J Environ Sci Public Health 2020; 4 (2): 112-133 DOI: 10.26502/jesph.96120089

Review Article

Biological Methods of Polluted Remediation for an Effective Economically-Optimal Recovery of and Services

Rafael G. Lacalle1*, José M. Becerril1, Carlos Garbisu2

1Department of Biology and , University of the Basque Country (UPV/EHU), P.O. Box 644, E-48080 Bilbao, Spain 2Department of Conservation of Natural Resources, NEIKER-Basque Institute for Agricultural Research and Development, Basque Research and Technology Alliance (BRTA), Parque Científico y Tecnológico de Bizkaia, P812, 48160 Derio, Spain

*Corresponding Author: Dr. Rafael G. Lacalle, Department of Plant Biology and Ecology, University of the Basque Country (UPV/EHU), Bilbao, Spain, Email : [email protected]

Received: 17 April 2020; Accepted: 23 April 2020; Published: 05 June 2020

Citation: Rafael G. Lacalle, José M. Becerril, Carlos Garbisu. Biological methods of polluted soil remediation for an effective economically-optimal recovery of soil health and ecosystem services. Journal of Environmental Science and Public Health 4 (2020): 112-133.

Abstract infeasible and/or environmentally-destructive Soil is one of our most important resources as it techniques. In consequence, in the last years and supports many critical ecological functions and decades, more sustainable and innovative biological ecosystem services. Nonetheless, due to a wide methods of soil remediation (belonging to the variety of environmentally-unsustainable anthropic sometimes called “gentle remediation options”) are activities, sadly, our are currently contaminated being developed in an attempt to combine: (i) an at a global scale with a myriad of potentially toxic efficient removal of soil contaminants (in terms of a inorganic and organic compounds. Regrettably, most, decrease of total and/or bioavailable contaminant if not all, traditional physicochemical methods of soil concentrations), (ii) a reduction of soil ecotoxicity, remediation are frequently based on economically- (iii) the legally- and ethically-required minimization

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J Environ Sci Public Health 2020; 4 (2): 112-133 DOI: 10.26502/jesph.96120089 of risk for environmental and human health, and, of European contaminated soils, respectively. concomitantly, (iv) a recovery of soil health and (v) Chlorinated hydrocarbons appear to a lesser extent associated ecosystem services. Ideally, any soil (8%) but still are a most relevant issue [3]. remediation method should not only decrease the Frequently, contaminated sites are characterized by concentration of soil contaminants below regulatory the simultaneous presence of different contaminants limits but should also recover soil health and [4, 5], thus potentially increasing their toxicity and alongside the provision of essential ecosystem environmental impact, and hampering the application services. Unquestionably, all this must be achieved in of soil remediation technologies [6]. Soil metal(oid) full compliance with the binding environmental contamination often results from agricultural, mining regulations and, most importantly, via the and metallurgical activities, while accidental spills implementation of economically-feasible (preferably, and/or industrial activities are recurrently the source profitable) strategies of soil remediation. of soil organic contaminants. Furthermore, waste discharge and waste treatment processes are a major Keywords: Bioremediation; Contamination; source of both types of soil contaminants. The U.S Phytoremediation; Pollution; ; Environmental Protection Agency (USEPA) reported Vermiremediation that 40% of the hazardous waste sites are contaminated with both organic and metal(oid) 1. contaminants [7]. The soil is both a highly complex ecosystem and a non-renewable resource on a human time scale, which 2. Soil Health harbors a range of physical, chemical and biological Soil contamination, along with other degradation processes supporting key functions and essential processes, can negatively affect soil health [8], often ecosystem services. Likewise, soil is a dynamic living defined as “the capacity of a given soil to perform its system that serves as habitat for a myriad of functions as a living system capable of sustaining organisms (micro-, meso- and macrofauna) with biological , promoting environmental essential roles in nutrient cycling and the quality and maintaining plant and animal health” [9]. mineralization of organic matter [1]. Lamentably, But soil is a vastly complex environmental matrix different anthropic activities are responsible for the which performs numerous, sometimes conflicting, current state of soil degradation through erosion, functions from both an ecocentric and anthropocentric compaction, contamination, sealing, salinization and perspective, and, in consequence, many different loss of organic matter and [2]. Soil aspects must be taken into consideration in order to contamination, in particular, is nowadays a serious properly assess soil health. Most importantly, to environmental threat and challenge worldwide. In appropriately assess soil health: (i) physical, chemical Europe, the existence of 2.5 million potentially- and biological properties with potential as indicators contaminated sites has been estimated [3]. In these of soil functioning must always be included in the sites, the most common environmental contaminants assessment (after all, physical, chemical and are metal(oid)s and mineral oils, affecting 35 and 24% biological processes in the soil ecosystem are not

