Plant-assisted bioremediation of a historically PCB and heavy metal-contaminated area in Southern Italy
Graphical abstract
Introduction
Polychlorinated biphenyls (PCBs) are persistent and ubiquitous organic contaminants widely used in industrial applications. Although their production has been banned since the 1970s their high recalcitrance and toxicity have caused the contamination of lakes, sediments and soils and their removal from contaminated ecosystems continues to present a challenge [1], [2]. Among remediation strategies, the use of biological systems represents an effective, cost-competitive and environmentally friendly alternative to the thermal and physico-chemical technologies more traditionally used [3]. Microbial metabolism is potentially capable of degrading persistent organic pollutants, including polychlorinated biphenyls (PCBs) [4]. Laboratory studies have identified several bacterial strains able to aerobically transform lower chlorinated congeners through metabolic and co-metabolic pathways, and anaerobically highly chlorinated ones by using them as electron acceptors [5], [6], [7], [8]. The role of specific microbial species in promoting PCB de-halogenation has been evaluated in several reports [9], [10], [11]. However, the complete degradative pathways and the environmental parameters involved in PCB transformation need to be better clarified [12]. Consequently, the next major focus of research into PCBs should be to maximise the potential of these natural degraders in order to accelerate environmental degradation processes [13]. Natural microbial communities in contaminated soils can be stimulated to degrade PCBs by providing them with specific nutrients [14] or the degradation can be promoted through the addition of specific degradative microbial populations [11].
Plant-microorganism association can improve PCB degradation in the rhizosphere thanks to synergic interactions between roots and the natural soil microbial community [15], [16], [17], [12], [13]. Plants can help natural microbial communities to transform, remove and contain contaminants in soil in so-called plant-assisted bioremediation [18]. Many plant species are capable of thriving in PCB contaminated soils and can stimulate indigenous soil populations with a degradative capability [3], [19], [20], [21]. Plant roots tend to transfer contaminants from the bulk soil to the rhizosphere where microbial activity and toxic compound degradation are promoted by root exudates. Some exudates may contain plant secondary metabolites, which can act as chemical signals promoting or inducing the bacterial enzymes involved in PCB degradation [12], [13], [22], [23], [24], [25]. In return, degrading bacteria can produce plant growth stimulators or can suppress pathogens through competition and antibiotic production [26], [27].
A wide range of plant genera has been shown to enhance the dissipation of PCBs in soil, from trees such as Populus and Salix to different forages, both grasses and legumes [28], [29], [30], [15]. In particular poplar, owing to its fast growth rate and deep and wide-spreading root system, plus its ability to grow in nutrient poor soil and to resist high metal concentrations [31], [32], [33], [34] it has been used successfully to stimulate the biodegradation of xenobiotic compounds. both in field [35], [36], [37] and microcosm studies [13], [38]. Poplar was also found to be effective in heavy metal phytoremediation experiments [39].
However, only a few investigations with large-scale trials have been attempted and were often not completed [16], [40]. No evidence of PCB degradation in the field has been found so far in historically and multi-contaminated soils, where PCB molecules are strongly bound to soil particles and therefore less available for biodegradation processes. Consequently, carrying out field experiments in degraded sites is a challenge whose implementation makes it possible to select new candidate plant and microbe species and/or identify bioremediation strategies for recovery of multi-contaminated soils.
In the present study an area in Southern Italy historically contaminated by PCBs and heavy metals was planted with a selected poplar clone in order to test its ability to promote PCB bioremediation. The overall results of the chemical and microbiological analyses performed 420 days after poplar planting showed not only a significant decrease in all PCB congeners detected, but also a considerable heavy metal phyto-containment and a general increase in the microbial activity of the autochthonous microbial community.
Section snippets
Experimental site and soil characterisation
The study site was located in Southern Italy (40°28′04.92″ N, 17°18′12.68″ E) close to the city of Taranto (Apulia Region). The northern part was next to a small power station with electrical transformers. Uncontrolled spilling and improper disposal of dielectric fluids have resulted in PCB pollution over a 30-year period. Moreover, since the same site was used as an uncontrolled waste dump, different waste layers (e.g. construction rubbish, polluted sediments originating from the “Mar Piccolo”
Poplar growth
Over 99% of the poplar cuttings took root, the vegetative growth of cuttings being rapid and luxuriant. During the summer (two months after planting), an attack by the parasitic wasp Messa hortulana was observed on some of the poplar leaves; however, the plants displayed an optimal resistance and the damage was limited and no longer visible after a short time. The Monviso clone proved able to grow luxuriantly in this area chronically polluted by PCBs and heavy metals and 420 days (14 months)
Discussion
The significant decrease in all PCB congeners, to less than the Italian environmental law limit (60 ng/g), in the poplar-planted plot shows the effectiveness of the Monviso clone at promoting the degradation of these persistent compounds. Confirming this result is the fact that in the control plot soil, outside the poplar-planting area, PCBs had not decreased by day 420 (Table 1). As can be seen in Fig. 2, a decreasing trend in the percentage of PCB removal is observable from the soil points at
Conclusions
The Monviso clone was applied to a historically contaminated soil to promote PCB biodegradation through its root system. At about 1 year after planting, the overall results of the chemical analyses (PCBs and heavy metals) showed the effectiveness of this green technology at recovering degraded soil not only from organic, but also from inorganic contamination (phyto-containment, [69]). The soil remediation strategy is still being applied and the planting of the Monviso clone in other contaminated
Acknowledgments
The authors thank Giuseppe Bagnuolo (CNR-IRSA) for his technical support in the chemical analyses of the pollutants, Guido Del Moro, Andrea Decembrino and Vito Nicola Palmisano (CNR-IRSA) for their useful assistance in the poplar planting, and Francesca Falconi (CNR-IRSA) for the microbiological analysis. The authors also thank Daniele Bianconi (CNR-IBAF) for his scientific support in the poplar plantation design and the Reverend Nicola Preziuso and Michele Arcangelo D’Alessandro (CEM of
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