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Effects of Rhizobacteria on the growth, and uptake of lead by tall fescue (Festuca arundinacea).

INTRODUCTION

Muscle and joint pain, and memory or concentration problems [2, 3].

According to the American Academy of Pediatrics (AAP), soil is contaminated by lead from various sources. Lead particles are deposited in the soil from flaking lead paint and incinerators, as well as from waste disposal [4]. Natural levels of lead in soil are usually below 50 ppm [5, 6].

Phytoremediation is an alternative way of reducing heavy metal contamination from the soil by using different plant species known as hyperaccumulators. Hyperaccumulators refer to plants that share the ability to grow on metalliferous soils and accumulate extraordinarily high amounts of heavy metals in the aerial organs without suffering phytotoxic effects. A strongly enhanced rate of heavy metal uptake, faster root-to-shoot translocation and a greater ability to detoxify and sequester heavy metals in leaves are the primary differences between hyperaccumulators and non-hyperaccumulators.

The combination of the two approaches, phytoremediation and bioaugmentation, results in a process known as rhizoremediation. During rhizoremediation, exudates derived from the plant can help to stimulate the survival and action of bacteria subsequently resulting in a more efficient degradation of pollutants. The bacteria are spread through the soil via the root system of plants penetrating otherwise impermeable soil layers [7].

It has been suggested that rhizosphere microbes may play an important role in phytoremediation. Microbes are ubiquitous in soils to which hyperaccumulators are native, even in those soils containing high concentrations of metals [8]. We envisioned that certain bacteria might have a beneficial effect on plant's growth especially root growth, an important component of phytoremediation. We also hypothesized that the presence of bacteria in the rhizosphere might increase the solubility of Pb in the soil, which may also increase Pb uptake by tall fescue.

Tall fescue (Festuca arundinacea Schreb.) is a robust long-lived, comparatively deep-rooted bunchgrass. It is adapted to cool and humid climates and will grow fairly well on soils low in fertility [9]. Fescue is distributed throughout the majority of the United States and it is easy to establish due to its rapid germination and good seedling vigor [9]. This plant is especially well adapted to acid, wet soils of shale origin and produces more forage than other cool-season grasses on soils with a pH of less than 5.5. Tall fescue has also been reported to be an efficient Pb-accumulating plant when coupled with other phytoextraction strategies such as lower pH, and the use of a chelate [10].

The two bacteria used in this study were Pseudomonas monteilii (ATCC 700476) and Wautersia metallidurans (ATCC 43123). Pseudomonas monteilii (ATCC 700476) is a gram-negative, rod-shaped bacterium that is nonhemolytic on blood agar and was isolated from clinical sources. Various rhizosphere bacteria are potential (micro) biological pesticides which are able to protect plants against disease and improve plant yield [11]. Gram-negative rods such as Pseudomonas spp. dominate the rhizosphere. The presence and survival of these beneficial rhizobacterial strains are, in contrast to the limited studies of rhizoremediation, presented in detail for processes such as biocontrol of soil borne plant diseases [12, 13], biofertilization, and phytostimulation [14]. Success of these important processes is based on the rhizosphere competence of the microbes [15], which is reflected by the ability of the microbes to survive in the rhizosphere, compete for the exudate's nutrients, sustain sufficient numbers, and efficiently colonize the growing root system [15]. Wautersia metallidurans (ATCC 43123) is thought to be resistant to zinc, cobalt, nickel, mercury, cadmium, and produces a zinc-binding protein. In broth, the cells may appear as short to long rods. These soil-borne bacteria with plant-growth promoting effects are generally termed plant growth-promoting rhizobacteria (PGPR) [11, 16].

MATERIAL AND METHODS

Chemical Reagents and Other Materials

Lead nitrate [(Pb[(N[O.sub.3]).sub.2]], and other chemicals were purchased from Sigma Chemical (St. Louis, MO), and Fisher Scientific (Houston, TX). Delta top soil, humus peat, and seeds of tall fescue were purchased from Hutto's Garden Supply (Jackson, MS). Deepot D40 656 mL planting tubes (referred to hereafter as planting tubes or tubes) and support trays were purchased from Stuewe and Sons, Inc. (Corvallis, OR). Delta top soil and peat were weighed on a Brainweight 1500 scale, Model B1500 (Ohaus Scale corp.).

Dry tissue biomass was determined using a Metler AE260 analytical balance. Reagents were weighed with a Wards Electronic top loading balance (Model 15 W6201). Plant tissue samples were dried in a Precision Thelco Model 18 convection oven at 75[degrees] C for approximately 48 hours. Lead concentration of plant tissues were analyzed with a Perkin Elmer Optima 3300 DV Inductively Coupled Plasma-Optical Emission Spectrometer (ICP-OES) and were expressed as pg Pb/g dry weight (ppm). Modified Hoagland's nutrient solution containing buffers and trace elements were prepared in the laboratory.

