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

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

Environmental Technology & Innovation 8 (2017) 309–326 Contents lists available at ScienceDirect Environmental Technology & Innovation journal homep...

2MB Sizes 0 Downloads 49 Views

Environmental Technology & Innovation 8 (2017) 309–326

Contents lists available at ScienceDirect

Environmental Technology & Innovation journal homepage: www.elsevier.com/locate/eti

Phytoremediation of contaminated soils by heavy metals and PAHs. A brief review Antonio Cristaldi a,b, *, Gea Oliveri Conti a , Eun Hea Jho c , Pietro Zuccarello a,b , Alfina Grasso a , Chiara Copat a , Margherita Ferrante a a

Department of Medical, Surgical and Advanced Technologies ‘‘G.F. Ingrassia’’, University of Catania, Via Santa Sofia 87, 95123, Catania, Italy b Department of Biological, Geological and Environmental Sciences, University of Catania, Corso Italia 57, 95129, Catania, Italy c Department of Environmental Science, Hankuk University of Foreign Studies Yongin-si, Gyeonggi-do, Republic of Korea

highlights

graphical abstract

• Our article we highlighted the various phytoremediation techniques to be applied for the soils remediation by heavy metals and polycyclic aromatic hydrocarbons pollution. • Manuscript synthesize the worldwide application available techniques of phytoremediation. • This review provides additional information about the application of phytoremediation processes.

article

info

Article history: Received 3 February 2017 Received in revised form 15 July 2017 Accepted 3 August 2017 Available online 15 August 2017 Keywords: Phytoremediation Soil contamination Heavy metals

*

a b s t r a c t Acute and diffuse contamination of soil by organic and inorganic pollutants causes wide concerns and intentional or accidental introduction of these substances poses serious impact in public health and environment. Heavy metals are elements not degradable and can be teratogenic, mutagenic, endocrine disruptors. PAHs are elements of difficult management and they can cause carcinogenesis and toxicity in human. Different techniques have been used for the remediation of contaminated soils, but the phytoremediation is proposed as possible alternative, convenient and environmentally friendly than traditional physicochemical techniques. Phytoremediation employs different plant species able to accumulate or degrade different contaminants and, the biomass produced can

Corresponding author at: Department of Medical, Surgical and Advanced Technologies ‘‘G.F. Ingrassia’’, University of Catania, Via Santa Sofia 87, 95123, Catania, Italy. E-mail address: [email protected] (A. Cristaldi). http://dx.doi.org/10.1016/j.eti.2017.08.002 2352-1864/© 2017 Elsevier B.V. All rights reserved.

310

A. Cristaldi et al. / Environmental Technology & Innovation 8 (2017) 309–326

PAHs Public health

be used for other purposes such as cogeneration of energy and/or biofuels production, obtaining benefits to health, environment and cost management. A better knowledge of phytoremediation potential is essential in order to increase the use of this technique in the near future for remediation of contaminated lands in the economic and sustainable way. This review provides additional information about the application of phytoremediation processes in soils contaminated by heavy metals and polycyclic aromatic hydrocarbons using herbaceous and woody plants. © 2017 Elsevier B.V. All rights reserved.

Contents 1. 2.

3.

4. 5.

Introduction............................................................................................................................................................................................. Soil contamination .................................................................................................................................................................................. 2.1. Soil contamination by heavy metals ......................................................................................................................................... 2.2. Soil contamination by PAHs ...................................................................................................................................................... Bioremediation........................................................................................................................................................................................ 3.1. Phytoremediation....................................................................................................................................................................... 3.1.1. Phytoextraction........................................................................................................................................................... 3.1.2. Phytostabilization ....................................................................................................................................................... 3.1.3. Phytovolatilization...................................................................................................................................................... 3.1.4. Phytodegradation ....................................................................................................................................................... 3.1.5. Rhizofiltration ............................................................................................................................................................. 3.1.6. Rhizodegradation........................................................................................................................................................ 3.1.7. Phytodesalination ....................................................................................................................................................... Plants used in phytoremediation and their biochemical processes .................................................................................................... Conclusions and future perspectives ..................................................................................................................................................... Acknowledgment .................................................................................................................................................................................... Conflict of interests ................................................................................................................................................................................. References ............................................................................................................................................................................................... Sitography ...............................................................................................................................................................................................

310 311 311 312 313 313 314 315 318 319 320 320 321 321 322 323 323 323 326

1. Introduction Excessive or improper use of synthetic chemical compounds have caused serious environmental issues and increased of several adverse effects on human health (toxicity and carcinogenicity). Various anthropogenic activities have negatively affected environmental matrices (air, water, soil, biota) by releasing solid, liquid and gaseous wastes, containing several pollutants such as heavy metals, hydrocarbons, organic solvents (Sciacca and Oliveri Conti, 2009; Miri et al., 2016). Direct input of contaminants and/or transfer of the contaminants present in other matrices has led to soil contamination (Shayler et al., 2009). Contamination of environmental matrices is an important public health problem. In fact, human can be exposed to numerous environmental contaminants through different routes of exposure: inhalation of particulate matter, ingestion, direct contact, ingestion through food chain (Dadar et al., 2016; Conte et al., 2016). It is possible to safeguard the public health through the recovery of contaminated sites, which can also be reused for various future activities. Furthermore, the ecologically sustainable remediation techniques involve a substantial reduction of waste volumes produced using physicochemical methods such as soil incineration or excavation and transfer to the landfill. These techniques have other disadvantages: high cost of remediation, possible pollution caused by the release of substances used in remediation processes. Then, eco-friendly biological methods are taken into consideration for soil remediation (Alì et al., 2013). Bioremediation is defined as the process whereby the pollutants are biologically removed or degraded under controlled conditions to an innocuous state, or to levels below concentration limits established by regulatory authorities (Kumar et al., 2011). Phytoremediation is an applicable technique to several reclaiming treatment, because it does not interfere with the ecosystem, it requires little manpower and therefore is not very expensive compared to traditional physicochemical methods. Advances in this sector have been significant in recent years thanks to the use of modern biotechnology as phytoextraction and phytodegradation (Rajakaruna et al., 2006; Souza et al., 2014). Phytoremediation techniques could be applied for the recovery of the industrial sites heavily contaminated. In Italy, for example, have been identified some highly contaminated areas, defined as Sites of National Interest (SIN) that are located near industrial centers and they were classified by the Italian law as high risk sites (Legislative Decree 22/97; Ministerial Decree 471/99; Legislative Decree 152/2006 and subsequent amendments). Currently, 39 SIN are been identified. The SIN must be reclaimed to avoid environmental damage and public health problems. Other examples of soil recovery were Chernobyl in Ukraine (Vinichuk et al., 2013), where sunflowers were used for the recovery of contaminated soil from radioactive material (137 Cesium) and the same was done in Fukushima, Japan, after the accident at the nuclear power plant (Sugiura et al., 2016); in Spain, where native plant species have been used for phytoremediation processes applied to mining waste (Fernandez et al., 2017).

A. Cristaldi et al. / Environmental Technology & Innovation 8 (2017) 309–326

311

Considering the need to increase knowledge about sustainable techniques for the remediation of contaminated soils through biological organisms as plants, because they can absorb and/or degrade inorganic and organic contaminants respectively, in this review we described the possible techniques of phytoremediation to be applied in contaminated soils by heavy metals and polycyclic aromatic hydrocarbons (PAHs), considering the advantages, disadvantages and possible applications, because heavy metals are not degradable and consequently persistent in the environment, while polycyclic aromatic hydrocarbons are difficult to manage (Copat et al., 2012; Das et al., 2014; Conte et al., 2016). 2. Soil contamination Soil acts as a final acceptor of substances that are released into the environment from various human activities. Inorganic and organic contaminants may accumulate in the soil because of their physicochemical properties (Shayler et al., 2009) and they pose a serious problems concerning public and environmental health. These substances affect the chemical, physical and biological equilibrium of the soil and they can enter in the food chain, so as to get to humans through the process of bioaccumulation and biomagnification. When the concentration of pollutants is above a defined legal standard value, water, air and soil are described as contaminated (Horta et al., 2015). Then, environmental remediation becomes fundamental in order to ensure a better health for the population and a better preservation of environment for future generations (Conceição Gomes et al., 2016). Soil, as well as air and water, may contain both natural or anthropogenic contaminants with a wide range of compositions and concentrations. The pollution caused by inorganic and organic compounds is due both to the natural pollution releases and to the not well managed human activities (Kavamura and Esposito, 2010) that representing a great problem for soil reuse. 2.1. Soil contamination by heavy metals Contaminated soils have different inorganic substances that can alter their natural balance and the heavy metals are the most represented. There is no universally accepted definition of heavy metals based on the physicochemical properties, but they are so defined if they have characteristics like ductility, conductivity, ligand specificity, and an atomic number >20 (Lasat, 2000; Duffus, 2003; Copat et al., 2012). Metals are natural constituents of the soil, but their presence has exponentially grown since the beginning of the industrial revolution (Kabata-Pendias, 1989; Chaney et al., 1997; Kos et al., 2003; Jing et al., 2007). Heavy metals are naturally occurring throughout the earth’s crust, but several heavy metals, such as Cadmium (Cd), Chromium (Cr), Copper (Cu), Mercury (Hg), Lead (Pb), Nickel (Ni), Zinc (Zn), and the metalloid Arsenic (As), are widely used by industries, agriculture and consequently released into the environment (Tchounwou et al., 2014). Wastewater from tanneries, for example, transporting various malodorous chemical substances containing hydrogen sulfide, ammonia, and chromium, widely used in the tanning industry (Chauhan et al., 2015). Several metals are released into the environment also by the petrochemical industry and vehicular traffic. Manno et al. (2006), have evaluated the influence of petrochemical and vehicular traffic on the city of Gela, Italy; they have collected eight samples of road dust for three different points (industrial, urban, peripheral) of the city and characterized their chemical composition. A comparison was made between the concentration of trace metals in road dusts and those in main local outcropping rocks; road dust samples contained nonsoil-derived elements. Traffic appears to be responsible for the high levels of Cu, Mo, Pb, Sb and Zn, and the petrochemical plant for the high concentrations of Ni, V, Ba and Cr. The heavy metals present in soil, as reported by Lasat (2000), can be found in different forms: (1) as free metal ions; (2) as a soluble metal complexes; (3) associated to soil organic matter; (4) as oxides, hydroxides, and carbonates; (5) incorporated into silicate minerals structure. To apply phytoremediation techniques, contaminants must be bioavailable and ready to be absorbed by roots. Bioavailability depends from solubility of the metals in soil. Heavy metals in soil, like Cd, Zn, Pb, Ni, Cu, cause diseases in human and animals, and have shown phytotoxic problems for sensible plants (Lasat, 2000). Cadmium in the soil spreads through both natural and anthropogenic sources. It is present dissolved in water or insoluble complexes with inorganic and organic compounds (Crea et al., 2013; Tchounwou et al., 2014). Zinc is naturally present in soil, but higher concentrations are due to anthropogenic sources. Zinc mobility in soil depends by the properties of the soil as pH, cations exchange and others chemical elements (Broadley et al., 2007). Lead is a naturally element present in the lithosphere, but it has many different industrial, agricultural and domestic applications. Lead exerts a toxic effect on all organisms. Compared to other pollutants it has high persistence in the soil due to the low solubility with several risks for humans and for this reason was banned in gasoline formulation. (Hernberg, 2000). Nickel is a component widely distributed in soil and sea water. Nickel has been used in different industrial and technological applications, so it has shown an increase of its concentration Nickel is retained by the soil due to: texture of soil, organic matter presence, quality and quantity of mineral crystals, pH, water and hydroxides presence (ATSDR, 2005). Copper is an element widely occurring in nature, especially in soil and water. It is a metal highly used in anthropogenic activities. After its input in environmental matrices, copper binds like, cupric ion (Cu2+ ) with inorganic and organic