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J Environ Sci Public Health 2020; 4 (2): 112-133 DOI: 10.26502/jesph.96120089 independent but interactive processes); (ii) chemical, conditioned by soil physicochemical properties such (eco)toxicological and ecological approaches must be as pH, redox potential, moisture content, organic incorporated to the evaluation; (iii) the intended use matter content, content, the presence of anionic for the contaminated site must be taken into close compounds, etc. [13]. Regarding organic consideration, as the very concept of soil health is contaminants, their bioavailability and mobility somewhat teleological and subjective; (iv) the depend largely on their solubility, hydrophobicity and intrinsic temporal and spatial variability of the system interaction, through a variety of physicochemical (i.e., spatial heterogeneity, temporal dynamics), as processes, with the mineral and organic fraction of the well as the scale of both soil processes and the soil matrix, e.g. via sorption and complexation assessment itself, must be taken into account; and (v) mechanisms [12]. Therefore, it is recommended to the selection of a suitable (inevitably, often far from always include the determination of the bioavailable perfect) “healthy” reference soil, for comparison and fraction of the contaminants when assessing soil the establishment of target purposes, should be health and, in particular, during the selection of a soil identified. remediation option and when monitoring the effectiveness of the chosen remediation methodology. Soil physicochemical properties such as pH, redox Nonetheless, regrettably, there is no consensus about potential, organic matter content, texture, etc., are the best way to accurately estimate soil contaminant relevant parameters with potential as indicators of soil bioavailability. For metallic contaminants, the most health which can strongly alter contaminant widely accepted methodology is the use of chemical bioavailability and, hence, (eco)toxicity in soil. extractants like, for instance, inorganic salts, e.g.

Unfortunately, for most environmental legislations, NaNO3, (NH4)2SO4 and CaCl2 [14-16]. In any event, the total concentration of the contaminants is the key for a proper assessment of the impact of soil factor for the Environmental Risk Assessment (ERA) contaminants on soil health (Figure 1), apart from of contaminated soils. Nevertheless, such aspect (i.e., total and bioavailable contaminant concentrations, total concentration of soil contaminants) is not enough biological indicators are required, as they directly to properly assess or estimate the potential harmful reflect the impact of the contaminants on the soil biota impact of contaminants on soil functioning [10]. As a [10]. Among them, soil microbial properties are matter of fact, the mobility and bioavailability of soil particularly adequate for this purpose, as contaminants both play a determining role in their play a key role in many uptake by organisms and, therefore, their (eco)toxicity and the provision of ecosystem services, while [11, 12]. Contaminant bioavailability is possibly a quickly delivering ecologically relevant information much more relevant factor, compared to total that integrates many environmental factors [17, 18]. contaminant concentrations, for a proper soil Similarly, standardized (eco)toxicological bioassays protection and risk assessment, as it represents the with model organisms have been developed and fraction that can be taken up by soil organisms and/or proposed for soil (eco)toxicity studies, including, for be leached to other environmental compartments. instance, Eisenia fetida [19], Vibrio fisheri [20], Specifically, metal(oild) bioavailability is mainly Lactuca sativa [21] and Cucumis sativus [22].

