Phytoremediation potential of Xanthium strumarium

International Journal of Environmental Science and Technology https://doi.org/10.1007/s13762-018-1825-5

ORIGINAL PAPER

Phytoremediation potential of Xanthium strumarium for heavy metals contaminated soils at roadsides N. Khalid1 · A. Noman2 · M. Aqeel3 · A. Masood4 · A. Tufail5 Received: 1 January 2018 / Revised: 21 May 2018 / Accepted: 29 May 2018 © Islamic Azad University (IAU) 2018

Abstract Xanthium strumarium was chosen in this study to evaluate its phytoremediation capacity for cadmium, lead, nickel and zinc metals. Five different sites were selected on Faisalabad–Sargodha road (FSR), Pakistan, to monitor the levels of cadmium, lead, nickel and zinc. Leaf and root samples were collected concurrently with soil samples to study the accumulation and tolerance of these metals in X. strumarium. To examine the health of X. strumarium, photosynthetic pigments, free amino acids concentration and total antioxidant activity were also tested. Highly significant concentrations of all metals were recorded in the soil and X. strumarium leaves and roots at all sites as compared to the control. On the average, X. strumarium leaves accumulated 0.27 ± 0.01 mg kg−1 cadmium, 3.33 ± 0.16 mg kg−1 lead, 54.5 ± 1.02 mg kg−1 zinc and 5.85 ± 0.11 mg kg−1 nickel from the soils that have average metal concentration of 0.25 ± 0.24 mg kg−1 cadmium, 3.38 ± 0.29 mg kg−1 lead, 118.7 ± 1.04 mg kg−1 zinc and 4.89 ± 0.12 mg kg−1 nickel. Overall, a slight variation in photosynthetic pigments was noted; however, plants growing at sites with higher metal concentrations exhibited reduced photosynthetic pigments. Increased total antioxidant activity and free amino acids were recorded. X. strumarium leaves showed high accumulation capacity for nickel, cadmium and lead as shown by their highest bio-concentration factors, i.e., 1.651, 1.574 and 1.048 for these metals, respectively. Significant correlations were also found in combinations of these metals in leaves and soils. This study identified X. strumarium as a strong phytoremediator of heavy metals at contaminated roadsides and potentially other areas. Keywords Bio-concentration factor · Phytoextraction · Roadside soil · Vehicular pollution

Introduction Heavy metal pollution has become a serious issue throughout the world with increasing industrialization and rapid urbanization (Noman et al. 2017). In the present century, Editorial responsibility: Necip Atar. * N. Khalid [email protected] 1

Department of Botany, Government College Women University, Sialkot, Pakistan

2

Department of Botany, Government College University, Faisalabad, Pakistan

3

School of Life Sciences, Lanzhou University, Lanzhou, People’s Republic of China

4

Department of Botany, The University of Lahore, Sargodha, Pakistan

5

Division of Science and Technology, Department of Botany, University of Education, Lahore, Pakistan

vehicular emissions are the single biggest source of metals which ends up in roadside soils making them metal hotspot areas (Ali 2006; Ali et al. 2009; Hwang et al. 2016; Gupta and Ali 2012) The metals most commonly released by vehicles during different processes are cadmium (Cd), lead (Pb), zinc (Zn), nickel (Ni) and iron (Fe) (Ali and Jain 2004; Wichmann et al. 2007; Chen et al. 2010; Zhang et al. 2015; De Silva et al. 2016; Dehghani et al. 2016; Ali et al. 2017; Khalid et al. 2017b, 2018a). The accumulation of heavy metals has become a matter of growing concern for modern societies as they are essentially non-biodegradable, unlike organic substances (Benavides et al. 2005; Ali et al. 2012; Khan et al. 2011b; Ali et al. 2014a, b; Ali et al. 2017). The buildup of heavy metals in water and soils poses a great risk to the environment. The high level of metals in the soil causes serious problems: Plants uptake leached metals and pass them through to animals that eat the plants. They, in turn, accumulate metals in their body tissues, and the concentration increases as it moves from lower to the higher trophic levels in the food chain (Chary et al. 2008; Khan