312

A. Cristaldi et al. / Environmental Technology & Innovation 8 (2017) 309–326

compounds in soil and sediments, and this reaction is influenced by pH values, redox potential and presence of anions (Van Sprang et al., 2008). Arsenic is a metalloid usually comprised between heavy metals and it is a ubiquitous element naturally present in the earth’s crust, oceans, lakes and rivers (Tchounwou et al., 2014). Environmental pollution by arsenic occurs as a result of natural phenomena and anthropogenic activities (Tchounwou et al., 2014). Toxicity, bioavailability and transport of As is dependent by its ionic forms: (As3+ and As5+ are the most dangerous forms) (Cullen and Reimer, 1989). Vanadium is a metal naturally present in the soil and it is present in different oxidation states: +2, +3, +4, +5. Pentavalent form is the most dangerous for its higher absorbing capacity in organism exposed (Kabata-Pendias, 2001). The major emissions of vanadium in environment are due to anthropogenic activities. Chromium is relatively abundant in Earth’s crust, rivers, lakes and marine waters. Chromium shows three oxidation states (+2, +3, +6) but the trivalent (very common in nature) and hexavalent are the most stable forms and are of greatest industrial interest (Sreeram and Ramasami, 2003). Industrial emissions are responsible of chromium increase in soil and waters (Kabata-Pendias, 2001). Mercury existing in three forms (elemental, inorganic, and organic); as Hg2+ is available in soil as organic and inorganic complex and it is liquid at room temperature (Tchounwou et al., 2014). It is quite widespread in nature and is released into the environment through the volcanic exhalations or thermal springs. Main anthropogenic sources are due to the activity of extraction of copper and zinc, the burning of fossil fuels and wastes in various industrial processes, but also to the use of fertilizers in agriculture, fungicides, sewage and sewage sludge which have increased the presence of this metal in soil (Pacyna et al., 2006). Methylated mercury forms are very dangerous for humans because through the biomagnification they can enter in the food chain (Copat et al., 2012). 2.2. Soil contamination by PAHs Organic pollutants are introduced in soil through industrial discharges and some agricultural traditions and improper practices for waste disposal. Persistence of these chemicals in soil is a threat for the human health and wildlife (Winquist et al., 2013). PAHs are a large group of semi-volatile organic compounds consist of carbon and hydrogen atoms, arranged to form structurally two or more benzene rings (Miani et al., 2007; Marquès et al., 2016). They may also include other elements, such as nitrogen, chlorine, oxygen and sulfur, forming the so-called aromatic heterocyclic compounds. PAHs are ubiquitous contaminants in all environmental compartments. Their presence is due to natural sources such as coal, oil, volcanic eruptions, and to human activities related to industrial processes, vehicular traffic, domestic heating (Venkata Mohan et al., 2006). It is estimated that in the last 100 years, their concentration in all biosphere environmental media (water, air, soil) is increasing (Jones et al., 1989), and this increase is mainly due to anthropogenic activities. Hydrophobic nature of the PAHs is the main factor that determines their persistence in environment and PAHs can be accumulate in the food chain (Mollea et al., 2005). The International Agency for Research on Cancer (IARC) declared some PAHs as probable or possible human carcinogens in 1987 (IARC, 1987). The risk for living organisms is associated with their toxicity, mutagenicity, teratogenicity and carcinogenicity (Roy et al., 2005). Although PAHs are subject to photosensitization and photodegradation, they are considered of persistent contaminants in the environment due to their physicochemical characteristics. Furthermore, the compounds are resistant to microbial degradation due to the low solubility in water and their complex structure, but despite this, there are some bacteria able to degrade them, obtaining carbon and energy for their growth. Generally, a group of bacteria both gram-positive and gram-negative are able to degrade PAHs thanks to the intervention of intracellular enzymes: the gram-negative bacterium Burkholderia (β -proteobacteria) is able to easily degrade PAHs having 2 or 3 aromatic rings; the gram-positive bacterium Mycobacterium is more efficient in degrading PAHs with a greater number of aromatic rings (Winquist et al., 2013). Other microorganisms able to perform these degradative processes are the ligninolytic fungi, which can also to be more effective than some bacteria, because this fungi possess special enzymes (lignin peroxidase, manganese peroxidase, laccase) which have an important role in the initial attack towards PAHs with a high molecular weight present in the soil. Jang et al. (2009), have showed that Trametes versicolor strains are able to degrade PAHs present in soil thanks to the combined action of three enzymes above mentioned. Cordyceps militaris, is a parasitic fungus capable of degrading PAHs through hydroxylation. It showed high degradation activity towards phenanthrene, pyrene and benzo(a)pyrene (Mori et al., 2015). The level and the rate of biodegradation of PAHs by fungal enzymes depends on several factors: oxygen, accessibility of nutrients, pH, temperature, chemical structure of the compound, cell transport properties and chemical breakdown in the soil (Kadri et al., 2015). Today, different strategies are evaluated for bioremediation of soils contaminated by PAHs, like the correction with various types of compost and bio-augmentation using various fungal species. The scientific community supports the bioremediation processes, not only through the use of bacteria, but also through the use of fungal organisms because they possess the ability to degrade PAHs (Winquist et al., 2013). Fungi represent an effective choice for degradation of PAHs because they have an important advantages compared to the bacteria like the ability to grow on a wide spectrum of substrates and the production of extracellular hydrolytic enzymes that may penetrate in the polluted soil and remove hydrocarbons (Kadri et al., 2015).

A. Cristaldi et al. / Environmental Technology & Innovation 8 (2017) 309–326

313

Table 1 Bioremediation methods (modified by Kavamura and Esposito, 2010). Methods

Principles

References

Natural attenuation

Natural presence in the soil of indigenous microorganisms able to degrading and lowering the organic and inorganic contaminants. Addition of non-indigenous microorganisms able to degrade the contaminants resistant to the action of the indigenous microbiota. Addition of nutrients promoting the growth and development of indigenous micro-organisms to increase their metabolic activity and so elevate the degradation of the contaminants. Use of specific microorganisms inoculum able to promote the solubilization of the metals by soil. Application of bacteria in bio-filters used for the decontamination of polluted water and sludge by wastewaters or landfills. The material to be processed is accumulated over an aerated system with addition of nutrients. Adsorption of metals and some ions present in an aqueous solution of polluted soil by the use of biological materials as ion-exchange resins. System that combines the ventilation of the polluted soil to remove the volatile compounds and, oxidative degradation of organic contaminants. Addition of nutrients to the polluted soil, with forced aeration for the activation of autochthonous microorganisms. Use of plantsable to extract, sequestrate or detoxify land or aquatic environments by inorganic and organic pollutants.

Margesin and Schinner (2001) and Conte et al. (2005).

Bioaugmentation

Biostimulation

Bioleaching Biofilters

Biopiling Biosorption

Bioventing

Composting

Phytoremediation

Landfarming

Rhizoremediation

Soil is arranged in piles and they are regularly turned to agricultural practices in order to stimulate degradation by indigenous microorganisms. The plants release exudates which feed and attract the microorganisms of the rhizosphere that promote both the growth of same plant and degradation of the contaminants.

Stormo and Crawford (1992) and Jacques et al. (2008).

Margesin and Schinner (1998), Margesin and Schinner (2001) and Anderson et al. (2003).

Mishra et al. (2001) and Kumar and Philip (2006). Taylor et al. (1992), Mohn et al. (2001), Duran et al. (2007) and Loutseti et al. (2009) Mohn et al. (2001). Kim et al. (2003) and Sari and Tuzen (2009).

Lei et al. (1994), Zenker et al. (2005), Suko et al. (2006), Sui et al. (2007). Bruns-Nagel et al. (1998) and Ahtiainen et al. (2002).

Al-awadhi et al. (1996), Burken and Schnoor (1996), Jacques et al. (2007), Grman et al. (2001), Visoottiviseth et al. (2002), Mancini et al. (2005) and Saadoun and Al-Ghzawi (2005). Al-awadhi et al. (1996), Jacques et al. (2007), Mancini et al. (2005) and Saadoun and Al-Ghzawi (2005). Yee et al. (1998), Johnson et al. (2005), Maila et al. (2005) and Villacieros et al. (2005).

3. Bioremediation Bioremediation, as reported by the US EPA (2001), is defined: ‘‘Use of living organisms to clean up oil spills or remove other pollutants from soil, water, or wastewater; use of organisms such as non-harmful insects to remove agricultural pests or counteract diseases of trees, plants, and garden soil’’ (US EPA, United States Environmental Protection Agency). Vidali (2001) has defined bioremediation as ‘‘the process whereby organic wastes are biologically degraded under controlled conditions to an innocuous state, or to levels below concentration limits established by regulatory authorities’’. This activity can be carried out by several microorganisms as bacteria and fungi, which are able to enzymatically degrade organic pollutants and thanks to some terrestrial and aquatic plants able to remove pollutants from the soil or water by absorption through the roots and next accumulation into the leaves. Microorganisms, indigenous or imported, can interact with plants through several biochemical pathways making the remediation process even more efficient (Vidali, 2001; McCutcheon and Jørgensen, 2008). There is a wide variety of bioremediation techniques that have been developed in the past years; the techniques are summarized in Table 1 (Kavamura and Esposito, 2010). However, in this review, the attention was focused on phytoremediation and the different techniques that it includes. 3.1. Phytoremediation Although the first studies were already carried out in the 50s of the twentieth century, the ‘‘Phytoremediation term’’ was coined in 1991 and it describes a technology that uses plants to remove contaminants from soil and water or to render them harmless (Vidali, 2001; Pulford, 2003; Kumar et al., 2011; Sharma and Pandey, 2014). Phytoremediation is currently attracting the attention of worldwide stakeholders both for its application in soils remediation but also for its ability to improve management of related wastes, because contamination of the environment involves serious risks and it also has an impact on human health: many pollutants are carcinogenic, mutagenic, teratogenic, and harmful to the nervous and endocrine systems, particularly in children. Different physical and chemical methods have been used to restore the various matrices, however with many limitations, because the traditional methods are expensive, they require excessive processing and cause changes in the soil properties,

314

A. Cristaldi et al. / Environmental Technology & Innovation 8 (2017) 309–326 Table 2 Costs related to type of soil treatment (modified by Glass, 1999; Lasat, 2000). Treatment

Cost ($/ton)

Additional factor

Vitrification Landfilling Chemical treatment Electrokinetics Phytoremediation

75–425 100–500 100–500 20–200 5–40

Long term monitoring Transport, excavation, monitoring Recycling of contaminants Monitoring Monitoring