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J Environ Sci Public Health 2020; 4 (2): 112-133 DOI: 10.26502/jesph.96120089

SOIL HEALTH ASSESSMENT

Physical and chemical Biological indicators indicators

Contaminant Biological (Eco)toxicity Soil properties concentrations communities bioassays

pH Total concentrations Biomass Plant bioassays

Available/mobile Animal Organic matter Activity concentrations bioassays

Microbial Biodiversity Redox potential, bioassays texture, nutrient contents, etc.

Figure 1: Soil health assessment.

3. From Physicochemical Techniques to with concomitant adverse effects on soil processes, Gentle Remediation Options functions and health [23]. On the other hand, the Traditionally, physicochemical methods, such as interaction between organic and inorganic excavation and transportation to a controlled landfill, contaminants in co-contaminated sites makes their incineration, chemical washing, vitrification, etc. [23], remediation by physicochemical techniques more have been used to remediate contaminated soils, complex [25]. However, many of these physicochemical methods of soil remediation have substantial disadvantages and Due to the abovementioned limitations of traditional limitations, such as their high-cost, which frequently physicochemical remediation technologies, in the last compromises their applicability [24], and, above all, decades a variety of biological and more sustainable the fact that they are often environmentally disruptive. remediation technologies, often termed Gentle Then, although their application can many times Remediation Options (GROs), have emerged (Figure effectively remove and/or immobilize the target 2). In contraposition to conventional physicochemical contaminants, in numerous cases the ecological status remediation techniques, GROs are commonly less of the remediated soil is not improved during the invasive and more respectful of the soil environment remediation process; on the contrary, the application and its biota [26]. Many of these GROs aim at of these traditional physicochemical methods often simultaneously (i) decrease the total and/or leads to a partial or total destruction of the soil biota bioavailable concentration of soil contaminants; (ii) recover soil functionality; and, sometimes, (iii)

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J Environ Sci Public Health 2020; 4 (2): 112-133 DOI: 10.26502/jesph.96120089 produce renewable resources for the bio-based particular, the combination of phytoremediation with economy [27, 28]. Gentle remediation options often a profitable crop production, i.e. phytomanagement, bring social, economic and environmental benefits by has great potential for the recovery of contaminated integrating sustainable remediation options (e.g., sites, while providing a range of economic and other bioremediation, phytoremediation, vermiremediation) (e.g., provision of ecosystem services) benefits. with the generation of economic revenues. In

GENTLE REMEDIATION OPTIONS

Phytoremediation Bioremediation Vermiremediation

Topsoil/Biopile Phytoextraction Natural attenuation remediation

Phytostabilization Bioaugmentation Deeper soil remediation

Phytodegradation Biostimulation Phytovolatilization

Figure 2: Gentle remediation options.

3.1 Phytoremediation often applied to soils contaminated with metals. The Phytoremediation has been defined as “the use of two most common phytoremediation strategies, i.e. and associated microbes to reduce the phytoextraction, phytostabilization, are described concentration and/or toxic effects of contaminants in below. the environment” [29]. Due to its low installation and maintenance costs, as well as its many environmental 3.1.1 Phytoextraction: Phytoextraction is a benefits, [30], this phytotechnology can be applied in phytotechnology that uses the capacity of some plants large field sites in which other remediation options to take up and translocate metal contaminants from are not cost-effective or practicable [31]. soil to aboveground plant tissues. Subsequently, the Phytoremediation techniques are suitable for the aerial part of the plants can be harvested and, finally, remediation of soils contaminated with both inorganic incinerated, with potential benefits in terms of energy and/or organic compounds; however, they are most production and/or the recovery of high-added value

