Thallium-Transfer from Artificially Contaminated Soil to Young Downy Oak Plants (QUERCUS PUBESCENS WILLD.)
Abstract
The aim of this study concerns the observation over time of some young downy oak plants (Quercus pubescens Willd.), grown in a soil artificially contaminated with thallium, to determine i) thallium uptake and concentrations in individual parts (roots, trunks and leaves); ii) thallium transfer capacity from soil to plants; iii) the behavior of growth of affected plants by thallium contamination.
The value of Bio -concentration Factor (BF) shows the ability of plants to accumulate and concentrate thallium from artificially contaminated s oil. Values of BF greater than 1 explain the tendency of Quercus Pubescens Willd. to accumulate thallium in higher concentration than soil. The translocation factor (TF), calculated as the percentage ratio of thallium concentration in aerial parts to thallium concentration in roots, yet asserts a total transfer of thallium through the roots to aerial parts of the plants These data once again demonstrate the roots collapse in the fifth phase (200 days) and the lost of the ability to keep thallium in soil.
The microbial biomass carbon was lower in contaminated soils compared to the controls, and the entity of reduction was proportional to depth. The upper layer showed a decline of microbial population of almost 70%, while in the latter end of soil microbial population was reduced of 30% compared to control. Simultaneously, variations of the enzyme activity in the soil samples showed an increase of arylsulphatase, cellulase and β-glucosidase activity but only in the latter part of top soil (10-15 cm) while other enzymes exhibited a remarkable reduction of their activity in both soil layers, compared to the control.
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Introduction
Thallium (Tl) is a little studied heavy metal although it has been reported to be extremely toxic for all organisms in both oxidation states: the more stable mono form Tl(I) (+1 thallous), which tends to create stable toxic complexes with sulphurcontaining compounds, and trivalent form Tl(III) (+3 thallic) (Pavlickova et al., 2006; Queirolo et al., 2009; Mercurio and Hoffman, 2011).
Despite its minor consideration, thallium has been classified as one of the most pollutant metals for mammals (Queirolo et al., 2009) and his toxicity seems to be similar to Hg and higher compared to Cd, Pb, Cu and Zn. (Lehn and Bopp,1987;Ralph et al., 2002; Lan et al., 2005; Vanek et al., 2011; Alvarez-Ayuso et al., 2013). Thallium is widely distributed in the environment in very low concentrations. The average Tl concentration is 0.1 -1.0 μg g-1 in the lithosphere, 0.01–0.02 μg l-1 in seawater, and 0.01-14 μg l-1 in fresh water (Queirolo et al., 2009). Furthermore, there is an increasing demand for thallium in the high-technology and future-technology fields (Nriagu, 2003), and by limited data available in literature on its pollution, it seems that Tl level in soils may increase near thallium-emitting industrial sources and hazardous waste sites. Thallium is released into the environment from natural processes, such as the oxidation of pyrite containing thallium impurity, and from industrial operations, which use high temperature processes, as in steel industry, coal combustion, smelting processes and cement production (Bojakowska et al., 2013;Stafilov et al., 2013; Karbowska et al., 2014).
Generally, the average of geogenic Tl content in soil is less than 1 μg g-1all over the world (Tremel et al., 1996; Madejon, 2013), even if, high concentration of thallium (>50 μg g-1) has been reported in Silesian and Krakowian Provinces soil in Poland (Lis et al., 2003; Yang et al., 2015), in Guizhou Province in China (Xiao et al., 2004a, 2004b; He et al., 2007; Jia et al., 2013), and in Republic of Macedonia (Stafilov et al., 2013) especially in the vicinity of heavy metals mining or volcanic areas. Furthermore in 1997, very high thallium concentrations have been found in some arable soils in France (Tremel et al., 1997) and Turkey (Sasmaz et al., 2007).