disturbing the native microflora. Phytoremediation is proposed as a relatively recent technology with sustainable costs (Hazrat et al., 2013). Phytoremediation process uses green plants, including herbs (e.g. Thlaspi caerulescens, Brassica juncea, Helianthus annuus) and woody (eg. Salix spp, Populus spp) species, because they are able to remove, uptake, or render harmless various environmental contaminants like heavy metals, organic compounds and radioactive compounds in soil or water, thanks to their transport capacity and accumulation of contaminants (Tahir et al., 2015). Furthermore, phytoremediation prevents excavation of contaminated sites, reduces risk of contaminants dispersion, and it is applicable for the decontamination of sites with various pollutants (Mudhoo et al., 2010). Mechanisms and efficiency of the phytoremediation depend on several factors such as the nature of contaminant, bioavailability, soil properties, plant species (Berti and Cunningham, 2000; Sreelal and Jayanthi, 2017). The plants considered more efficient in phytoremediation processes are the so-called ‘‘hyperaccumulator’’. These plants can tolerate and accumulate metals present in the soil, but they have a low production of biomass (Van Oosten and Maggio, 2014). Extraction efficiency of the pollutants also depends on the biomass produced by the plant: a big biomass is able to uptake a big quantity of metals but it will require more harvests to remove the plants. Consequently, the number of harvests will determine the total cost of the entire operation, including disposal, incineration or composting of biomass (Roy et al., 2005; Rajakaruna et al., 2006; Sharma and Pandey, 2014). Phytoremediation has some disadvantages (slowness of the process, affected area of the land is next to the root, several species cannot be planted in places strongly polluted), but it is applicable at various types of remediation treatment. Its strengths are represented by: – it does not interfere with the ecosystem but confers to the treated land an added aesthetic value through the plant cover; – it requires little labor and therefore it is inexpensive; – it is applies in situ and it is also well accepted by residents. Biomass harvested can be used in the field of renewable energies like biofuel production (Jiang et al., 2015; Tahir et al., 2015) reducing waste disposal. The application of phytoremediation and consequently its market are not yet very strong in Europe as in the USA, where revenues exceeded the $ 300 million already in 2007 (Campos et al., 2008). These data clearly demonstrate the commercial viability of the phytoremediation and in fact, it represents one of the innovative technologies promoted already in 2001 by the US EPA after a careful evaluation of its potential on the field (US EPA, 2001). However, also in Europe the use of phytoremediation technologies has increased in recent years, because they represent an eco-friendly and cheaper alternative method for the environmental remediation than traditional techniques. Already in 1999 (Glass) and in 2000 (Lasat), have shown that the cost of phytoremediation is very low compared to the resources required for the use of conventional technologies (Table 2), such as excavation and conferment of the soil in landfill, soil washing with water and solubilizing agents, vitrification of contaminated soil at high temperatures, electrochemical separation, solidification through use of stabilizing agents. Many studies have reported use of phytoremediation techniques in different countries and for different contaminants (see Table 3). Depending on the nature of the contaminants and/or mechanism of bioremediation, there are various techniques of phytoremediation (see Table 4 and Fig. 1). 3.1.1. Phytoextraction Phytoextraction is a technique used in situ for the treatment of contaminated soils (Barceló and Poschenrieder, 2003; Newman and Reynolds, 2004; Kavamura and Esposito, 2010; Alì et al., 2013; Van Oosten and Maggio, 2014). Contaminants are absorbed by the roots, transported and accumulated in the shoots and leaves (Mahar et al., 2016; Sreelal and Jayanthi, 2017). Plants involved in this process should ideally have the ability to accumulate contaminants and produce a high biomass. The hyperaccumulator species (e.g. Thlaspi caerulescens, Alyssum bertholonii, Arabidopsis halleri) are able to accumulate contaminants but produce little biomass and then, it is possible to use species that accumulate less but which produce more biomass like Brassica spp., Arundo donax and Typha spp. (Barceló and Poschenrieder, 2003; Gou and Miao, 2010; Fiorentino et al., 2012; Shiri et al., 2015). The removal of contaminants happens with the harvest of plants, and the process will continue with the incineration and landfilling. Phytoextraction is an eco-friendly technology and has important advantages: – it does not damage/change the landscape; – it preserves the conservation and consequently the ecosystem;

A. Cristaldi et al. / Environmental Technology & Innovation 8 (2017) 309–326

315

Table 3 Some examples of phytoremediation techniques applied in different countries. Author

Title

Plant species

Accumulation (mg kg−1 )

Site

Period

Torvicosa (Udine)

May–September 2005

Napoli

July 1999–July 2000

Soil treatment: plowing

Vamerali et al. (2009)

Phytoremediation trials on metal- and arsenic-contaminated pyrite wastes (Torviscosa, Italy)

P.alba P.nigra P.tremula S.alba

Macro- and trace-element concentrations in leaves and roots of Phragmites australis in a volcanic lake in Southern Italy

Zn 62.1 ± 0.95 76.8 ± 10.1 106 ± 8.64 56.7 ± 8.47

Soil treatment: subsoiling

P.alba P.nigra P.tremula S.alba

Baldantoni et al. (2014)

Cu 4.95 ± 0.23 4.01 ± 0.50 9.11 ± 1.42 7.61 ± 1.17

Phragmites australis

Cu

Zn

4.41 ± 0.15 4.31 ± 0.14 6.59 ± 0.15 7.50 ± 0.61

65.4 ± 8.19 103 ± 7.59 116 ± 11.6 93.8 ± 12.4

Cr

Cu

Site A: 5.15 Site B: 4.38 Site C: 2.56

Site A: 75.87 Site B: 65.51 Site C: 6.05

Fe

Mg

Site A: 17.58 Site B: 17.78 Site C: 17.18

Site A: 2.83 Site B: 3.11 Site C: 3.24

Mn

Ni

Site A: 763.3 Site B: 951.7 Site C: 740

Site A: 7.49 Site B: 4.70 Site C: 3.07

Pb

V

Site A: 92.57 Site B: 69.09 Site C: 47.37

Site A: 21.21 Site B: 29.92 Site C: 28.65 Zn

Site A: 118.7 Site B: 149 Site C: 126.7 (continued on next page)

– it is the main technique of phytoremediation to the removal of heavy metals from soil, sediment and water; – it is also considered as the most commercially promising technique because it is inexpensive. However, although it presents some advantages, there are some factors that limit the metals phytoextraction (Sharma and Pandey, 2014): – a lower bioavailability of metal in the rhizosphere; – a lower absorption rate of the metal from the roots; – the metals are detained within the roots. Several research work have been performed for demonstrate the ability of some plant species to implement the phytoextraction processes in respect of some heavy metals: Kos et al. (2003) and Guo and Miao (2010) evaluated the phytoextraction capacity of the perennial herbaceous plant Arundo donax versus a contaminated soil by Cd and they have obtained values of 2.92–4.02 mg kg−1 and 0.57–1.42 mg kg−1 of Cd in leaves and rhizomes respectively. Fiorentino et al. (2012), have repeated the tests using Arundo donax assisted by the fungal microorganism Trichoderma harzianum and the phytoextraction of Cd is increased in leaves (+20%) and rhizomes (+30%). 3.1.2. Phytostabilization Pollutants are immobilized in the root system through absorption of the roots or precipitation in the rhizosphere. This process reduces the contaminant mobility, preventing migration into groundwater and reduce the bioavailability in the food chain (Barceló and Poschenrieder, 2003; Alì et al., 2013; Sharma and Pandey, 2014; Van Oosten and Maggio, 2014). Metal-tolerant species are used to restore vegetation in contaminated sites. Phytostabilization was useful for the treatment of Pb, As, Cd, Cr, Cu and Zn (Zhao et al., 2016; Yang et al., 2016). The advantage of this technique consists in the changes of soil chemistry composition induced by presence of the plant itself and such these changes can facilitate the absorption or cause the precipitation of metals on the roots (Zhang et al., 2009). However, this technique is not able to remove the contaminant by

316

A. Cristaldi et al. / Environmental Technology & Innovation 8 (2017) 309–326

Table 3 (continued) Author

Title

Plant species

Accumulation (mg kg−1 )

Plantago major

Ni

Cr

Leaves Roots


3.4 ± 0.4 3.9 ± 0.2

Cu

Pb

Leaves Roots

45.3 ± 0.2 325.5 ± 3.2

76.8 ± 3.5 77.2 ± 0.3

Zn

Fe

Leaves Roots

77.2 ± 0.3 152.5 ± 1

876.8 ± 1.1 6244.3 ± 20.8

Site

Period

Imperina (Belluno)

Spring–Summer 2008

Mn Leaves Roots

Fontana et al. (2010)

Preliminary observations on heavy metal contamination in soils and plants of an abandoned mine in Imperina Valley (Italy)

19 ± 0.1 42.7 ± 0.4

Salix eleagnos

Ni

Cr

Leaves Stem Root

4.8 ± 0.2

3.3 ± 0.3 2.8 ± 0.2 3.2 ± 0.2

Cu

Pb

Leaves Stem Root

27.8 ± 0.1 16.3 ± 0.1 80.5 ± 0.7

26.4 ± 0.2 7.2 ± 0.2 32.7 ± 2.1

Zn

Fe

Leaves Stem Root

516.6 ± 3.1 388 ± 2.2 227.8 ± 1.5

569.5 ± 5.4 66.7 ± 0.4 427.2 ± 2.9 Mn

Leaves Stem Root

19 ± 0.1 42.7 ± 0.4 69.9 ± 0.7

Salix purpurea

Ni

Cr

Leaves Stem Root


3.7 ± 0.2 2.7 ± 0.2 3.0 ± 0.3

Cu

Pb

Leaves Stem Root

27.8 ± 0.8 14.1 ± 0.1 15.8 ± 0.2

25.6 ± 1.2

Zn

Fe

Leaves Stem Root

231.8 ± 1.1 189.9 ± 0.7 92.7 ± 0.3

660.7 ± 2.7 79.1 ± 0.3 217.3 ± 1.1 Mn

Leaves Stem Root

81.8 ± 0.6 19.7 ± 0.6 34.8 ± 0.1

Salix caprea

Ni

Cr

Leaves Stem Root


3.7 ± 0.2 2.4 ± 0.3 2.9 ± 0.1

Cu

Pb

Leaves Stem Root

39.9 ± 0.2 50.2 ± 0.2 55.5 ± 0.8

156.1 ± 2 99.3 ± 2.7 573.1 ± 18.7

Zn

Fe

Leaves Stem Root

339 ± 0.9 239.7 ± 1.3 155.7 ± 0.8

926.6 ± 5.9 122.1 ± 0.7 650.1 ± 2.5 (continued on next page)

A. Cristaldi et al. / Environmental Technology & Innovation 8 (2017) 309–326

317

Table 3 (continued) Author

Title

Plant species

Accumulation (mg kg−1 )

Site

Period

Cava del Predil (Udine)

Spring 2005 (50 days)

Acerra (Napoli)

2 years

Livorno

18 week

Mn Leaves Stem Root

Marchiol et al. (2011)

Fiorentino et al. (2013)

A decade of research on phytoremediation in north-east Italy: lessons learned and future directions

Assisted phytoextraction of heavy metals: compost and Trichoderma effects on giant reed (Arundo donax L.) uptake and soil N-cycle microflora

104 ± 0.4 10.8 ± 0 13.4 ± 0.1

Sorghum bicolor

As

Cd

Roots Shoots

67.5 ± 18 5.23 ± 0.93

1.75 ± 0.31 0.20 ± 0.06

Co

Cu

Roots Shoots

9.42 ± 3 0.47 ± 0.05

594 ± 121 28.6 ± 4.5

Pb

Zn

Roots Shoots

60.1 ± 26 2.73 ± 0.38

265 ± 70 86.4 ± 19

H. annuus

As

Cd

Roots Shoots

48.6 ± 7.17 0.62 ± 0.18

2.31 ± 0.68 0.64 ± 0.08

Co

Cu

Roots Shoots

7.48 ± 1.54 0.55 ± 0.18

837 ± 141 36.2 ± 12

Pb

Zn

Roots Shoots

42.9 ± 4.63 2.52 ± 0.82

242 ± 43.4 118 ± 9.09

Zn 94.7 ± 28.6

Cu 54.4 ± 16.2

Cd 3.1 ± 0.6

Pb 73.7 ± 18.2

Arundo donax

Cr 14.8 ± 1.7 Andreolli et al. (2013)

Fumagalli et al. (2014)

Agnello et al. (2016)

Endophytic Burkholderia fungorum DBT1 can improve phytoremediation efficiency of polycyclic aromatic hydrocarbons

The rotation of white lupine (Lupinus albus L.) with metal-accumulating plant crops: A strategy to increase the benefits of soil phytoremediation

Comparative bioremediation of heavy metals and petroleum hydrocarbons co-contaminated soil by natural attenuation, phytoremediation, bioaugmentation and bioaugmentation-assisted phytoremediation

Naphthalene 0.01–0.26

Phenanthrene 3.1 ± 0.9

Fluorene 4.9 ± 1.6

Dibenzothiophene 6.9 ± 1.4

Lupinus alba

Cu

Pb

Root Shoot

28 ± 7 16 ± 5

22 ± 19 10 ± 0.3

Ni

Zn

Root Shoot

12 ± 2 5±2

158 ± 95 118 ± 37

Cr

Cd

Root Shoot

21 ± 5 11 ± 5


Medicago sativa

Zn

Hybrid poplar (P. deltoides x P. nigra)

September– March (year not available)

Not available

90 days

Cu

169; 78 Root; Shoot

Ferrara

71; 21 Pb 23; 17

Petroleum hydrocarbons removed M. sativa with P. aeruginosa

C10–C12: 78%–95% C12–16: 58%–90% C16–C21: 35%–65% C21–40: 15%–45% (continued on next page)

soil remediated until the plant is eradicated. Yang et al. (2016), carried out a study in southern China, applying this technique by revegetation in an mine soils extremely acid bringing the initial pH of 2.6 to a 3.8 after two years of phytostabilization.