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J Environ Sci Public Health 2020; 4 (2): 112-133 DOI: 10.26502/jesph.96120089 metals [32]. For an effective phytoextraction, the determined not only by contaminant concentrations in selection of appropriate metal-tolerant plant species is aboveground tissues, but also shoot biomass [40]. Due a crucial aspect. Plants can be classified in three to their faster growth rate, adaptability to categories depending on their strategy to cope with environmental stress and high biomass, herbaceous metals: (i) excluders, which actively limit metal plants are often preferred for phytoextraction uptake and can then immobilize the metal purposes, in comparison to shrubs or trees [41]. contaminants in the ; (ii) indicators, which Examples of plants with potential for phytoextraction maintain a metal concentration in their tissues that strategies are: sunflower (Helianthus annuus), hemp reflects soil metal concentrations; and (iii) (Cannabis sativa), and several species of the Brassica accumulators, which actively take up and translocate genus, such as Indian mustard (B. juncea), canola (B. metals from soil to their shoots, thus reaching metal napus) and turnip rape (B. rapa) [42-44]. concentrations in their aboveground tissues higher than those present in the contaminated soil. Inside this Unfortunately, phytoextraction has serious limitations last group, hyperaccumulators are extremely when it comes to its practical application in the field. specialized plants that can accumulate heavy metals in The major drawback for the successful application of their aboveground tissues at remarkably high this phytotechnology is the great amount of time concentrations (1-10%) [33, 34]. required to effectively extract the metals from the contaminated soil, particularly from those with Accumulators and hyperaccumulators have frequently medium and high levels of metal contamination [45]. been used for phytoextraction purposes. Noccaea Due to the low biomass characteristic of most caerulescens (f.k.a. Thlaspi caerulescens), for hyperaccumulators, as well as the low metal uptake of instance, has been widely studied due to its non-accumulator plants that show high biomass remarkable capacity to accumulate zinc and/or production, a great number of harvests are required cadmium in its shoots [35, 36]. Some other commonly for a successful phytoextraction. Other limitations of studied accumulators are Elsholtzia splendens phytoextraction are: (i) root depth, which narrows the (copper) [37], Sedum plumbizincicola (cadmium) [38] applicability of this phytotechnology to surface soils; and Chenopodium spp. (chromium, nickel, cadmium) (ii) lack of well-known agronomic practices; and (iii) [39]. (Hyper)accumulators are certainly adapted to the incapability of most plants to accumulate more environments with high metal concentrations, but than one metal [46]. their growth rate and biomass are generally low. Therefore, alternatively, non-accumulator plant Another relevant aspect that cannot be neglected species but which can produce more aboveground when applying phytoextraction strategies is the biomass, are easier to cultivate and harvest, and show bioavailability of the metal contaminant. When a better adaptability to prevailing environmental and applying this phytotechnology, it must always be climatic conditions, have also been used for taken into account that only a fraction of the total soil phytoextraction purposes [23]. After all, the metal will be available for uptake by plants [47], effectiveness of a phytoextraction process is which a priori is the only fraction that can be

