphere of tall fescue (Festuca arundinacea)

    J. Hazard Mater.

    (2009)
  • B. Chefetz et al.

    Pyrene sorption by natural organic matter

    (2000)
  • T. Chekol et al.

    Assessing the potential of using phytoremediation for pyrene-contaminated soils

  • T. Chekol et al.

    Plant-soil-contaminant specificity affects phytoremediation of organic contaminants

    Int. J. Phytoremediation

    (2002)
  • T. Chen et al.

    Effect of alkyl polyglucoside and nitrilotriacetic acid combined application on lead/pyrene bioavailability and dehydrogenase activity in co-contaminated soils

    Chemosphere

    (2016)
  • T. Chen et al.

    Enhanced Scirpus triqueter phytoremediation of pyrene and lead co-contaminated soil with alkyl polyglucoside and nitrilotriacetic acid combined application

    J. Soils Sediments

    (2016)
  • X. Chen et al.

    Past, present, and future perspectives on the assessment of bioavailability/bioaccessibility of polycyclic aromatic hydrocarbons: a 20-year systemic review based on scientific econometrics

    (2021)
  • K.Y. Cheng et al.

    Effects of pig manure compost and nonionic-surfactant Tween 80 on phenanthrene and pyrene removal from soil vegetated with Agropyron elongatum

    Chemosphere

    (2008)
  • C. Chigbo et al.

    Phytoremediation potential of Brassica juncea in Cu-pyrene co-contaminated soil: comparing freshly spiked soil with aged soil

    J. Environ. Manag.

    (2013)
  • C. Chigbo et al.

    Chelate-assisted phytoremediation of Cu-pyrene-contaminated soil using Z. mays. Water

    Air, and Soil Pollution

    (2015)
  • C. Chigbo et al.

    Interactions of copper and pyrene on phytoremediation potential of Brassica juncea in copper-pyrene co-contaminated soil

    Chemosphere

    (2013)
  • M.K. Chung et al.

    Pollutants in Hong Kong soils: polycyclic aromatic hydrocarbons

    Chemosphere

    (2007)
  • A. Cristaldi et al.

    Phytoremediation of contaminated soils by heavy metals and PAHs. A brief review

    Environmental Technology and Innovation

    (2017)
  • A. Cruz-Hernández et al.

    Inoculation of seed-borne fungus in the rhizosphere of Festuca arundinacea promotes hydrocarbon removal and pyrene accumulation in roots

    Plant and Soil

    (2013)
  • V. D'Orazio et al.

    Phytoremediation of pyrene contaminated soils by different plant species

    Air, Water

    (2013)
  • Y. Dai et al.

    Fire Phoenix facilitates phytoremediation of PAH-Cd co-contaminated soil through promotion of beneficial rhizosphere bacterial communities

    Environ. Int.

    (2020)
  • L.R.P. de Andrade Lima et al.

    Remediation of Clay Soils Contaminated with Potentially Toxic Elements: the Santo Amaro Lead Smelter, Brazil, Case. Soil And Sediment Contamination

    (2018)
  • P. Dhanwal et al.

    Recent advances in phytoremediation technology

    Advances in Environmental Biotechnology

    (2017)
  • P.N. Diagboya et al.

    Assessment of the effects of soil organic matter and iron oxides on the individual sorption of two polycyclic aromatic hydrocarbons

    Environmental Earth Sciences

    (2021)
  • D. Dong et al.

    Investigation on the photocatalytic degradation of pyrene on soil surfaces using nanometer anatase TiO2 under UV irradiation

    J. Hazard Mater.

    (2010)
  • A. Esmaeili et al.

    Advancing prediction of polycyclic aromatic hydrocarbon bioaccumulation in plants for historically contaminated soils using Lolium multiflorum and simple chemical in-vitro methodologies

    Science of the Total Environment

    (2021)
  • S. Fan et al.

    Promotion of pyrene degradation in rhizosphere of alfalfa (Medicago sativa L.)

    Chemosphere

    (2008)
  • H. Farraji et al.

    Advantages and disadvantages of phytoremediation: a concise review

    Int J Env Tech Sci

    (2016)
  • C. Fernández-López et al.

    Root-mediated bacterial accessibility and cometabolism of pyrene in soil

    Science of the Total Environment

    (2020)
  • N. Fiorentino et al.

    Assisted phytoremediation for restoring soil fertility in contaminated and degraded land

    (2018)
  • Y.-Z. Gao et al.

    Surfactant-Enhanced Phytoremediation of Soils Contaminated with Hydrophobic Organic Contaminants: Potential and Assessment. Pedosphere

    (2007)
  • Y. Gao et al.

    Uptake pathways of polycyclic aromatic hydrocarbons in white clover

    Environmental Science and Technology

    (2009)
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