318

A. Cristaldi et al. / Environmental Technology & Innovation 8 (2017) 309–326

Table 3 (continued) Author

Fiorentino et al., 2017

Title Giant reed growth and effects on soil biological fertility in assisted phytoremediation of an industrial polluted soil

Almansoory Potential application of a et al. biosurfactant in (2015) phytoremediation technology for treatment of gasoline-contaminated soil Burges et al. (2017)

Li et al. (2003)

Ecosystem services and plant physiological status during endophyte-assisted phytoremediation of metal contaminated soil

Plant species

Accumulation (mg kg−1 )

Arundo donax

Pb

Zn

Culms (2nd year) Leaves (2nd year) Shoot (2nd year) Rizome (2nd year)

0.36 ± 0.04 0.67 ± 0.02

50.1 ± 4.62 74.9 ± 8.00

0.41 ± 0.03 9.2 ± 1.67

54.2 ± 5.07 86.6 ± 12.29

L. octovalvis with S. marcescent S. marcescens

Site

Period

Bagnoli– Fuorigrotta (Napoli)

2 years

TPH (Total petroleum hydrocarbon)

Malaysia

72 days

58.8

N. caerulescens R. acetosa

Development of a technology for A. bertolonii commercial phytoextraction of nickel: economic and technical considerations

Cd

Pb

Zn

11.2 ± 0.9

3583 ± 277

14 446 ± 2736

11.7 ± 1.4

4301 ± 550

13,095 ± 696

Coto ‘‘Txomin’’, province of Biscay, Spain

24 weeks

Ni Oregon, USA

120 days

Zaire

Not available

New Caledonia

Not available

Zaire

Not available

New Caledonia

Not available

Germany

Not available

Iowa, USA

Not available

Gothenburg, Sweden

76 days

Himedia, India

21 days

10 900 A. cacricum A. corsicum

12 500 18 100

Aeolanthus biformifolius

Cu 13 700

Chaney et al. (2010)

Phytoremediation of soil trace elements

Alyxia rubricaulis

Mn 11 500

Haumaniastrum robertii

Co 10 200

Phyllanthus serpentinus

Ni 38 100

Thlaspi caerulenscens

Zn 39 600

Koptsik et al. (2014)

Wang et al. (2005) Goswami and Das (2016)

Problems and prospects concerning the phytoremediation of heavy metal polluted soils: a review

Helianthus annuus

Changes in Hg fractionation in soil induced by willow

Salix viminalis

Hg 0.66

Salix schwerinii

0.55

Copper phytoremediation potential of Calandula officinalis L. and the role of antioxidant enzymes in metal tolerance

Pb 5600

Calandula officinalis Root Shoot

Cu 1.96 ± 0.17 2.09 ± 0.13

Results of this study highlight that the assisted phytostabilization can be a practical and effective strategy for the reclaim of mine soils. 3.1.3. Phytovolatilization In phytovolatilization process the pollutants are absorbed at root level, transported through the xylem and released into the atmosphere from the aerial parts of plant in less toxic forms as a result of metabolic modification. Therefore, pollutants are not removed but rather transferred from one compartment to another (Barceló and Poschenrieder, 2003; Alì et al., 2013; Sharma and Pandey, 2014; Van Oosten and Maggio, 2014). Diffusion of these substances in air compartment can also be through other parts of plant before they reach the leaves and shoots. The most advantage of this technique is the possibility that the contaminant can be transformed into a less toxic substance, but, on the other hand, the weakness of this application

A. Cristaldi et al. / Environmental Technology & Innovation 8 (2017) 309–326

319

Table 4 Different approach of phytoremediation (Alì et al., 2013). Techniques

Description

Phytoextraction

Pollutants are absorbed by the roots, transported and accumulated in the shoots and leaves. Pollutants are immobilized in the root system and it is reduces their mobility. Pollutants are converted in a less toxic forms and released in atmosphere. Plant enzymes degrade organic contaminants. Removal of pollutants from surface water or wastewater through adsorption or precipitation. Degradation of pollutants in the rhizosphere through rhizospheric microorganisms. Removal of salts from salt-affected soils through halophyte plants.

Phytostabilization Phytovolatilization Phytodegradation Rhizofiltration Rhizodegradation Phytodesalination

Fig. 1. Techniques of phytoremediation and alternative destinies of the pollutants.

is the possibility that the modified substance, and still potentially toxic, can be released into atmosphere and then resettling into the environment. The phytovolatilization can be applied to contaminants present in soil, sediment or water, especially for organic contaminants like tetrachloroethane, trichloromethane and tetrachloromethane (Susarla et al., 2002; Zhang Yu and Dong Gu, 2006; San Miguel et al., 2013) and only for some metals like Hg and Se that have a relatively high volatility (Wang et al., 2012; Van Oosten and Maggio, 2014). The mercury ion, can be transformed in a less toxic form and released into the atmosphere later. However, this involves a high risk of a new emission into the environment of this metal because, through precipitation, it can settle on lakes and oceans forming organic compound methylmercury thank to the action of anaerobic bacteria (Sharma and Pandey, 2014). Release of mercury from leaf tissues is highly influenced by environmental parameters such as light intensity and air temperature (Wang et al., 2012). Wang et al. (2012) have reported a study carried out by Leonard et al. (1998) where have analyzed the mercury exchange between the aerial parts of the plant and the air. They examined five plant species (Lepidium latifolium, Artemisia douglasiana, Caulanthus sp., Fragaria vesca, Eucalyptus globulus) cultivated in contaminated soil with a mercury concentration between 450 and 1605 mg kg−1 . Caulanthus sp. showed a higher rate of mercury emissions (92.6 ng m−2 h−1 ) in the daytime compared to other plant species, instead, the emissions in the dark were an order of magnitude lower during the day for all plant species (Wang et al., 2012). 3.1.4. Phytodegradation In Phytodegradation process, organic contaminants, after absorption by the root system, are degraded thanks to the action performed by enzymes involved in metabolism of the plant, or they will be incorporated into the plant tissues ( Barceló and Poschenrieder, 2003; Trap et al., 2005; Alì et al., 2013; Sharma and Pandey, 2014; Van Oosten and Maggio, 2014). The involved enzymes in phytodegradation process are: (1) dehalogenase (transformation of chlorinated compounds); (2) peroxidase

320

A. Cristaldi et al. / Environmental Technology & Innovation 8 (2017) 309–326

(transformation of phenolic compounds); (3) nitroreductase (transformation of explosives and other nitrate compounds); (4) nitrilase (transformation of cyanated aromatic compounds); (5) phosphatase (transformation of organophosphate pesticides) (Susarla et al., 2002; Winquist et al., 2013; Deng and Cao, 2017). Phytodegradation can be used in remediation processes of contaminated sites by organic contaminants, like chlorinated solvents, herbicides (Bamforth and Singleton, 2005) and PAHs, (Yin et al., 2011) and it can also be applied to the recovery of surface and ground waters. Different types of plants have been used for this technique. Gutiérrez-Ginés et al. (2014), used the plant species Lupinus luteus associated with endophytic bacteria for the remediation of landfill soils in Iberian peninsula with organic pollutants including PAHs such as benzo(a)pyrene. Two experiments were conducted in a greenhouse: (1) growing in a substrate artificially contaminated with benzo(a)pyrene; (2) using the soil of the landfill. Then, endophytic bacteria were isolated from roots and shoots of the plants used for the two experiments conducted in greenhouse. The growth tests and tolerance to organic pollutants and degradation tests were performed on all isolates in bioassay 1, and those coming from cultures in bioassay test 2. Results obtained indicate that the plants showed no toxicity symptoms when exposed to benzo(a)pyrene but this occurred when it grown in soil of the landfill. Some endophytic bacteria showed plant growth-promotion capacity and tolerance to benzo(a)pyrene and other organic compounds (diesel and PCBs). Some strains can also have the ability to metabolize these organic pollutants. 3.1.5. Rhizofiltration Rhizofiltration permits the removal of organic and inorganic pollutants from groundwater, surface water and wastewater by adsorption or precipitation on the roots, or for adsorption of contaminants around the root zone (Zhang et al., 2009). This method uses both terrestrial and aquatic plants for in situ or ex situ applications, however, terrestrial plants are preferred because they have a more developed root and fibrous system, so they have a greater surface area for absorption. The plants used, in addition to being tolerant metal, must have a high absorption surface and tolerate hypoxia (e.g. Salix spp, Populus spp, Brassica spp.). Some disadvantages of this technique consist in: adjust the pH, necessity of a first cultivation in a greenhouse, frequent harvests and subsequent disposal of the plants (Barceló and Poschenrieder, 2003; Sharma and Pandey, 2014). This technique can be applied for the removal of heavy metals (Susarla et al., 2002), because they are maintained at root level, which, once saturated of these elements, will be harvested. This technique is used also to remove radioactive elements. A famous cases concern the sunflowers that have been successfully used to remove radioactive contaminants (cesium and strontium) from contaminated soil in Chernobyl, Ukraine. The researchers saw that the sunflowers had been able to accumulate Cs and Sr; the first remaining in the roots, the second moving into the shoots (Prasad, 2007). Lee and Yang (2010), have reported a rhizofiltration test using sunflower (Helianthus annuus) and bean (Phaseolus vulgaris) to remediate contaminated groundwater by uranium. For this experiment were used an artificially uranium contaminated solution and three genuine groundwater samples. More than 80% in the artificial solution and uranium in groundwater, respectively, has been removed using the sunflower and the residual concentration of uranium present in the treated water was less than 30 µg/L (US EPA drinking water limit). Regarding the bean, the efficiency of uranium removal was approximately 60%–80%. The maximum removal of uranium through rhizofiltration for the two plant cultivars used has exceeded 90% and the most uranium has been accumulated at root level. 3.1.6. Rhizodegradation Rhizodegradation consists in the biodegradation of the organic contaminants at level of the radical apparatus of the plant, in a soil area called rhizosphere. This process occurs thanks to the action of bacteria, fungi and yeasts (several studies have shown that the number of microorganisms in the rhizosphere is 100 times greater than the quantity present on the surface), which obtain nutrients from the root exudates of the plant. Root exudates are a carbon and nitrogen source, and they are able to increase the efficiency of extraction and removal of contaminants by the plant (Barceló and Poschenrieder, 2003; Gerhardt et al., 2009; Leung et al., 2013; Liu et al., 2014; Van Oosten and Maggio, 2014)). Microorganisms are more expressed in the rhizosphere thanks to the presence of various nutrients like sugars and amino acids, but also due to enzymes and other compounds synthesized by plant and that stimulate their growth. Roots, in their turn, provide a greater surface area available for microbial growth and a sufficient quantity of oxygen. So, considering all these factors, the association between microorganisms and plants leads to advantages for both. Among the various soil microorganisms, mycorrhizal fungi are able to interact with the host plants, constituting a symbiotic association. Interaction occurs at level of the root system and there are two categories of mycorrhizae: endomycorrhiza, if the fungus is within in the root tissue; ectomycorrhiza, if the fungus is outside of the root tissue (Leung et al., 2013). Obviously, the rhizodegradation also shows advantages and disadvantages. Among the advantages (Shimp et al., 1993; Cunningham and Ow, 1996; Kaimi et al., 2006; Kavamura and Esposito, 2010; Fiorentino et al., 2012): – it is a process that occurs in situ; – translocation of the compounds to other parts of the plant or in the atmosphere is lesser than other technologies of phytoremediation; – it can get a complete mineralization; – installation and maintenance costs are low. Among the disadvantages (Shimp et al., 1993; Cunningham and Ow, 1996; Kavamura and Esposito, 2010; Fiorentino et al., 2012):