Soil and Growth Medium Preparation

Appropriate amounts of lead nitrate [Pb[(N[O.sub.3]).sub.2]] were mixed with delta top soil and humus peat. Delta top soil is a silt loam soil, a member of the fine, kaolinitic, thermic typic kandiudult soils [17]. Representative samples of the prepared soil mixture were sent to Mississippi State University Soil Testing Laboratory, Mississippi State, MS for determination of its physical and chemical characteristics.

Approximately 550 g of the dry, sieved delta topsoil, peat mixture (2:1 v/v) were placed in a plastic zip lock bag and amended with either 0, 500, 1000, or 2000 mg Pb/kg dry soil mixture using lead nitrate. Deionized distilled water (DDW) was added to the bags to adjust the soil moisture content to approximately 30% field capacity. The bags of soil were left to equilibrate (age) on a laboratory bench in the greenhouse for six months. The bags were occasionally turned and mixed during the incubation period to ensure thorough mixing.

Sterile soils were prepared by placing 550g of each soil mixture with the appropriate metal concentration into separate brown paper bags and autoclaved at 121[degrees] C, 15 psi, for one hour on three consecutive days. The autoclaved soil in each bag was dispensed into each sterile 660 mL black plastic planting tubes, and pre-treated, bacterial-inoculated seeds of tall fescue were planted. All treatments were carried out in three replicates.

Preparation and Inoculation of Seeds

Tall fescue seeds were surface-sterilized by shaking in 70% ethanol for one minute then rinsed five times with sterile water. A germination test was conducted for axenic seeds and non-sterile seeds to determine their viability.

Two strains of commercial bacteria were used: Pseudomonas monteilii (B1 [Bacteria 1]) and Wautersia metallidurans (B2 [Bacteria 2]) based on a viability study previously conducted in our laboratory (data not presented). Following the procedure of Whiting and his colleagues [8], a mixed inoculum of these two bacterial strains was prepared for seed inoculation. One loopful of each bacterial strain was added to 5 mL of sterile 0.85% saline (NaCl) solution in a sterile plastic 15 mL BD Falcon tube and vortexed to suspend the bacteria. Specifically, one mL of this suspension was added to 4 mL of sterile 0.5% methylcellulose solution prepared with 0.85% sterile saline solution to provide a bacterial suspension for inoculation of seeds.

To estimate the number of bacteria in the culture, serial dilutions of each of the bacterial solutions were spread on 1.5% trypticase soy agar (TSA) plates and incubated at 25[degrees] C for 7 days. The live bacterial suspension contained a total of 2.52 x 108 colony-forming units (CFU) per milliliter. One set (n=144) of sterile fescue seeds were soaked in the bacterial solution containing B1 (Pseudomonas monteilii). A second set (n=144) of sterile fescue seeds were soaked in a bacterial solution containing B2 (Wautersia metallidurans). A third set (n=144) of sterile fescue seeds were soaked in bacterial solution containing both B1 and B2. After 20 minutes of soaking, all seeds were removed from the bacterial solutions and dried on sterile filter papers in a laminar-flow cabinet. All subsequent seed transfers from the filter papers to the growth media were performed using flamed, autoclaved forceps in a laminar-flow cabinet.

Planting, Plant Establishment and Maintenance, and Harvesting

After the seeds of tall fescue were inoculated with Pseudomonas monteilii and Wautersia metallidurans, they were planted in sterile plastic D40 planting tubes containing sterile or non-sterile metal-contaminated soil. Each sterile planting tube was filled with 550 g of the appropriate sterile Pb-spiked soil mixture (0, 500, 1000, 2000 mg Pb/kg dry soil) previously prepared. Eight of the pre-treated seeds were sown in each of the planting tubes and watered with 10 mL autoclaved water.

Emerged seedlings were thinned out to a desired population density of four plants per tube at 5 days after emergence. In this experiment, each treatment replicate consisted of one tube containing four plants. Any symptoms of metal toxicity (e.g., discoloration, pigmentation, yellowing, stunting) exhibited by plants were noted during the experimental period. Additionally, the position of each D40 tray was rotated one position clockwise each week to prevent any growth discrepancies that may occur due to shadowing by another plant.

Plants were maintained at the naturally lit Jackson State University greenhouse throughout the experimental period.

Each planting tube was watered with 10 mL of autoclaved water as needed. After 15 days, the plants were watered with modified Hoagland's nutrient solution on alternating days. The chelating agent ethylenediaminetetraacetic acid (EDTA) was applied to the soil one week before harvest. The plants were allowed to grow for six weeks. After harvesting, the root and shoot lengths were measured, roots and shoots were separated and roots were washed with DDW to remove any adhering soil particle and debris. The roots and shoots were placed separately in brown paper bags and oven dried at 75[degrees]C for 48 hours. The dry weight of roots and shoots were determined using a Metler AE260 analytical balance.