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International Journal of Environmental Science and Technology

et al. 2008; Ali et al. 2016c). Activities of soil microbes are also badly affected by the toxic effects of metals (Nayak et al. 2015). Heavy metals Cd and Pb are nonessential to life as they are naturally not found within organisms and are not reported to have any metabolic function in biological systems up till now. While, Zn and Ni are essential heavy metals which are required in small quantities for the normal growth of plants. However, they can be lethal in excess quantities (Rout and Das 2003; Noman et al. 2018). Metal toxicity can disrupt physiological activities of plants such as photosynthesis, nutrient absorption and gaseous exchange. It can also reduce growth, yield and dry matter accumulation (Sharma and Agrawal 2005). Upon exposure to humans, these metals can cause cancer, diabetes, cardiovascular disease, atherosclerosis, neurological disorders and chronic inflammation (Turkdogan et al. 2003; Jomova and Valko 2011). Possible sources of these metals on roadsides are: fossil fuel combustion, wear and tear of automobile tires, metals in catalysts and degradation of various vehicle parts, especially paints (Ozaki et al. 2004; Suzuki et al. 2009; Yola et al. 2014; Göde et al. 2017). To clean contaminated soils, various technologies have been established (Ali et al. 2016a, b). Among them, phytoremediation has been recognized as eco-friendly, sustainable and an economical alternative (Rungwa et al. 2013). Phytoremediation is the process whereby selected plants extract and accumulate metals and other pollutants into their tissues from the environment (Ali et al. 2013). For example, the role of plants in controlling and reducing air pollution has been increasingly documented in current years (Houda et al. 2016; Kumari et al. 2016). Many plant species have been recognized as hyperaccumulators, phytoremediators and indicators of metal pollutants in the environment (Wong 2003; Hanikenne et al. 2008). Most of the known hyperaccumulator or phytoremediator plants can accumulate and tolerate only a single toxic element (Robinson et al. 1997; Zhang et al. 2002; Schwartz et al. 2003; Lopez et al. 2005; Tamura et al. 2005). The roadside soils are multi-element contaminated soils. The cleanup of such soils can be negatively influenced if the hyperaccumulator cannot adapt to soils with high concentrations of several toxic elements. In order to evaluate the plant’s ability to absorb heavy metals from the soil, the bio-concentration factor (BCF) has been applied which shows the relationship between heavy metal content of soils and the corresponding plants species. BCF is a ratio of heavy metal concentration in plant leaves to that in soil. It shows the uptake capability of the plant for heavy metals from contaminated soils and is an appropriate measure for assessment. Many studies have calculated the BCF of plants for various elements (Zhao et al. 2003; Yoon et al. 2006; Zhuang et al. 2007; Balabanova et al. 2015; Khan et al. 2016). But few studies explore the relationship

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between heavy metals contamination in the soil resulting from traffic emissions in roadside farmland areas to native plant species. Xanthium strumarium L., a toxic inedible annual native plant, was found to be the dominant species growing at all sites in the study. It is self-sow plant, hardy to a wide range of temperatures and has wide adaptability to both dry and moist places. Additionally, it has been found naturalized in most areas of the world including developing countries like Pakistan, China and India. Therefore, this plant species appeared to be of particular interest and selected for study. To assess the phytoremediation potential of X. strumarium along roadside belts, Faisalabad–Sargodha road was selected. This road is very old major highway in the Punjab, Pakistan with high traffic volume and high emission of heavy metals. Other studies have been performed to assess the level of some of the heavy metals of vehicular origin along this road previously (Khalid et al. 2017a, b; Khalid et al. 2018a, b). But, until now, no other study was performed to evaluate the phytoremediation capacity of X. strumarium. Therefore, this study highlights the need to evaluate the accumulation potential and response of X. strumarium toward common road-borne heavy metals, specifically Pb, Cd, Zn and Ni.

Materials and methods Experimental design A survey was carried out to evaluate the level of Cd, Pb, Zn and Ni in soil at five sites along a major highway in the Punjab, Pakistan. The leaves and roots of Xanthium strumarium were also collected along with soil samples to assess the plant’s tolerance to these metals. Chlorophyll contents were tested to determine the effect of metal toxicity on the overall health of the plants. Bio-concentration factor (BCF) was calculated to determine the potential of the plant species to accumulate Cd, Pb, Ni and Zn metals.