A. Cristaldi et al. / Environmental Technology & Innovation 8 (2017) 309–326

321

– it is a slow process and efficient only on surface of contamination (20–25 cm of depth); – the depth of the roots may be limited by the physical structure of soil; – plants may require fertilizer. Rhizodegradation improves the soil characteristics and it is particularly useful for the remediation of contaminated soils with a wide range of chemicals, including PAHs, pesticides, polychlorinated biphenyls (PCBs), BTEX compounds (benzene, toluene, ethylbenzene, xylene). A few studies have evaluated the ability to degrade PAHs, like phenanthrene and pyrene, using the rhizodegradation process with the employment of some plants as Kandelia candel (Lu et al., 2011) or Avicennia marina (Jia et al., 2016), suggesting how the presence of these mangroves is effective for promoting the degradation of such compounds at rhizosphere level. The exposure tests with Kandelia candel were conducted in greenhouse, adding to the rhizosphere of the plant 10 mg kg−1 of phenanthrene and 10 mg kg−1 of pyrene. After 60 days of plant growth, researchers have seen that the plant’s presence has considerably improved degradation of phenanthrene (47.7%) and pyrene (37.6%) from the contaminated sediment. The higher PAHs degradation rates were detected at 3 mm from the root zone (56.8% phenanthrene and 47.7% pyrene). The degradation rate has had the following sequence: near rhizosphere >root compartment >far-rhizosphere soil zones for both contaminants where mangroves was grown (Lu et al., 2011). In a study carried out by Jia et al. (2016) is showed that the degradation of phenanthrene and pyrene was improved in the rhizosphere compared to non rhizosphere sediments. Furthermore, there was a significant relationship (R2 >0.91) among dissolved organic carbon concentrations and the residual PAHs in rhizosphere and non rhizosphere sediment after 120 days of growing. 3.1.7. Phytodesalination Compared to the techniques examined, less studies are available in the scientific literature regarding the phytodesalination (Pouladi et al., 2016). This technique is not applicable for remediation of soil contaminated with heavy metals and PAHs but it is considered the capacity of some halophytes plants to accumulate sodium quantities in their shoots (Zorrig et al.,2012). Halophytes plants are able to tolerate high concentrations of Na+ and Cl− ions and so they are able to settle on saline soils (Flowers and Colmer, 2015). Saline soils cover about 6% of the world’s land (Zorrig et al., 2012) and salinity is the main environmental factor limiting plant growth and productivity. Several methods (chemical, physical and biological) have been established to reclaim the saline soils and phytodesalination is a biological methods used for this aim (Sakai et al., 2012). Zorrig et al. (2012), have carried out a phytodesalination study in arid and semi-arid areas of China. They have been used four halophytic plants: Artemisia argyi, Limonium bicolor, Melilotus suaveolens and Salsola collina; they were tested in pot experiment by using three salt-affected soils (Dagang district, Xiqing district and county Jixiang) in Tianjin. Soil physicochemical properties and concentrations of ions were evaluated, both before and after the growth of the plants used, and it was possible to see that in all test the concentrations of Na+ and Cl− ions were decreased after the growth of halophytic plants. 4. Plants used in phytoremediation and their biochemical processes Essential nutrients for the plants (N, P, K, Ca, Mg, S, Fe, Cl, Zn, Mn, Cu, B, Mo), present in soil, are absorbed through the root system. This can occur through passive mechanisms such as the flow of transpiration, or through active mechanisms, thanks to the action of transport proteins associated with the cell membrane. These elements are transported within the plant via two routes: the apoplast and symplast. Once inside the roots, the dissolved nutrients are transferred to the rest of the plant through a vascular system, known as xylem. In addition to essential nutrients, the plants can also absorb nonessential inorganic compounds considered as potential pollutants such as heavy metals. Elements normally considered nutrient for the plants, such as Cu, Zn and Mn, could become toxics if presents a high concentrations, so, the plants utilize various mechanisms to retain or stabilize them. Considering these characteristics, plants can be employed in remediation processes of contaminated soils, thanks to their ability to accumulate or degrade some contaminants, then also reducing the volumes of waste going to the landfills. Several plants are capable of absorbing various contaminants through the roots, which accumulate in the leaves inside the vacuoles where remain trapped until the leaves do not fall on the ground or, at least, until they are removed. Plants suitable for phytoremediation processes are chosen according to the ability to absorb contaminants of interest. Metallophytes are herbaceous or woody plants able to accumulate and tolerate heavy metals (Barceló and Poschenrieder, 2003) with concentrations up to 100 times higher respect to the non-hyperaccumulator species (Lasat, 2000). It is possible distinguish between obligate metallophytes, (presence of some metals is need for their survival) and facultative metallophytes (able to tolerate the high concentration of metals but, their are not necessary for the survival). Hyperaccumulator species (e.g. Brassica juncea, Helianthus annuus, Festuca arundinacea, Populus spp., etc.) have developed mechanisms that allow to tolerate high metals concentrations, which could be toxic for other organisms. (Lasat, 2000; Ernst, 2006; Kavamura and Esposito, 2010). Some species, such as Brassicaceae, are good hyperaccumulator (Jing et al., 2007). Thlaspi caerulescens has a good tolerance towards Cd and Zn thanks to phytochelatins, because they are able of chelating various metal ions, reducing their concentration in cytosol and allowing their storage in vacuoles (Ernst, 2006; Deniau et al., 2007; Kavamura and Esposito, 2010). Thlaspi caerulescens (hyperaccumulator) and Thlaspi arvense (not hyperaccumulator) have been used to evaluate the absorption and zinc transport (Barceló and Poschenrieder, 2003). Various Willows (Salix spp) were used to study the ability to uptake heavy metals in field and greenhouse, and Landberg and Greger have tested various clones to evaluate accumulation and tolerance versus Zn and Cd (Pulford and Watson, 2003).

322

A. Cristaldi et al. / Environmental Technology & Innovation 8 (2017) 309–326

Some clones has reported tolerant for both metals and other just only. Absorption and transporting of metals were in a range between 1% and 72%. Also Wani et al. (2011) have reported that Willow shows a good uptake capacity for various metals (Cd, Cu, Zn, Ni, Pb and Fe). Willow compared to herbaceous hyperaccumulator plants, having a deeper root system, is able to reclaim a greater depths of the soil. Marmiroli et al. (1999), have carried out a study to verify the phytoremediation ability of Walnut (Juglans regia) and Maple (Acer saccharinum) versus Pb and Cr. Both plants showed a greater accumulation of Pb in the roots due to limited translocation of the metal in the stems, but the Walnut was more efficient than Maple in the absorption of both metals. Some plants have been used in soil polluted by organic substances. Several years ago, in some refinery plants evaluated the use of some fruit trees such as mulberry, apple, and Osage orange, for their ability to release flavonoids and polyphenols compounds which are known to induce the enzymes in PAH-degrading organisms (Fletcher, 1995; Schnoor, 1997). Today, it is preferred to use ornamental plants, like Echinacea purpurea, Callistephus chinensis, Festuca arundinacea, Medicago sativa (Xiao et al., 2015) Kandelia candel (Lu et al., 2011), Avicennia marina (Jia et al., 2016) Populus spp, Salix spp and still others. The plants live in symbiosis with microorganisms naturally present in the rhizosphere. The rhizosphere has an intense microbial activity due to the presence of organic matter that comprehends root exudates. So, the plant provides the root exudates to microorganisms which in turn can help the plant to absorb nutrients improving so the plant performance and consequently, the soil quality (Kavamura and Esposito, 2010). Thanks to the interaction with microorganisms, the plants have shown good degradative capacity of different organic compounds such as PAHs (Alkorta and Garbisu, 2001; Roy et al., 2005; Stroud et al., 2007). Xiao et al. (2015), showed that M. sativa is effective to degrade PAHs (e.g. fluoranthene, pyrene, benzo(a)anthracene, chrysene, benzo(b)fluoranthene, benzo (k)fluoranthene, benzo(a)pyrene, dibenzo(a,h)anthracene) after planting at 60, 120 and 150 days. After 150 days, PAHs were degraded, in particular: fluoranthene (90.67%), pyrene (79,53%), benzo(a)anthracene (100%), chrysene (100%), benzo(b)fluoranthene (100%), benzo(k)fluoranthene (100%), benzo(a)pyrene (99.6%), dibenzo(a,h)anthracene (100%). Organic substances will be modified by several chemical reactions such as oxidation, reduction and/or hydrolysis and subsequent conjugation with glutathione (GSH), sugars or organic acids, enhancing your solubility and moved into vacuoles, where they can be further metabolized to CO2 and water (Chaney et al., 1997; Campos et al., 2008; McCutcheon and Jørgensen, 2008; Nunes de Silva et al., 2014). Several enzymes can play an important role in the degradation of contaminants, such as mono and dioxygenase, dehydrogenase, hydrolase, peroxidase, nitroreductase, dehalogenase, phosphatase, carboxylesterase and others. These enzymes are released naturally in soil, where they are able to degrade various organic pollutants (Campos et al., 2008). Ability to phytoremediation through the use of appropriate engineered plant species and coupled to proteomics techniques (McCutcheon and Jørgensen, 2008) has also been evaluated. In fact, a transgenic test was carried out by French et al. (1999), showing a significant rising of capacity of the tobacco plant to degrades the explosives such as TNT and GTN. Other studies with genetically modified plants have proven that engineered plants can be used to reclaim the soils polluted by herbicides, PCBs, nitroaromatic compounds, etc. (Campos et al., 2008; Kawahigashi, 2009). 5. Conclusions and future perspectives In this review the phytoremediation techniques available today for the recovery of contaminated soils by metals and organic substances were reported. Until 15–20 years ago, the phytoremediation could be considered an emerging and innovative technology (Schwitzguébel et al., 2002). In recent years, European researchers have filled up the initial gap with the United States regarding the knowledge on phytoremediation but, still remains a certain difference concerning their application (Marmiroli et al., 2006). Private companies of countries like the United States and Canada, have as their objective the application of phytoremediation techniques for pollution management (Sharma and Pandey, 2014). Conventional methods have a higher removal efficiency of contaminants, the times of application are shorter than the phytoremediation but they are more expensive and change the characteristics of both soil and groundwater. Instead, phytoremediation can be a good alternative than to conventional physicochemical methods (excavation and landfilling, washing, vitrification, electrochemical separation), because, it is a clean and economical technology using living organisms. Furthermore, phytoremediation requires minimal intervention by specialists and can be applied for longer time, it involves a smaller amount of material going to landfills and not release substances potentially dangerous in the environment (Sharma and Pandey, 2014). Environmental problems caused by the landfills and/or petrochemical complexes are well documented, and both in developed countries than in developing, the scarcity of free land and the need to reuse the spaces provided require the rehabilitation of these soils polluted. In Italy, as in Europe and USA, it would be desirable some intervention in those areas subject to intense contamination that need of remediation and possibly to be converted into productive areas. This approach can be used for remediation, e.g., of several Italian contaminated sites as Ilva of Taranto in Puglia region, the petrochemical pole of Syracuse province (formed by the towns of Augusta, Melilli and Priolo), the petrochemical of Gela city and the industrial center of Milazzo city and the famous case of ‘‘the Italian triangle of death’’ of Acerra, in Campania region (Mazza and Senior, 2004; Manno et al., 2006; Basile et al., 2009; Marinaccio et al., 2011). Phytoremediation provides obvious benefits, and the product biomass may be employed again for cogeneration of energy and production of biofuels, after removing of the extracted contaminants; the metals recovered after the incineration of the plants may become a raw material for industrial processes. Furthermore, additional benefits can be obtained by