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J Environ Sci Public Health 2020; 4 (2): 112-133 DOI: 10.26502/jesph.96120089 phytoextracted. Numerous studies have explored the soils such as an increase in organic matter content, utilization of chelating agents to increase metal nutrients and soil biological activity; protection from bioavailability in order to maximize phytoextraction ; improvement of ; etc. [57, efficiency by high biomass plants [48-50]. However, 58]. this technology, known as chelator-induced phytoextraction, has raised environmental concerns Apart from being metal tolerant, suitable plants for derived from the risk of metal to and phytostabilization should have an extensive root and/or negative effects of persistent system, produce a large amount of biomass, and show chelants on the soil biota [46,51,52]. In any case, it a low root-to-shoot metal translocation rate [59]. should be noted that if the goal of a given Many metal excluder plants, such as grasses (Agrostis phytoextraction initiative is only the removal of the stolonifera, Lolium perenne) and legumes (Trifolium bioavailable fraction of the metal contaminant, the repens, Medicago sativa, Ulex europaeus), have been time required for the process will be significantly effectively used to revegetate metal contaminated shorter, which is, as previously mentioned, the main soils for phytostabilization purposes [34, 60-62]. critique to phytoextraction [53]. Unlike for metal phytoextraction, shrubs and trees are commonly selected as suitable candidates for 3.1.2 Phytostabilization: Phytostabilization, focused phytostabilization initiatives. Indeed, due to their on metal immobilization in the rhizosphere, is a GRO capacity to stabilize metals in their massive root with great potential for those soils with moderate or systems, tree and shrub species (e.g., Populus spp., high levels of metal contamination. Such Salix spp.) have been widely used for immobilization can be achieved through metal phytostabilization purposes [63, 64]. Interestingly, the precipitation or absorption/adsorption in the plant use of trees can lower the risk of metal leaching by roots [26, 54]. Indeed, besides metal absorption reducing the downward flow of water due to their and/or adsorption in the root system, metal high rates of transpiration [63]. phytostabilization can also be achieved through the modification of the soil conditions: for instance, the The application of phytostabilization can be a root exudates of some plants have been reported to challenge in highly degraded soils which, apart from modify the rhizosphere pH and redox conditions, thus metal contamination, present other problems like provoking the precipitation or complexation of erosion, poor physical structure, shortage of essential potentially toxic metals [8, 55]. Thus, nutrients and organic matter, etc. [34]. These phytostabilization reduces the bioavailable fraction of problems are frequent in mine tailings and dumpsites, metals in soil [46]. By reducing the bioavailability hampering the establishment of a healthy plant cover and mobility of metals in soil, the risk of [65]. In this respect, for an effective phytostabilization contamination of groundwater by metal leaching is in highly degraded soils, the use of organic and/or reduced, as well as the entry of the metal inorganic amendments is often recommended to contaminants to the food chain [56]. Furthermore, a facilitate plant establishment and growth. This plant cover brings additional benefits to contaminated methodology is usually termed assisted

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J Environ Sci Public Health 2020; 4 (2): 112-133 DOI: 10.26502/jesph.96120089 phytostabilization, aided phytostabilization or practical application is the fact that current chemophytostabilization [59]. In aided environmental legislations are normally based on total phytostabilization, the promotion of plant growth can metal concentrations, not on bioavailable metal be achieved by raising soil pH, enhancing the organic concentrations, and since this phytotechnology cannot matter content, providing essential nutrients, reduce total metal concentrations below the reference increasing the water holding capacity, reducing metal critical values established by legislation, it is bioavailability, etc. [17, 66]. Besides, the utilization impractical from a legal point of view. of organic and inorganic amendments opens the door to the recycling of wastes, residues and byproducts 3.2 Phytomanagement from diverse origins, in a context of Circular Despite the number of research papers on Economy [67]. Some amendments commonly used in phytoremediation, its application at field scale is still aided phytostabilization studies are: animal slurry and limited. Some of the reasons for this phenomenon are, , paper mill sludge, sewage sludge, urban solid among others, the uncertainty around the required wastes, litter, leonardite, lime (CaCO3), etc. [22, 60, time-scales, the reproducibility of the results, and the 66, 68]. However, prior to their use, amendments current legal frameworks [26, 70]. As a matter of fact, should be thoroughly analyzed. In this respect, an many stakeholders perceive GROs in general, and exhaustive physical, chemical and biological phytoremediation in particular, as slow technologies characterization of the amendments is required to which are difficult to apply and suited only for large minimize/avoid the risk of introducing toxic and marginalized areas with low value [26, 28, 70]. compounds or potential human into the Nonetheless, it must be emphasized that contaminated amended soil, with concomitant hazards for lands are an extensive and underutilized resource [71] environmental and human health [69]. which, when properly managed, can provide economic revenues and valuable ecosystem services. In any event, it must be emphasized that In this respect, phytomanagement encourages the use phytostabilization does not decrease the total of plants with phytoremediation potential as part of an concentration of metals in the soil (i.e., the metal integrated site management which pursues, along with contaminants remain in the soil) but only immobilizes the mitigation of the risks derived from the presence them, thereby reducing their mobility and of the contaminants, the accomplishment of bioavailability. Consequently, there is always the economic, social and environmental benefits [46]. possibility that the metal contaminants are later These benefits include the provision of green space mobilized due to changes in the soil conditions, with and ecosystem services, the control of soil erosion potential adverse consequences in terms of and, above all, the generation of products and (eco)toxicity and/or metal dispersion. Therefore, commodities (e.g., bioenergy, wood, , phytostabilization processes must always be subjected biofortified products) [26, 28, 71]. For that purpose, to long-term monitoring programs regarding metal fast growing, deep rooted and easily propagated high bioavailability, (eco)toxicity and soil functioning [8]. biomass plants are often used, such as agronomical The main limitation of phytostabilization for its and herbaceous crop plants and trees.