In Italy, high thallium concentration has been reported in the Apuan Alps (Biagioni et al., 2013, 2014a, 2014b, 2014c), in the Julian Alps (Fellet et al., 2012), and in volcanic soil of Ischia Island (Frattini et al., 2006). Thallium phytoavailability depends on plant species, its form of binding or chemical speciation and total concentration in soil (Pavlìčková et al., 2006; Vanek et al., 2011; Markert at al., 2013). In addition to above-mentioned factors, it is important to consider other intrinsic and external factors, such as soil pH, temperature, soil water content, soil concentration of other elements (e.g. K+) (Kwan et al., 1990; Escarré et al., 2011), soil organic material and cation exchange capacity of rhizosphere (Wenzel et al., 2009; Jia et al., 2013).Thallium toxicity is mainly due to its similarity to potassium (K+), thus thallium can replace it in some metabolic processes (Wedepohl, 1995; Galvan-Arzate and Santamaria, 1998). Therefore, Tl has a strong affinity to sulfhydryl, aminoand imino-groups, which are normally included in peptides and amino acids, thereby inhibiting and inactivating enzymes activity (Pavlìčková et al., 2005 and 2006; Queirolo et al. 2009). In addition, inhibiting K-controlled activities of enzymes and membrane processes, thallium can deregulate the mitochondrial respiratory chain (Augustynowicz and Tokarz., 2014).As a result of this complex framework, thallium bioaccumulation can significantly vary among plant species because certain of them are more susceptible to accumulate it (Tremel et al., 1997;Pavlìčková et al., 2005; Jia et al., 2013), according to physiological adaptation, and only a few numbers of plants are able to grow in metal-polluted areas. Thallium in soil may be uptaken by plants, then translocated and bioconcetrated into their organs, considering that competitive interactions between pollutants and nutrients may reduce roots ability to absorb essential elements (Dominguez et al., 2009). Brassicaceae crops are Tl accumulator, as a result of their substantial potential to accumulate elevated amounts of Tl (Pavlìčková et al., 2006 and 2007; Madejon et al., 2007; Vanek et al., 2011; Wang et al., 2013). This aptitude highlights their potential for phytoremediation (Escarré et al., 2011; Vanek et al., 2011; Jia et al., 2013) that should be a bright strategy to improve not only the revegetation process in soil highly polluted but also to immobilized thallium preventing its release and migration into groundwater and surface water (Mueller, 2001; Paoletti and Günthardt-Goerg, 2006; Escarré et al., 2011). On the other hand, this peculiar aptitude confirms that food is probably the major source of thallium exposure of the general population (Sabbioni et al., 1994; White and Sabbioni, 1998). For this reason thallium contaminated soils and thallium transfer into the food chain, represent a significant threat to human health (Apostoli et al., 1988; Borges and Daugherty, 1994).
The Valdicastello-Pietrasanta site in Tuscany (Italy) is characterized by dismissed mine sites that release high concentration of thallium in soil and surface water, due to the oxidation of pyrite containing thallium impuritywhich can affect soil and water and increase Tl hazard. The Tl fate in this “extreme” mine environment, due to high thallium concentrations in both soil and water, has not been exhaustively studied neither in both field or mesocosm experiments.Therefore, because only a few numbers of previous studies on thallium transfer from soil to plant have been performed, we decided to assess 1) the Tl effect on the Quercus pubescens Willd. an autochthon plant possible candidate for future re-vegetation process (Bran et al., 1990; Wisniewsi and Dickinson, 2003; Paoletti and Günthardt-Goerg, 2006) in vicinity of mine sites; 2) the Tl uptake and translocation in soil-oak system(Hermle et al., 2006);3) distribution of major elements (Ca, Mg, K, Na, P and S) in different oak organs (e.g. root, trunk and leaves) in the control plants and Tl-exposed ones; 4) the consequences on both microbial biomass C and N content and enzymes activities in forest natural soil affected by Tl exposition.
Conclusion
Evidence shows that Tl(III) is slowly converted to a monovalent state because of its strong oxidizing properties. It is not yet clarify how the plants up taken the Tl from soil, if they taken it in trivalent form or the Tl(III) is reduced to Tl(I) onto the root surface. The hypothesis is that Tl(I) may be taken up by plants in the same mechanism of K uptake due to similar ionic radii and valence. The toxicity of Tl(III) is difficult to estimate because it easy reduced and this form seem to be more toxic than Tl(I) (Ralph and Twiss, 2002).
