Elsevier

Chemosphere

Volume 73, Issue 5, October 2008, Pages 635-642
Chemosphere

The effect of nitrogen form on rhizosphere soil pH and zinc phytoextraction by Thlaspi caerulescens

https://doi.org/10.1016/j.chemosphere.2008.07.034Get rights and content

Abstract

The phytoextraction of Zn may be improved by applying N fertilizers to increase the biomass and Zn content of shoots. Rhizosphere-pH change from uptake of different N forms will affect Zn phyto-availability in the rhizosphere and Zn phytoextraction. This glasshouse study examined the effect of N form on Zn phytoextraction by Thlaspi caerulescens (Prayon). The plants were grown in a Zn-contaminated soil (total Zn 250 mg kg−1 soil; pHwater 5.7) and supplied with (NH4)2SO4, Ca(NO3)2 or urea [(NH2)2CO]. The NH4+ form was maintained by applying the nitrification inhibitor dicyandiamide. A biodegradable chelator ethylenediaminedisuccinic acid (EDDS) was included for comparison. The addition of N doubled the shoot biomass. The highest shoot Zn content occurred in the Ca(NO3)2 treatment and was associated with the highest rhizosphere pH. The lowest shoot dry weight occurred in the EDDS treatment. The Zn concentration in the shoots increased as the rhizosphere pH increased. A significant correlation occurred between Ca and Zn concentrations in the shoots. This study demonstrated that Ca(NO3)2 is a more effective treatment than NH4+, urea or EDDS for enhancing Zn phytoextraction in a mildly acidic soil.

Introduction

Soils can become contaminated with Zn from metalliferous mining wastes, smelters, refractories, industry, galvanized metalwork, sewage sludge and excess fertilization (Vangronsveld and Cunningham, 1998). Zinc-contaminated soils are a concern when plants are unable to be successfully grown either for agriculture, mine-site stabilization or urban purposes as a result of Zn phytotoxicity. Remediation of contaminated soils can be achieved by either removal of the contaminated soil, dilution with cleaner soil, or chelate/acid-washing of the soil to remove the Zn. However, these methods destroy the soil structure, often introduce new contaminants, and can be expensive (Vangronsveld and Cunningham, 1998). Alternatively, contaminated soils can be remediated using phytoextraction. Zinc phytoextraction is based upon enhanced Zn uptake by Zn-tolerant plants, and then harvest of the Zn-containing shoot biomass. This method is applicable to sites where other remediation options are uneconomical or unavailable and the timeframe for phytoremediation is acceptable. Currently, phytoremediation is being researched to increase phytoextraction and hence to decrease the time and financial cost for site remediation.

Thlaspi caerulescens is a Zn hyperaccumulator (Baker and Brooks, 1989) which typically produces a small biomass in the range 140–360 mg plant−1 (Knight et al., 1997), and shows much variability in growth rate and biomass potential in its natural populations (Bennett et al., 1998). Treatments which increase shoot biomass, without reducing Zn concentration in shoots, have the potential to enhance Zn phytoextraction.

Plants can only extract Zn from soil in the soluble form (Marschner, 1995). Therefore, Zn uptake depends upon Zn solubility, which can be increased by three common methods: acidification, complexation with chelates and Zn desorption or dissolution when the soluble Zn fraction is depleted. Zinc becomes 100 times more soluble for each unit of pH decreased from around pH 8 due to dissolution and desorption (Basta and Tabatabai, 1992, Stumm and Morgan, 1996, Adriano, 2001). Thus rhizosphere acidification should increase the soluble Zn concentration directly in the rhizosphere where it can improve phytoextraction and reduce remediation time (Brown et al., 1994). Rhizosphere acidification is preferable to acidification of the bulk soil because Zn and other co-occurring heavy metals are less likely to leach further into the environment. Furthermore, T. caerulescens is capable of depleting soluble zinc fractions (1 M NH4NO3), resulting in Zn mobilization from less available fractions in a passive equilibration of solid and solution phases (Whiting et al., 2001).