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J Environ Sci Public Health 2020; 4 (2): 112-133 DOI: 10.26502/jesph.96120089

Phytomanagement makes site remediation an the target contaminants. Under favorable conditions, attractive option for stakeholders due to the some contaminants (e.g., short-chain petroleum environmental, economic and social benefits that can hydrocarbons) show high levels of degradation by be obtained, while mitigating the risk resulting from natural attenuation [22, 74]. However, the efficiency the presence of the contaminants. Then, of natural attenuation for more recalcitrant phytomanagement has been proposed as a very compounds is very low or null, especially for aged appealing “holding strategy” until full site contaminants [12]. regeneration is possible [26]. In order to maximize the efficiency of bioremediation 3.3 Bioremediation processes, the degrading capacity of indigenous Bioremediation, or the use of microorganisms microbial populations can be stimulated, via (mainly, and fungi) to clean up contaminated biostimulation strategies, by adjusting the supply of sites, is a sustainable option for the remediation of essential macro- and/or micronutrients, temperature, contaminated soils [72]. Although bioremediation can available oxygen, soil pH, redox potential, moisture, indeed be used for inorganic contaminants [73], its etc. [75]. However, the most common practice is application is more frequent for organic contaminants probably the addition of nutrients, either in inorganic such as mineral oils, petroleum hydrocarbons, form [76] or as organic amendments such as sewage polycyclic aromatic hydrocarbons (PAHs), sludge, manure, compost, etc. [73, 77, 78]. Again, it polychlorinated biphenyls (PCBs), , etc. must be taken into consideration that the rate of [12]. There are three main approaches for the contaminant degradation will depend on the (i) bioremediation of contaminated areas [74]: (i) natural physicochemical characteristics of the soil; (ii) attenuation, which is naturally carried out by the specific degrading microbial populations present in native microbial populations present in the the contaminated soil; and (iii) chemical nature of the contaminated area; (ii) bioaugmentation, which is contaminants themselves. Therefore, it is not based on the inoculation of selected microbial strains surprising than the type and dose of the amendments with the capacity to degrade the target contaminants at (inorganic and/or organic) must always be carefully a fast rate; and (iii) biostimulation, which is focused selected considering these three aspects [12]. Other on the modification of the environmental conditions practices include the addition of surfactants to (e.g., moisture, pH, nutrients, oxygen), in order to increase contaminant availability [79], the application stimulate the biodegradation of the target of biochar [80], and the growth of plants for contaminants. phytostimulation purposes [22].

In natural attenuation processes, the degradation of Bioaugmentation is focused on the inoculation of the contaminants is strongly determined by the (i) previously isolated and cultivated microbial strains, metabolic capacity of the native microbial individually or as a consortium, to stimulate the populations; (ii) the physicochemical properties of the biodegradation of the target organic contaminants. contaminated soil; and (iii) the chemical properties of The inoculation of “cocktails” of degrading strains is