In this framework, the our experiment was address to evaluate the Tl(III) toxicity in soil-plant system. The Tl added into soil is accumulated and the average shows a good correlation between the calculated dose and measured one. A slight mobility of thallium has been observed in our experiment where the Tl added into soil was mainly immobilized in the upper part of soil (0-10 cm). Laboratory leaching test showed that the Tl mobility depends on composition of the aqueous phase of soil and the pH value between 5-6 strongly influences its mobility in soil (Lin and Nriagu (1998a; 1998b). The oak-soil maintains constant the pH value (7.2) for whole time of experiment, decreasing the leaching of Tl. Furthermore, there are some indications that thallium binds strongly to organic matter of soil showing low mobility into soil.
This hypothesis is further supported by the bio-concentration factor (BF) that comparing the thallium calculated dose added to the soil to the thallium concentration in aerial parts of the plants, revealed a complete transfer of thallium to the epigeal parts of plants. Values of BCF higher than resulted in a rising accumulation of thallium in aerial parts of Quercus Pubescens Willd. This tendency of preferential accumulation in the aerial parts of the plants is even more evident by calculating the value of the Translocation Factor (TF), which related the transfer of thallium from roots to aerial parts of plants, confirming the capability to accumulate thallium in the above ground tissues. This phenomenon could be an effect of a collapse of roots maybe caused by the necrosis of cellular structure, highly compromised by thallium concentration. This is probably due to thallium competition with potassium in membrane transporter that can cause deregulation of osmosis and of the transport of small molecules. The inefficiency in roots absorption resulted evident in Table 2, where a fall of thallium concentration in roots is associated with an increase of thallium absorption in leaves and trunks. Roots collapse is well demonstrated by the comparison between dry matters of contaminated plants to the controls. A significant reduction of weight and length of roots confirmed again the suppose death of roots tissues in contaminated soil. The dry weight of roots helped us to calculate the Tolerance Index of Quercus Pubescens Willd. Grown in contaminated soil. The ratio between the weights of plants raised in contaminated soil to that of plants grown into uncontaminated soil showed a tolerance of almost 50% up to 200 days of treatment, moment after which, as mentioned above, the collapse of roots is supposed. The results of the analysis showed that addition of thallium to the soils significantly influenced physiology of plants and their growth.
At the end of the experiment, we decided to assess the effect of thallium contamination on the microbial metabolism, assessing thallium effect on enzyme activities of soil. Soil enzymology can indeed serve as an indirect although very sensitive assessment of soil health. First of all, we noticed a decrease in soil microbial biomass carbon (C ) and nitrogen mic (N ) with increasing levels of thallium in soil. However, the ratio C:N remained stable on a value of 12, meaning that mic thallium contamination did not change the microbial population composition. However, the decrease of total microbial population confirms thallium toxicity in affecting soil health. The Figure 2 reports data on soil enzyme activities. A massive increase in the activity of arylsulphatase, cellulase and β-glucosidase is evident, especially in the latter part of the pots (10-15 cm). Cellulase and β-glucosidase are involved in catalysing the hydrolysis and biodegradation of plant debris incorporated to the soil in glucose as final product. This increased activity supports our hypothesis of increased roots decomposition into the soil that should induce hydrolyses action (Marinari and Vittori Antisari, 2010). Bacteria secrete Arylsulphatases into the external environment leading to S mobilization that has a main role in plant nutrition. A recent research suggested that plants control the activity of Arylsulphatases in the rhizosphere through root exudates in promoting both transcriptional and post transcriptional level. It could be possible that the increase of quantity of roots debris had stimulated a rise of secretion of arylsulphatase, to contrast the S fall due to contamination of thallium.
The experimentation performed during the growth early stages of young downy oak plants have shown that the contamination of thallium triggered to a deregulation of several processes in soil, such as microbial metabolism, soil retention ability and roots absorption. Thallium contamination interferes also with microbial ecology that can be considered an important indicator of soil quality. The lasts results are preliminary data collection on the influence of thallium contamination on enzyme activities that will be surely further explore in next experiments.