A. Cristaldi et al. / Environmental Technology & Innovation 8 (2017) 309–326

323

genetic modified plants in order to maximize the purification efficiency respect to a particular contaminant, but their use and their risks should be evaluated case by case (Baglivo, 2007). Given the potential benefits, there is no doubt that the phytoremediation techniques represent a valid alternative to the physicochemical methods, to obtain benefits in both economic and environmental terms. A more complete knowledge of the potentialities and the limitations of phytoremediation surely can increase the use of this technique in the next future for the soil remediation. Acknowledgment None. No funding to declare. Conflict of interests The authors declare that there is no conflict of interests regarding the publication of this paper. References Agency for Toxic Substances & Disease Registry (ATSDR), 2005. Toxicological profile for Nickel. In: Agency for Toxic Substances and Disease Registry Report, Atlanta, GA, USA, 2005. www.atsdr.cdc.gov/ToxProfiles. Agnello, A.C., Bagard, M., Van Hullebusch, E.D., Esposito, G., Huguenot, D., 2016. Comparative bioremediation of heavy metals and petroleum hydrocarbons co-contaminated soil by natural attenuation, phytoremediation, bioaugmentation and bioaugmentation-assisted phytoremediation. Sci. Total Environ. 563–564, 693–703. Ahtiainen, J., Valo, R., Järvinen, M., Joutti, A., 2002. Microbial toxicity tests and chemical analysis as monitoring parameters at composting of creosotecontaminated soil. Ecotoxicol. Environ. Saf. 53, 323–329. Al-awadhi, N., Al-Daher, R., Elnawawy, A., Balba, M.T., 1996. Bioremediation of oil-contaminated soil in Kuwait. I. Landfarming to remediate oilcontaminated soil. J. Soil Contam. 5, 243–260. Alì, H., Khan, E., Sajad, M.A., 2013. Phytoremediation of heavy metals - Concepts and applications. Chemosphere 91, 869–881. Alkorta, I., Garbisu, C., 2001. Phytoremediation of organic contaminants in soil. Bioresour. Technol. 79, 273–276. Almansoory, A.F., Hasan, H.A., Idris, M., Abdullah, S.R.S., Anuar, N., 2015. Potential application of a biosurfactant in phytoremediationtechnology for treatment of gasoline-contaminated soil. Ecol. Eng. 84, 113–120. Anderson, R.T., Vrionis, H.A., Ortiz-Bernad, I., Resch, C.T., Long, P.E., Dayvault, R., 2003. Stimulating the in situ activity of Geobacter species to remove uranium from the groundwater of a uranium-contaminated aquifer. Appl. Environ. Microbiol. 69, 5884–5891. ´ B., Vallini, G., 2013. Endophytic burkholderia fungorum dbt1 can improve phytoremediation efficiency Andreolli, M., Lampis, S., Poli, M., Gullner, G., Bir0, of polycyclic aromatic hydrocarbons. Chemosphere 92, 688–694. Baldantoni, D., Cicatelli, A., Bellino, A., Castiglione, S., 2014. Different behaviours in phytoremediation capacity of two heavy metal tolerant poplar clones in relation to iron and other trace elements. J. Environ. Manage. 146, 94–99. Bamforth, S.M., Singleton, I., 2005. Bioremediation of polycyclic aromatic hydrocarbons: current knowledge and future directions. Rev. J. Chem. Technol. Biotechnol. 80, 723–736. http://dx.doi.org/10.1002/jctb.1276. Barceló, J., Poschenrieder, C., 2003. Phytoremediation: principles and perspectives. Contrib. Sci. 2 (3), 333–344 Institut d’Estudis Catalans, Barcelona. Basile, A., Sorbo, S., Aprile, G., Conte, B., Castaldo Cobianchi, R., Pisani, T., Loppi, S., 2009. Heavy metal deposition in the Italian ‘‘triangle of death’’ determined with the moss Scorpiurum circinatum. Environ. Pollut. 157, 2255–2260. Berti, W.R., Cunningham, S.D., 2000. Phytoremediation of Toxic Metals: Using Plants To Clean Up the Environment. Wiley-Interscience, John Wiley and Sons, Inc., New York, NY, pp. 71–88. Broadley, M.R., White, P.J., Hammond, J.P., Zelko, I., Lux, A., 2007. Zinc in plants. New Phytol. 173 (4), 677–702. Bruns-Nagel, D., Drzyzga, O., Steinbach, K., Schmidt, T.C., Löw, E., Gorontzy, T., 1998. Anaerobic/aerobic composting of 2, 4, 6-trinitrotoluene-contaminated soil in a reactor system. Environ. Sci. Technol. 32, 1676–1679. Burges, A., Epelde, L., Blanco, F., Becerril, J.M., Garbisu, C., 2017. Ecosystem services and plant physiological status during endophyte-assisted phytoremediation of metal contaminated soil. Sci. Total Environ. 584–585, 329–338. Burken, J.G., Schnoor, J.L., 1996. Phytoremediation: plant uptake of atrazine and role of root exudates. J. Environ. Eng. 122, 958–963. Campos, V.M., Merino, I., Casado, R., Pacios, L.F., Gómez, L., 2008. Review - Phytoremediation of organic pollutants. Span. J. Agric. Res. 6, 38–47. Chaney, R.L., Malikz, M., Li, Y.M., Brown, S.L., Brewer, E.P., Angle, J.S., Bake, A.J.M., 1997. Phytoremediation of soil metals. Curr. Opin. Biotechnol. 8, 279–284. Chaney, R.L., Broadhurst, C.L., Centofanti, T., 2010. Phytoremediation of soil trace elements. In: Hooda, P.S. (Ed.), Trace Elements in Soils. John Wiley & Sons, Chichester, pp. 311–352. Chauhan, S., Das, M., Nigam, H., Pandey, P., Swati, P., Tiwari, A., Yadav, M., 2015. Implementation of phytoremediation to remediate heavy metals from tannery waste: A review. Adv. Appl. Sci. Res. 6 (3), 119–128. Conceição Gomes, M.A., Hauser-Davis, R.A., Nunes de Souza, A., Vitória, A.P., 2016. Metal phytoremediation: General strategies, genetically modified plants and applications in metal nanoparticle contamination. Ecotoxicol. Environ. Safety 134, 133–147. Conte, P., Agretto, A., Spaccini, R., Piccolo, A., 2005. Soil remediation: humic acids as natural surfactants in the washings of highly contaminated soils. Environ. Pollut. 135, 515–522. Conte, F., Copat, C., Longo, S., Oliveri Conti, G., Grasso, A., Arena, G., Dimartino, A., Brundo, M.V., Ferrante, M., 2016. Polycyclic aromatic hydrocarbons in Haliotis tuberculata (Linnaeus, 1758) (Mollusca, Gastropoda): Considerations on food safety and source investigation. Food Chem. Toxicol. 94, 57–63. Copat, C., Bella, F., Castaing, M., Fallico, R., Sciacca, S., Ferrante, M., 2012. Heavy metals concentrations in fish from Sicily (Mediterranean Sea) and evaluation of possible health risks to consumers. Bull. Environ. Contam. Toxicol. 88, 78–83. Crea, F., Foti, C., Milea, D., Sammartano, S., 2013. (Chapter 3). Speciation of cadmium in the environment. In: Sigel, Astrid, Sigel, Helmut, Sigel, Roland K.O. (Eds.), Cadmium: from Toxicology To Essentiality. Metal Ions in Life Sciences, Vol. 11. Springer, pp. 63–83. Cullen, W.R., Reimer, K.J., 1989. Arsenic speciation in the environment. Chem. Rev. 89 (4), 713–764. Cunningham, S.D., Ow, D.W., 1996. Promises and prospects for phytoremediation. Plant Physiol. 110, 715–719. Dadar, M., Adel, M., Ferrante, M., Nasrollahzadeh Saravi, H., Copat, C., Oliveri Conti, G., 2016. Potential risk assessment of trace metals accumulation in food, water and edible tissue of rainbow trout (Oncorhynchus mykiss) farmed in Haraz River, northern Iran. Toxin Rev. 1–6. http://dx.doi.org/10.1080/ 15569543.2016.1217023. Das, S., Raj, R., Mangwani, N., Dash, H.R., Chakraborty, J., 2014. Heavy metals and hydrocarbons: adverse affects and mechanism of toxicity. Microb. Biodegrad. Bioremediat..

324

A. Cristaldi et al. / Environmental Technology & Innovation 8 (2017) 309–326

Deng, Z., Cao, L., 2017. Fungal endophytes and their interactions with plants in phytoremediation: A review. Chemosphere 168, 1100–1106. Deniau, A.X., Schat, H., Aarts, M.G.M., 2007. Genetics and genomics of the heavy metal hyperaccumulator model species thlaspi caerulescens. Genes Genomes Genomics 1 (1), 81–88. Duffus, J.H., 2003. ‘‘Heavy Metals’’ - A meaningless term? (IUPAC Technical Report). Pure Appl. Chem. 75 (9), 1357. Duran, N., Marcato, P.D., De Souza, G.I.H., Alves, O.L., Esposito, E., 2007. Antibacterial effect of silver nanoparticles produced by fungal process on textile fabrics and their effluent treatment. J. Biomed. Nanotech. 3, 203–208. Ernst, W.H.O., 2006. Evolution of metal tolerance in higher plants. For. Snow Landsc. Res. 80 (3), 251–274. Fernandez, S., Poschenrieder, C., Marcenò, C., Gallego, J.R., Jimenez-Gamez, D., Bueno, A., Afif, E., 2017. Phytoremediation capability of native plant species living on Pb-Zn and Hg-As mining wastes in the Cantabrian range, north of Spain, Vol. 174, March 2017, pp. 10–20. Fiorentino, N., Fagnano, M., Ventorino, V., Pepe, O., Zoina, A., Impagliazzo, A., Spigno, P., 2012. Assisted phytoextraction of heavy metals: compost and Trichoderma effects on giant reed uptake and soil quality. Plant Soil Environ.. Fiorentino, N., Fagnano, M., Adamo, P., Impagliazzo, A., Mori, M., Pepe, O., Ventorino, V., Zoina, A., 2013. Assisted phytoextraction of heavy metals: compost and trichoderma effects on giant reed (Arundo donax L) uptake and soil N-cycle microflora. Ital. J. Agron. 8:e29. Fletcher, J., et al., 1995. Chemosphere 28:881, 31:3009. Flowers, T., Colmer, T.D., 2015. Plant salt tolerance: adaptations in halophytes. Ann. Botany 115, 327–331. http://dx.doi.org/10.1093/aob/mcu267. Available online at www.aob.oxfordjournals.org. Fontana, S., Wahsha, M., Bini, C., 2010. Preliminary observations on heavy metal contamination in soils and plants of an abandoned mine in Imperina Valley (Italy) Agrochimica, Vol. LIV - N 4, July–August 2010. French, C.E., Rosser, S.J., Davies, G.J., Nicklin, S., Bruce, N.C., 1999. Biodegradation of explosives by transgenic plants expressing pentaerythritol tetranitrate reductase. Nat. Biotechnol. 17, 491–494. Fumagalli, P., Comolli, R., Ferr, C., Ghiani, A., Gentili, R., Citterio, S., 2014. The rotation of white lupin (lupinus albus l) with metal-accumulating plant crops: a strategy to increase the benefits of soil phytoremediation. J. Environ. Manage. 145, 35e42. Gerhardt, K.E., Huang, X.D., Glick, B.R., Greenberg, B.M., 2009. Phytoremediation and rhizoremediation of organic soil contaminants: Potential and challenges. Plant Sci. 176, 20–30. Glass, D.J., 1999. Economic potential of phytoremediation. In: Raskin, I., Ensley, B.D. (Eds.), Phytoremediation of Toxic Metals: Using Plants To Clean Up the Environment. John Wiley & Sons Inc., New York, NY, pp. 15–31. Goswami, S., Das, S., 2016. Copper phytoremediation potential of Calendula officinalis L and the role of antioxidant enzymes in metal tolerance. Ecotoxicol Environ. Saf. 126, 211–218. http://dx.doi.org/10.1016/j.ecoenv.2015.12.030. Epub 2016 Jan 7. Gou, Z.H., Miao, X.F., 2010. Growth changes and tissues anatomical characteristics of giant reed (Arundo donax L,) in contaminated soil with arsenic, cadmium and lead. J. Cent. South Univ. Technol. 17, 770–777. Grman, H., Velikonja-Bolta, S., Vodnik, D., Kos, B., Letan, D., 2001. EDTA enhanced heavy metal phytoextraction: metal accumulation, leaching and toxicity. Plant Soil 235, 105–114. Gutiérrez-Ginés, M.J., Hernández, A.J., Pérez-Leblic, M.I., Pastor, J., Vangronsveld, J., 2014. Phytoremediation of soils co-contaminated by organic compounds and heavy metals: Bioassays with Lupinus luteus L. and associated endophytic bacteria. J. Environ. Manag. 143, 197–207. Hazrat, A., Ezzat, K., Muhammad, A.S., 2013. Phytoremediation of heavy metal–Concepts and applications. In: Chemosphere, Vol. 91. Elsevier. Hernberg, S., 2000. Lead Poisoning in a Historical Perspective. Amer. J. Ind. Med. Rep. 38 (3), 244–254. Horta, A., Malone, B., Stockmann, U., Minasny, B., Bishop, T.F.A., McBratney, A.B., Pallasser, R., Pozza, L., 2015. Potential of integrated field spectroscopy and spatial analysis for enhanced assessment of soil contamination: A prospective review. Geoderma 241–242, 180–209. IARC (International Agency for Research on Cancer), 1987. Polynuclear Aromatic Compounds. Part 1. Chemical, Environmental and Experimental Data. In: IARC Monographs on the Evaluation of Carcinogenic Risks to Humans, vol. 32, World Health Organization, Lyon, France, pp. 419–430. Jacques, R.J.S., Okeke, B.C., Bento, F.M., Peralba, M.C.R., Camargo, F.A.O., 2007. Characterization of a polycyclic aromatic hydrocarbon-degrading microbial consortium from a petrochemical sludge landfarming site. Biorem. J. 11, 1–11. Jacques, R.J.S., Okeke, B.C., Bento, F.M., Teixeira, A.S., Peralba, M.C.R., Camargo, F.A.O., 2008. Microbial Consortium bioaugmentation of a polycyclic aromatic hydrocarbons contaminated soil. Bioresour. Technol. 99, 2637–2643. Jang, K.Y., Cho, S.M., Seok, S.J., Kong, W.S., Kim, G.H., Sung, J.M., 2009. Screening of biodegradable function of indigenous ligno-degrading mushroom using dyes laccase of Trametes versicolor in the presence of different mediator compounds. Appl. Microbiol. Biot. 46, 313–317. http://dx.doi.org/10.1007/ s002530050823. Jia, H., Wang, H., Lua, H., Jiang, S., Dai, M., Liu, J., Yan, C., 2016. Rhizodegradation potential and tolerance of Avicennia marina (Forsk,) Vierh in phenanthrene and pyrene contaminated sediments. Mar. Pollut. Bull. 110, 112–118. Jiang, Y., Lei, M., Duan, L., Longhurst, P., 2015. Integrating phytoremediation with biomass valorisation and critical element recovery: A UK contaminated land perspective. Biomass Bioenergy 83, 328–339. Jing, Y., He, Z., Yang, X., 2007. Role of soil rhizobacteria in phytoremediation of heavy metal contaminated soils. J. Zhejiang Univ. Sci. B 8 (3), 192–207. Johnson, D.L., Anderson, D.R., Mcgrath, S., 2005. Soil microbial response during the phytoremediation of a PAH contaminated soil. Soil Biol. Biochem. 37, 2334–2336. Jones, K.C., Grimmer, G., Jakob, J., Johnston, A.E., 1989. Changes in the polynuclear aromatic hydrocarbon content of wheat frain and pasture grassland over last century from one site in the UK. Sci. Total Environ. 78, 117–130. Kabata-Pendias, A., 1989. Trace Elements in the Soil and Plants. CRC Press, Boca Raton, FL. Kabata-Pendias, A., 2001. Trace Elements in the Soil and Plants. CRC Press, Boca Raton, FL. Kadri, T., Rouissi, T., Brar, S.K., Cledon, M., Sarma, S., Verma, M., 2015. Biodegradation of polycyclic aromatic hydrocarbons (PAHs) by fungal enzymes: A review. J. Environ. Sci. 83. Kaimi, E., Mukaidani, T., Miyoshi, S., Tamaki, M., 2006. Ryegrass enhancement of biodegradation in dieselcontaminated soil. Environ. Exp. Bot. 55, 110–119. Kavamura, V.N., Esposito, E., 2010. Biotechnological strategies applied to the decontamination of soils polluted with heavy metals. Biotechnol. Adv. 28, 61–69. Kawahigashi, H., 2009. Transgenic plants for phytoremediation of herbicides. Biotechnology 20, 225–230. Kim, S.K., Park, C.B., Koo, Y.M., Yun, H.S., 2003. Biosorption of cadmium and copper ions by Trichoderma reesei RUT C30. J. Ind. Eng. Chem. 9, 403–406. Koptsik, G.N., 2014. Problems and prospects concerning the phytoremediation of heavy metal polluted soils: a review. Eurasian Soil Sci. 47, 923–939. Kos, B., Grčman, H., Leštan, D., 2003. Phytoextraction of lead, zinc and cadmium from soil by selected plants. Plant Soil Environ. 49 (12), 548–553. Kumar, A., Bisht, B.S., Joshi, V.D., Dhewa, T., 2011. Review on bioremediation of polluted environment: A management tool. Int. J. Environ. Sci. 1 (6), 2011. Kumar, M., Philip, L., 2006. Bioremediation of endosulfan contaminated soil and water –optimization of operating conditions in laboratory scale reactors. J. Hazard. Mater. 136, 354–364. Lasat, M.M., 2000. Phytoextraction of metals from contaminated soil: a review of plant/soil/metal interaction and assessment of pertinent agronomic issues. J. Hazard. Subst. Res. 2 (5), 1–25. Lee, M., Yang, M., 2010. Rhizofiltration using sunflower (Helianthus annuus L) and bean (Phaseolus vulgaris L. var. vulgaris) to remediate uranium contaminated groundwater. J. Hazard. Mater. 173, 589–596.