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J Environ Sci Public Health 2020; 4 (2): 112-133 DOI: 10.26502/jesph.96120089 more frequent, compared to the inoculation of the target contaminants [91]. Some studies have individual strains, as microorganisms in consortium investigated the interaction between and can combine different metabolic activities that metal contaminants [92, 93], but vermiremediation is complement each other from a bioremediation point more commonly used for organic contaminants. of view [76, 81, 82]. The microbial strains used for Indeed, organic contaminants such as herbicides, bioaugmentation are commonly isolated from PCBs, PAHs or, in general, petroleum-derived similarly contaminated soils, sometimes from the hydrocarbons have been successfully remediated same soil to be remediated, in order to increase the through vermiremediation using a variety of probability of their survival and their capacity to species [94-97]. A particularly interesting express their biodegrading activity when inoculated in earthworm species, Eisenia fetida, has been used for the contaminated soil [83, 84]. The genetic vermiremediation purposes [98], as well as modification of bacterial strains to improve their bioindicator of metal ecotoxicity in soil [19, 99]. biodegradation performance, by means of genetically optimizing the production of enzymes and metabolic In order to successfully apply vermiremediation, pathways relevant for the biodegradation of the target several aspects need to be considered, such as the contaminants, has also been studied [85, 86]. behavior of the earthworms, their nutritional However, when selecting the different strains for the requirements, the characteristics of the soil, and the bioaugmentation consortium, their compatibility with nature of the contaminants themselves. According each other and their ecological fitness in the soil with their location in the soil, earthworms can be under remediation must be taken into consideration. cataloged as epigeic, endogeic and anecic: epigeic Actually, bioaugmentation initiatives fail quite often, earthworms, such as E. fetida, require high amounts mostly due to the incapability of the inoculated strains of organic matter and, then, they live at or near the to compete and properly develop in the contaminated soil surface where they feed on leaf litter, decaying soil [12, 87]. roots and dung. In consequence, they can (i) be used to remediate ; and (ii) be inoculated in biopiles 3.4 Vermiremediation employed for bioremediation purposes, where little Vermiremediation has been described as the use of burrowing is necessary. Endogeic and anecic earthworms for the removal of contaminants from soil earthworms, e.g. Lumbricus terrestris, on the other [88]. Earthworms are known to burrow through the hand, are better suited for the vermiremediation of soil, mixing it in their guts [89], and, consequently, deeper soil [91]. In order to guarantee the survival of they are capable of changing the physicochemical and the inoculated earthworms, sometimes it is required to biological properties of the soil, such as nutrient first ameliorate soil contamination levels [100]. availability, aeration, soil structure and, hence, the Certainly, extreme conditions (in terms of soil pH, activity of soil microbial communities [90]. In salinity, contaminant bioavailability) or a lack of addition, earthworms can increase the interaction organic matter can complicate the establishment of between soil microbial communities and the inoculated earthworms [92]. Organic amendments contaminants, thus facilitating the biodegradation of can then be used to reduce contaminant

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J Environ Sci Public Health 2020; 4 (2): 112-133 DOI: 10.26502/jesph.96120089 bioavailability, while adding organic matter and performed with each contaminant individually [106]. improving soil structure [101]. As a result, the application of only one remediation technology might not be effective for soils with mixed 4. Mixed remediation technologies for mixed contamination. Regrettably, many remediation studies contamination are focused on just one type of contaminant, probably Mixed contamination, when inorganic and organic due to the complexity of tackling mixed contaminants appear together, is present in many contamination cases. Nevertheless, in the last years, contaminated soils. Soils with mixed contamination more and more remediation studies have dealt with combine the individual challenges from each mixed-contaminated soils. For instance, individual class of contaminant with those derived bioaugmentation with a bacterial consortium has been from the combination of two or more types of reported to be effective for the remediation of soils contaminants with different properties. Regarding simultaneously contaminated with Cr (VI) and (eco)toxicity, synergistic effects on soil biota can lindane [107] or pyrene [108]. occur from that combination. Likewise, from a remediation point of view, the efficiency of the The combination of plants and bacteria for applied techniques may be reduced by the presence of phytoremediation purposes offers great potential for other types of contaminants or by the interaction soils with mixed contamination [109]. The presence between them [22]. For instance, in mixed of plants can enhance the activity and functional contaminated soils, it has been reported that co- diversity of soil microbial communities by releasing contamination with metals and organic compounds root exudates and improving the conditions for can cause metal immobilization [102] or, by contrast, microbial growth in the rhizosphere [62, 110]. Root an increase in metal mobility [25]. Therefore, the exudates create a nutrient-rich environment which can outcome of the interaction between different types of influence the behavior of metals [111] and enhance contaminants is site-specific, as it depends on the the biodegradation of organic contaminants [112]. specific properties of the contaminated soil, as well as The combination of vermiremediation with on the type and concentration of the contaminants phytoremediation and bioremediation has been themselves [103]. successfully tested for the remediation of soils contaminated with metals and organic contaminants Regarding the effectiveness of remediation [85, 113-115]. The combination of these biological technologies, metals can provoke toxic effects on soil remediation technologies appears promising for microbial communities, decreasing their abundance mixed-contaminated soils. Expectedly, factors such as and/or activities [104] and, consequently, reducing type of soil, chemical properties of the contaminants, their capacity to degrade the target organic and the biological species selected for the remediation contaminants [105]. In a phytoremediation (e.g., the specific species of plants, bacteria and experiment, it was observed that co-contamination earthworms) will strongly modify the outcome of the with copper and pyrene decreased plant growth and remediation process. the removal of pyrene, compared to the experiments