Nitrogen fertilization has been shown to increase shoot biomass and enhance Zn extraction (Ebbs et al., 1997, Bennett et al., 1998, Schwartz et al., 2003). A greater shoot biomass provides more leaf area for storage of sequestered Zn thus enhancing total Zn content per plant. The chemical form of N taken up by a plant can distinctly influence the rhizosphere pH (Nye, 1981, Gijsman, 1990, Tang and Rengel, 2003). Nitrogen can be absorbed by plant roots as NH4+, NO3- or as neutral urea (NH2)2CO. Urea can also be hydrolyzed by microbially produced urease into NH4+. When plants take up NH4+, there are more cations than anions taken into the root cells. Consequently, H+ is exuded to regulate cytosolic pH and charge balance, and the rhizosphere pH decreases. In contrast, uptake of NO3- can cause H+ influx (or OH efflux) with a rhizosphere pH increase, while neutral urea causes little pH change (Nye, 1981, Haynes, 1990, Mengel and Kirkby, 2001, Hinsinger et al., 2003). Fertilization with (NH4)2SO4 and subsequent rhizosphere acidification enhanced Zn accumulation in non-accumulators such as willow cultivars (Salix viminalis L.), field bean (Phaseolus vulgaris L. cv. Saxa), radish (Raphanus sativus L.) and barley (Hordeum vulgare L., cv. Dorirumugi) (Sarkar and Jones, 1982a, Sarkar and Jones, 1982b, Youssef and Chino, 1989, Thomson et al., 1993, Lorenz et al., 1994, Kashem and Singh, 2002, Schmidt, 2003). In contrast, Schwartz et al. (2003) observed that (NH4)2SO4 fertilization reduced Zn accumulation and shoot dry weight in the hyperaccumulator T. caerulescens compared to NaNO3. However, they did not compare these findings with the rhizosphere pH.

Ethylenediaminedisuccinic acid (EDDS) is a naturally occurring aminopolycarboxylic acid produced by actinomycetes, and is often used as a biodegradable chelator for transition metal phytoextraction (Nishikiori et al., 1994, Bucheli-Witschel and Egli, 2001). The EDDS forms stable hexadentate complexes with transition metals (Vandevivere et al., 2001), and increases the concentration of total soluble Zn (Zn2+ and Zn–EDDS) in the soil solution. It has been shown to enhance Zn phytoextraction (Meers et al., 2005, Luo et al., 2006, Tandy et al., 2006), and was included in this study to compare its phytoextraction efficiency against the proposed fertilization method. EDDS is preferred over the historically favored EDTA for chelate-assisted phytoextraction since EDTA persists in the soil where it contributes to further contamination by nutrient and heavy metal leaching. The effectiveness of EDDS for Zn phytoextraction is dependent on four main factors: the presence of other competing metals and ions which may react with EDDS in preference to Zn, the activities of these metals in solution, the concentration of EDDS, and the solution pH. In contrast to the benefits of EDDS-assisted phytoextraction, EDDS is currently expensive to apply at the required rates, and metal-EDDS complexes have been found to degrade much more slowly than the tri-sodium complex form which is applied initially (Vandevivere et al., 2001).

The aim of this study was to compare the effect of three different N fertilizers and a chelator on rhizosphere pH, and Zn uptake by T. caerulescens. A nitrification inhibitor was used to maintain the NH4+ form of N available for uptake. We also aimed to understand the mechanisms associated with enhanced Zn extraction. We hypothesized that T. caerulescens would respond to NH4+ fertilization by an acidification of the rhizosphere, and to NO3- by rhizosphere alkalization, while acidification would favor Zn phytoextraction.

Section snippets

Soil collection and characterization

A Zn-contaminated soil (377 ± 20 mg Zn kg−1) was collected from the A horizon beneath a galvanized electricity pylon at Narre Warren, Victoria. The soil was sandy loam. The soil was air-dried, crushed to pass through a 2 mm sieve and mixed with washed river sand to obtain a homogenous soil with approximately 250 mg Zn kg−1. Selected properties of the final soil mixture are listed in Table 1.

Experimental design

A randomized pot experiment was conducted in a temperature-controlled glasshouse (20 ± 5 °C) with natural light.

Plant growth

All plants appeared healthy during growth, with an apparent difference in shoot biomass and color between the treatments, and very little difference within treatments and within each pot. The control and EDDS-treated plants, which received no N fertilizer, appeared paler than the other treatments. After the EDDS treatment, the leaves wilted and began to senesce. The DCD-treated plants showed some chlorosis of leaf-tips. The average shoot dry weights ranged from 0.17 to 0.38 g plant−1, and were

Discussion

This study illustrated that rhizosphere acidification did not enhance Zn extraction by T. caerulescens grown in a mildly acid soil. A contradictory result to our hypothesis was that a higher rhizosphere pH enhanced Zn extraction. This occurred with application of Ca(NO3)2 and was associated with an increased Zn content.

Enhanced shoot biomass following N fertilization improved Zn extraction by this typically low biomass species. An important result was the >100% increase in dry weight of

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