A. Cristaldi et al. / Environmental Technology & Innovation 8 (2017) 309–326

325

Lei, J., Sansregret, J.L., Cyr, B., 1994. Biopiles and biofilters combined for soil cleanup. Pollut. Eng. 26, 56–58. Leonard, T.L., Taylor, G.E., Gustin, M.S., Fernandez, G.C.J., 1998. Mercury and plants in contaminated soils: 1. Uptake, partitioning, and emission to the atmosphere. Environ. Toxicol. Chem. 17, 2063–2071. Leung, H.M., Wang, Z.W., Ye, Z.H., Yung, K.L., Peng, X.L., Cheung, K.C., 2013. Interactions between arbuscular mycorrhizae and plants in phytoremediation of metal-contaminated soils: A review. Pedosphere 23 (5), 549–563. Li, Y.M., Chaney, R., Brewer, E., Roseberg, R., Angle, J.S., Baker, A., Reeves, R., Nelkin, J., 2003. Development of a technology for commercial phytoextraction of nickel: economic and technical considerations. PlantSoil 249, 107–115. Liu, R., Xiao, N., Wei, S., Zhao, L., An, J., 2014. Rhizosphere effects of PAH-contaminated soil phytoremediation using a special plant named Fire Phoenix. Sci. Total Environ. 473–474, 350–358. Loutseti, S., Danielidis, D.B., Economou-Amilli, A., Katsaros, C., Santas, R., Santas, P., 2009. The application of a micro-algal/bacterial biofilter for the detoxification of copper and cadmium metal wastes. Bioresour. Technol. 100, 2099–2105. Lu, H., Zhang, Y., Liu, B., Liu, J., Ye, J., Yan, C., 2011. Rhizodegradation gradients of phenanthrene and pyrene in sediment of mangrove (Kandelia candel) (L, Druce). J. Hazard. Mater. 196, 263–269. Mahar, A., Wang, P., Ali, A., Awasthi, M.K., Lahori, A.H., Wang, Q., Li, R., Zhang, Z., 2016. Challenges and opportunities in the phytoremediation of heavy metals contaminated soils: A review. Ecotoxicol. Environ. Safety 126, 111–121. Maila, M., Randima, P., Cloete, T.E., 2005. . Multispecies and monoculture rhizoremediation of polycyclic aromatic hydrocarbons (PAHs) from the soil. Int. J. Phytoremediat. 7, 87–98. Mancini, O., Cuccu, W., Molinari, M., 2005. Landfarming and phytoremediation in an urban area: a case study. In: situ and on-site bioremediation, Proceedings of the International In Situ and On-Site Bioremediation Symposium, 8th, Baltimore, MD, United States 2005 June 6–9. Manno, E., Varrica, D., Dongarrà, G., 2006. Metal distribution in road dust samples collected in an urban area close to a petrochemical plant at Gela, Sicily. Atmos. Environ. 40, 5929–5941. Marchiol, L., Fellet, G., Pošćić, F., Zerbi, G., 2011. A decade of research on phytoremediation in north east Italy: lessons learned and future directions. In: Golubev, Ivan A. (Ed.), Handbook of Phytoremediation. Nova Science Publishers, Inc., ISBN: 978-1-61728-753-4 (Chapter 4). Margesin, R., Schinner, F., 1998. Low-temperature bioremediation of a waste water contaminated with anionic surfactants and fuel oil. Appl. Microbiol. Biotechnol. 49, 482–486. Margesin, R., Schinner, F., 2001. Bioremediation (natural attenuation and biostimulation) of diesel-oil-contaminated soil in an Alpine glacier skiing area. Appl. Environ. Microbiol. 67, 3127–3133. Marinaccio, A., Belli, S., Binazzi, A., Scarselli, A., Massari, S., Bruni, A., Conversano, M., Crosignani, P., Minerba, A., Zona, A., Comba, P., 2011. Residential proximity to industrial sites in the area of Taranto (Southern Italy), A case-control cancer incidence study. Ann. Ist. Super. Sanità 47 (2), 192–199. Marmiroli, N., Maestri, E., Antonioli, G., Conte, C., Monciardini, P., Marmiroli, M., Mucchino, C., 1999. Application of synchrotron radiation X-ray fluorescence (µ-SRXF) and X-ray microanalysis (SEM/EDX) for the quantitative and qualitative evaluation of trace element accumulation in woody plants. Int. J. Phytoremed. 1 (2). Marmiroli, N., Marmiroli, M., Maestri, E., 2006. Phytoremediation and Phytotechnologies: A Review for the Present and the Future. In: Soil and Water Pollution Monitoring, Protection and Remediation, Springer, pp. 3–23. Marquès, M., Mari, M., Audì-Mirò, C., Sierra, J., Soler, A., Nadal, M., Domingo, J.L., 2016. Photodegradation of polyciclic aromatic hydrocarbons in soils under a climate change base scenario. Chemosphere 148, 495–503. Mazza, A., Senior, K., 2004. In Italia il ‘‘triangolo della morte’’ è collegato alla crisi dei rifiuti. Lancet Oncol. 5, settembre 2004. McCutcheon, S.C., Jørgensen, S.E., 2008. Phytoremediation. Ecol. Eng. Phytorem. 2751–2766. Miani, N., Skert, N., Giorgini, L., Falomo, J., Grahonja, R., 2007. Monitoraggio di IPA aerodispersi nella provincia di Trieste tramite Moss-Bags e quadrelli come accumulatori. Relazione ARPA FVG - Dipartimento di Trieste, 2007. Miri, M., Derakhshan, Z., Allahabadi, A., Ahmadi, E., Oliveri Conti, G., Ferrante, M., Ebrahimi Aval, H., 2016. Mortality and morbidity due to Exposure to Outdoor Air Pollution in Mashhad Metropolis, Iran. The AirQ Model Approach. Environ. Res. 151, 451–457. http://dx.doi.org/10.1016/j.envres.2016.07. 039. Mishra, S., Jyot, J., Kuhad, R.C., Lal, B., 2001. Evaluation of inoculum addition to stimulate in situ bioremediation of oily-sludge-contaminated soil. Appl. Environ. Microbiol. 67, 1675–1681. Mohn, W., Radziminski, C., Fortin, M.C., Reimer, K., 2001. On Site Bioremediation of Hydrocarbon-Contaminated Arctic Tundra Soils in Inoculated Biopiles. Appl. Microbiol. Biotechnol. 57, 242–247. Mollea, C., Bosco, F., Ruggeri, B., 2005. Fungal biodegradation of naphthalene: microcosms studies. Chemosphere 60, 636–643. Mori, T., Watanabe, M., Taura, H., Kuno, T., Kamei, I., Kondo, R., 2015. Degradation of chlorinated dioxins and polycyclic aromatic hydrocarbons (PAHs) and remediation of PAH-contaminated soil by the entomopathogenic fungus, Cordyceps militaris. J. Environ. Chem. Eng. 3, 2317–2322. Mudhoo, A., Sharma, S.K., Lin, Z.Q., Dhankher, O.P., 2010. Phytoremediation of arsenic-contaminated environment an overview. In: Sharma, A., Mudhoo, S.K. (Eds.), Green Chemistry for Environmental Sustainability, Vol. 127. Taylor and Francis Group, Boca ratan London, New York. Newman, L.A., Reynolds, C.M., 2004. Phytodegradation of organic compounds. Curr. Opin. Biotechnol. 15, 225–230. Nunes da Silva, M., Mucha, A.P., Rocha, A.C., Silva, C., Carli, C., Gomes, C.R., Almeida, C.M.R., 2014. Evaluation of the ability of two plants for the phytoremediation of Cd in salt marshes. Estuar. Coast. Shelf Sci. 141, 78–84. Pacyna, E.G., Pacyna, J.M., Steenhuisen, F., Wilson, S., 2006. Global anthropogenic mercury emission inventory for 2000. Atmos. Environ. 40 (22), 4048. Pouladi, S.F., Anderson, B.C., Wootton, B., Rozema, L., 2016. Evaluation of phytodesalination potential of vegetated bioreactors treating greenhouse effluent. Water 8, 233. http://dx.doi.org/10.3390/w8060233. Prasad, M.N.V., 2007. Sunflower (Helinathus annuus L.) - A potential crop for environmental industry. HELIA, 30, Nr. 46, 167–174, 2007. Pulford, I.D., Watson, C., 2003. Phytoremediation of heavy metal-contaminated land by trees - a review. Environ. Int. 29, 529–540. Rajakaruna, N., Tompkins, K.M., Pavicevic, P.G., 2006. Phytoremediation: an affordable green technology for the clean-up of metal contaminated sites in Sry Lanka. Cey. J. Sci. (Biol. Sci.) 35 (1), 25–39. Roy, S., Labelle, S., Mehta, P., Mihoc, A., Fortin, N., Masson, C., Leblanc, R., Cha, G., Sura, C., Gallipeau, C., Olsen, C., Delisle, S., Labrecque, M., Greerl, C.W., 2005. Phytoremediation of heavy metal and PAH-contaminated brownfield sites. Plant Soil 272, 277–290. Saadoun, I.M.K., Al-Ghzawi, Z.D., 2005. Bioremediation of petroleum contamination. Biorem. Aquat. Terr. Ecosys. 173–212. Sakai, Y., Ma, Y., Xu, C., Wu, H., Zhu, W., Yang, J., 2012. Phytodesalination of a salt-affected soil with four halophytes in China. J. Arid Land Stud. 22–1, 17–20. San Miguel, A., Ravanel, P., Raveton, M., 2013. A comparative study on the uptake and translocation of organochlorines by Phragmites australis. J. Hazard. Mater. 244–245, 60–69 15 January 2013. Sari, A., Tuzen, M., 2009. Kinetic and equilibrium studies of biosorption of Pb(II) and Cd(II) from aqueous solution by macrofungus (Amanita rubescens) biomass. J. Hazard. Mater. 164, 1004–1011. Schnoor, J.L., 1997. Phytoremediation. Ground-Water Remediation Technologies Analysis Center. E Series: TE-98–01 Phytoremediation. Schwitzguébel, J.P., van der Lelie, D., Baker, A., Glass, D.J., Vangronsveld, J., 2002. Phytoremediation: European and American Trend Successes, Obstacles and Needs. JSS–J Soils Sediments (OnlineFirst).