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As mentioned above, the use of amendments is very contaminated with organic compounds, especially common during the implementation of GROs. In those contaminated with organochlorinated particular, organic amendments provide soil nutrients compounds [127, 128]. Nevertheless, the use of and organic matter, improve soil structure, enhance nanoparticles for soil remediation has been questioned water holding capacity, alter contaminant due to their potential negative impact on soil biota. In bioavailability, etc. In consequence, organic any case, there is still a lack of information regarding amendment can alleviate toxicity for the species the mobility, bioaccumulation, dynamics and involved in the biological remediation of mixed- (eco)toxicity of nZVI in the soil environment [129, contaminated soils. Many studies have reported the 130]. Zero-valent iron nanoparticles have been benefits of using organic amendments during the described to provoke toxicity through two implementation of GROs [22, 114, 116, 117]. Other mechanisms: (i) physical damage by direct contact, authors have combined the application of disrupting cell membrane architecture and increasing nanoremediation (with, for instance, nanoscale zero permeability; and (ii) oxidative stress, leading to valent iron) with GROs with mixed results [118-121]. molecular and biochemical destruction [131]. Adverse The term nanoremediation refers to the application of effects of nZVI have been reported in plants [132], metallic nanoparticles (<100 nm) for the remediation animals [133] and microbial communities [134]. As of contaminated sites [122]. In particular, the use of expected, the potential effects of nZVI on soil biota zero-valent iron nanoparticles (nZVI) has caught the are highly conditioned by the and attention of the scientific community for the environmental conditions [121,131]. Therefore, it is remediation of contaminated waters and soils [123]. essential to perform an assessment of the potential Zero-valent iron nanoparticles have an iron core and a effects of nZVI on soil biota prior to their application shell of iron oxide and, due to their small size, show a under real field conditions, in order to first establish a very high surface/volume ratio [124]. The iron core safe, non-toxic and effective concentration for acts as the electron donor, while the shell plays nanoremediation purposes [130]. Indeed, despite their coordination and electrostatic functions, attracting and proven effectiveness for remediation, the effect of adsorbing charged ions [125]. Zero-valent iron nanoparticles on soil biota, including the biological nanoparticles have been applied for the remediation of species used for remediation, is yet full of both organic and inorganic contaminants. Regarding uncertainties. Then, the potential adverse impact of inorganic contaminants, nanoparticles can form nZVI on soil organisms must be tested prior to their complexes with soil metals, thus decreasing their use, alone or in combination with GROs. bioavailability [122]. Besides, by changing the redox potential of the soil, nZVI can alter the speciation of In conclusion, when facing a mixed-contaminated the metal contaminants, decreasing their soil, it is essential to first take into account a variety bioavailability and (eco)toxicity. For instance, nZVI of aspects, such as soil type, nature of the can reduce Cr (VI) to Cr (III), a less toxic and contaminants, compatibility of the remediation bioavailable form [126]. On the other hand, nZVI technologies, etc. in order to then be able to apply a have been reported to effectively remediate soils tailor-made strategy for each case. Besides, as

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Journal of Environmental Science and Public Health 133