Description of sites Data were collected from five sites on Faisalabad–Sargodha road (FSR) with an average distance of 10 km between consecutive sites (Fig. 1). The sites are named: Pull Dingro, Chiniot, Chenab Nagar, Adda-46 and Pull-111. The characteristics of the sites selected are: Pull Dingro is near cultivated crops; Chiniot is near the Bridge of the Chenab River; Chenab Nagar is along a big town with traffic of cars, motorcycles and buses; Adda-46 passes through a local market situated on the road’s edge. The traffic is mainly vans, trucks, cars and animal-driven carts; Pull-111 runs beside a stone crushing industry, where traffic is mainly trucks and multi-wheeler loaders.


Fig. 1 Sites along FSR road were: 1. Pull Dingro; 2. Chiniot; 3. Chenab Nagar; 4. Adda-46; 5. Pull-111

Collection of samples Soil and plant samples were collected 100 m away from the road as a control (Ma et al. 2009). pH of soils at all sites was also measured with a pH meter. Triplicate leaf and root samples of X. strumarium were collected nearest to the road’s edge from each site. Selected leaves were not very old. Samples were put in zip-locked bags, placed in an iced cooler immediately and brought to the laboratory. Three random soil samples were collected from each study site at a depth of 0–10 cm with an iron spatula (Werkenthin et al. 2014). Soil samples were passed through a fine mesh sieve after air drying and stored in polythene zip lock bags before analysis. The sampling was done in the spring season with average day temperature of 27 °C and average rainfall in the area of 21 mm/month.

Determination of metals Oven-dried plant and soil samples were subsequently digested by following the method of USEPA (1996). Pb,

Cd, Zn and Ni metals were determined by using Inductively Coupled Plasma-Atomic Emission Spectrometer (ICP-AES) Thermo iCAP Model 6300. Although several other novel techniques are in use for the detection of heavy metals in different kinds of samples (Yola et al. 2012; Gupta et al. 2013a, b; Göde et al. 2017), using ICPAES is the most advanced and reliable technique of metal determination. For calibration, standard solutions of High Purity Standards were used.

Determination of chlorophyll content For the extraction of chlorophyll, fresh leaves of X. strumarium were ground well and dissolved in 80% acetone solution at − 4 °C. Supernatant was separated after centrifugation. Optical densities were measured at 645, 663 and 480 nm on spectrophotometer (IRMECO U2020). The concentrations of chlorophyll contents were calculated by following the formulae given by Arnon (1949).

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Determination of total free amino acids Fresh plant material was extracted with phosphate buffer (pH 7), and 1 mL was taken in 25-mL test tube. In each test tube, 1 mL of 2% ninhydrin and 1 mL of 10% pyridine solutions were added. They were heated for 30 min in a boiling water bath. Volume was made up to 50 mL with distilled water. Optical density of the solution was noted at 570 nm on spectrophotometer (Hitachi 220, Japan). A standard curve was made with leucine, and total free amino acids were calculated by following the formula given by Hamilton and Van-Slyke (1943).

Determination of antioxidant activity To determine total antioxidant activity, 20 mL of 0.45% salt solution was added to 1 g of dried plant sample, heated in the water bath at 40 °C for 20 min. The solution was centrifuged for 30 min at 3000 rpm. Supernatant was collected and stored at − 20 °C before beginning the experiment. Then antioxidant activity was analyzed by following the method of Rahmat et al. (2003). Plant extract (4 mL) and 4 mL of absolute ethanol were mixed in a test tube, and then 4.1 mL of 2.52% linoleic acid in absolute alcohol, 8 mL of 0.05 M phosphate buffer (pH 7) and 3.9 mL of distilled water were added. The mixture was placed in an oven at 40 °C in darkness for 24 h. 0.1 mL of this solution was taken in another test tube, and 9.7 mL of 7.5% ethanol and 0.1 mL of ammonium thiocyanate were added. After 3 min, 0.1 mL of 0.02 M ferrous chloride in 3.5% hydrochloric acid was added to the reaction mixture. Absorbance was measured at 500 nm on spectrophotometer. The antioxidant activity was determined by using the following formula:

Total antioxidant activity =

Absorbance of control × 100 Absorbance of sample

Bio‑concentration factor (BCF) Bio-concentration factors (BCF) of X. strumarium for different metals were calculated using the following formula:

BCF =

Metal concentration in leaves Same metal concentration in soil

Statistical analysis Data were analyzed by using one-way analysis of variance, and means were compared using the LSD test at probability level of 0.05. Pearson’s coefficient for correlation

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(2-tailed test) for the data was statistically analyzed at P