326

A. Cristaldi et al. / Environmental Technology & Innovation 8 (2017) 309–326

Sciacca, S., Oliveri Conti, G., 2009. Mutagens and carcinogens in drinking water. Mediterr. J. Nutr. Metabol. 2, 157–162. http://dx.doi.org/10.1007/s12349-009-0052--5. Sharma, P., Pandey, S., 2014. Status of phytoremediation in world scenario. Int. J. Environ. Bioremediat. iodegrad. 2 (4), 178–191. Shayler, H., McBride, M., Harrison, E., 2009. Sources and Impacts of Contaminants in Soils. Cornell Waste Management Institute. Department of Crop & Soil Sciences. http://cwmi.css.cornell.edu. Shimp, J.F., Tracy, J.C., Davis, L.C., Lee, E., Huang, W., Erickson, L.E., 1993. Beneficial effects of plants in the remediation of soil and groundwater contaminated with organic materials. Crit. Rev. Environ. Sci. Technol. 23, 41–77. Shiri, M., Rabhi, M., Abdelly, C., Amrani, A. El., 2015. The halophytic model plant Thellungiella salsuginea exhibited increased tolerance to phenanthreneinduced stress in comparison with the glycophitic one Arabidopsis thaliana: Application for phytoremediation. Ecol. Eng. 74, 125–134 January 2015. Souza, E.C., Vessoni-Penna, T.C., de Souza Oliveira, R.P., 2014. Biosurfactant-enhanced hydrocarbon bioremediation: An overview. Int. Biodeterior. Biodegrad. 89, 88–94. Sreelal, G., Jayanthi, R., 2017. Review on phytoremediation technology for removal of soil contaminant. Indian J. Sci. Res. 14 (1), 127–130. Sreeram, K., Ramasami, T., 2003. Sustaining tanning process through conservation, recovery and better utilization of chromium. Resour. Conserv. Recy. 38 (3), 185–212. Stormo, K.E., Crawford, R.L., 1992. Preparation of encapsulated microbial cells for environmental applications. Appl. Environ. Microbiol. 58, 727–730. Stroud, J.L., Paton, G.I., Semple, K.T., 2007. Microbe-aliphatic hydrocarbon interactions in soil: implications for biodegradation and bioremediation. J. Appl. Microbiol. 102, 1239–1253. Sugiura, Y., Michihiro, S., Yoshimune, O., Hajime, O., Tsutomu, K., Chisato, T., 2016. Evaluation of radiocesium concentrations in new leaves of wild plants two years after the Fukushima Dai-ichi Nuclear Power Plant accident. J. Environ. Radioact. 160, 8–24 August 2016. Sui, H., Li, X., Jiang, B., Huang, G., 2007. Simulation of remediation of multiple organic contaminantssystem by bioventing. Huagong Xuebao 58, 1025–1031 (Chinese Edition). Suko, T., Fujikawa, T., Miyazaki, T., 2006. Transport phenomena of volatile solute in soil during bioventing technology. J. ASTM Int. 3. Susarla, S., Medina, V.F., McCutcheon, S.C., 2002. Phytoremediation: An ecological solution to organic chemical contamination. Ecol. Eng. 18, 647–658. Tahir, U., Yasmin, A., Khan, U.H., 2015. Phytoremediation: Potential flora for synthetic dyestuff metabolism. J. King Saud Univ.–Sci.. Taylor, R.T., Duba, A.G., Durham, W.B., Hanna, M.L., Jackson, K.J., Jovanovich, M.C., 1992. In situ bioremediation of trichloroethylene-contaminated water by a resting-cell methanotrophic microbial filter, Conference of the International in situ bioremediation, Ontario (Canada) 1992, pp. 20–24. Tchounwou, P.B., Yedjou, C.G., Patlolla, A.K., Sutton, D.J., 2014. Heavy metals toxicity and the environment. NIH Public Access. Vamerali, T., Bandiera, M., Coletto, L., Zanetti, F., Dickinson, N.M., Mosca, G., 2009. Phytoremediation trials on metal- and arsenic-contaminated pyrite wastes (Torviscosa, Italy). Environ. Pollut. 157 (2009), 887. Van Oosten, M.J., Maggio, A., 2014. Functional biology of halophytes in the phytoremediation of heavy metal contaminated soils. Environ. Exp. Bot. 111, 135–146. Van Sprang, P., Vangheluwe, M., Van Hyfte, A., Heijerick, D., Vandenbroele, M., Verdonck, F., 2008. Voluntary risk assessment of copper, copper (II) sulphate pentahydrate, copper (I)oxide, copper(II)oxide, dicopper chloride trihydroxide. Available at: European Chemicals Agency (ECHA), http://echa.europa. eu/it/. Venkata Mohan, S., Kisa, T., Ohkuma, T., Kanaly, R.A., Shimizu, Y., 2006. Bioremediation technologies for treatment of PAH-contaminated soil and strategies to enhance process efficiency. Rev. Environ. Sci. Biotechnol. 5, 347–374. Vidali, M., 2001. Bioremediation. An Overview. Pure Appl. Chem. 73 (7), 1163–1172. Villacieros, M., Whelan, C., Mackova, M., Molgaard, J., Sánches-Contreras, M., Lloret, J., 2005. Polychlorinated biphenyl rhizoremediation by Pseudomonas fluorescens F113 derivatives using a Sinorhizobium meliloti nod system to drive bph gene expression. Appl. Environ. Microbiol. 71, 2687–2694. Vinichuk, M., Martensson, A., Rosen, K., 2013. J. Environ. Radioact. 126, 14–19 December 2013. Visoottiviseth, P., Francesconi, K., Sridokchan, W., 2002. The potential of Thai indigenous plant species for the phytoremediation of arsenic contaminated land. Environ. Pollut. 118, 453–461. Wang, Y., Stauffer, C., Keller, C., 2005. Changes in Hg fractionation in soil induced by willow. Plant Soil 275, 67–75. Wang, J., Feng, X., Anderson, C.W.N., Xing, Y., Shang, L., 2012. Remediation of mercury contaminated sites–A review. J. Hazard. Mater. 221–222, 1–18. Wani, B.A., Khan, A., Bodha, R.H., 2011. Salix: a viable option for phytoremediation. Rev. African J. Environ. Sci. Technol. 5 (8), 567–571 Available online at http://www.academicjournals.org/AJEST ISSN 1996-0786. Winquist, E., Björklöf, K., Schultz, E., Räsänen, M., Salonen, K., Anasonye, F., Cajthaml, T., Steffen, K.T., Jørgensen, K.S., Tuomela, M., 2013. Bioremediation of PAH-contaminated soil with fungi - From laboratory to field scale. Int. Biodeterior. Biodegrad. 86, 238–247. Xiao, N., Liu, R., Jin, C., Dai, Y., 2015. Efficiency of five ornamental plant species in the phytoremediation of polycyclic aromatic hydrocarbon (PAH)contaminated soil. Ecol. Eng. 75, 384–391. Yang, S.X., Liao, B., Yang, Z.H., Chai, L.Y., Li, J.T., 2016. Revegetation of extremely acid mine soils based on aided phytostabilization: A case study from southern China. Sci. Total Environ. 562, 427–434. Yee, D.C., Maynard, J.A., Wood, T.K., 1998. Rhizoremediation of trichloroethylene by a recombinant, root-colonizing pseudomonas fluorescens strain expressing toluene orthomonooxygenase constitutively. Appl. Environ. Microbiol. 64, 112–118. Yin, H., Tan, Q., Chen, Y., Lv, G., He, D., Hou, X., 2011. Polycyclic aromatic hydrocarbons (PAHs) pollution recorded in annual rings of gingko (Gingko biloba L,): Translocation, radial diffusion, degradation and modeling. Microchem. J. 97, 131–137. Zenker, M.J., Brubaker, G.R., Shaw, D.J., Knight, S.R., 2005. Passive bioventing pilot study at a former petroleum refinery, In Situ and On-Site Bioremediation. In: Proceedings of the International In Situ and On-Site Bioremediation Symposium, 8th, Baltimore, MD, United States 2005 June 6–9. Zhang, H., Zheng, L.C., Yi, X.Y., 2009. Remediation of soil co-contaminated with pyrene and cadmium by growing maize (Zea mays L). Int. J. Environ. Sci. Tech. 6, 249–258. Zhang Yu, X., Dong Gu, J., 2006. Uptake, metabolism, and toxicity of methyl tert-butyl ether (MTBE) in weeping willows. J. Hazard. Mater. 137 (3), 1417–1423 October 2006. Zhao, L., Li, T., Yu, H., Zhang, X., Zheng, Z., 2016. Effects of [S,S]-ethylenediaminedisuccinic acid and nitrilotriacetic acid on the efficiency of Pb phytostabilization by Athyrium wardii (Hook.) grown in Pb-contaminated soils. J. Environ. Manag. 182, 94–100. Zorrig, W., Rabhi, M., Frechichi, S., Smaoui, A., Abdelly, C., 2012. Phytodesalination: a solution for salt-affected soils in arid and semi-arid regions. J. Arid Land Studies 22–1, 299–302.

Sitography US EPA, 2001. United States Environmental Protection Agency. https://search.epa.gov/epasearch/epasearch?querytext=bioremediation&areaname= &areacontacts=&areasearchurl=&typeofsearch=epa&result_template=2col.ftl.