Lead Extraction and Analyses

Lead was extracted from all root and shoot samples using a nitric acid-hydrogen peroxide procedures with slight modifications [18]. Lead contents of digestates were quantified using ICP-OES (Perkin Elmer Optima 3300 DV). In general, experimental units were arranged in a randomized complete block design (RCBD) with three replications. Data were analyzed using SAS V9. Statistical analysis of variance was performed on all data sets. Least significant difference (Fisher's LSD) was used for multiple comparisons between different treatments and control groups. Results of the statistical data were summarized in figures and tables. In this study, a probability of 0.05 or less was considered to be statistically significant.

RESULTS

The delta top soil used in this study was classified as a silt loam soil, belonging to the family of fine, Kaolinitic, thermic typic Kandiudult soils [17]. The soil had a sandy loam texture with a cation exchange capacity (CEC) of 17.6 and a pH of 6.3. The extractable magnesium was considered to be very high at 726 lbs/acre.

Tall fescue plants grown in sterile Pb-contaminated soils with treatments of EDTA and bacteria (previously described) indicated that shoot Pb concentrations were highest in treatments of 2000 mg Pb/kg dry sterile soil (Figure 1). Shoot Pb concentrations of tall fescue grown in non-sterile soil followed the same trend as shoots of tall fescue grown in sterile soil (Figure 2).

Figures 3 and 4 show the root Pb concentrations of tall fescue plants grown in sterile and non-sterile soils, respectively. Root Pb concentrations in sterile soils were highest in treatments using bacteria alone without the addition of EDTA at 2000 mg Pb/kg dry soil treatment, though not significantly so. Root Pb concentrations of plants inoculated with B2 and B1 + B2, and were significantly higher than treatments with EDTA + B1 and EDTA + B2 +B2. (Figure 3).

Root Pb concentrations of tall fescue that were grown in non-sterile soils were generally higher in treatments with bacteria + EDTA as compared to bacterial treatments without EDTA (Figure 4). The highest concentrations were observed in plants grown in non-sterile soil with treatments of EDtA and B1 + B2 treatments.

Shoot and root biomass of tall fescue plants grown in sterile soils were lowest at 2000 mg Pb/kg dry soil. Conversely, shoot biomass was highest in 1000 mg Pb/kg dry soil across all treatments (Figure 5). On the other hand, shoot biomass of tall fescue grown in non-sterile soil were generally greater in plants exposed to 500 and 1000 mg Pb/kg non-sterile soil (Figure 6) compared to the control and 2000 mg Pb/kg treatments

Root biomass of tall fescue grown in sterile soil (Figure 7) were higher in treatments of 500 and 1000 mg Pb/kg sterile soil and lowest in treatments of 2000 mg Pb/kg dry sterile soil. In Pb soil treatments of 2000 mg Pb/kg dry sterile soil, root biomass was lower than the control across all treatments. Our research showed that the root biomass of tall fescue grown in non-sterile soil was highest in the control and lowest in treatments of 2000 Pb/kg dry non-sterile soil. Tall fescue grown in soil treated with bacteria had generally higher root biomass than those plants treated with no bacteria (Figure 8).

DISCUSSION

Soil pH is one of the most influential parameters controlling the mobility and availability of metals in the soils. In our greenhouse study, soil pH before planting was 6.3 and decreased with increasing amounts of soil-applied Pb. After chelate application, the soil pH remained in the range of 5.5-6.5 (data not shown), a range not unusual in chelate-assisted phytoextraction [19]. Unlike nitrilotriacetic acid (NTA), another strong complexing agent, which exhibits a significant pH dependency, ethylene diamine tetraacetic acid (EDTA), the chelating agent used in this study, is generally pH-insensitive and can remain relatively constant over a broad pH range (4.9 11.3) as demonstrated by Peters and Shem [19].

In general, the chemistry of metal interaction with soil matrix is central to the phytoremediation concept. While the soil used in this study was high in phosphorus, potassium and zinc; and very high in magnesium, these were, nonetheless, essential plant nutrients. Overall, the parameters of the soil used in this study were well within limits for our objectives.

A relevant control soil which accurately represents the polluted soil in its pristine state is rarely available. The polluted soil is often contaminated with more than one metal, and except around point sources of pollution, a gradient of metal concentrations is rarely available. Ideally, the control soil should be the same soil lacking in only the additions of metals, but in reality this is hardly ever achieved [20].

This study was therefore carried out using a laboratory prepared Pb-spiked soil that had been aged for six months. This approach is simplistic in that it bears little relation to most "real-life" contaminated soils where metal concentrations are gradually built up due to atmospheric deposition, fertilizers and contaminated wastes [20].

Although the total Pb concentration in many contaminated soils may be high, the bioavailable Pb fraction (water soluble and exchangeable) is usually very low due to the strong association of Pb with organic matter, Fe-Mn oxides, and clays, and precipitation as carbonates, hydroxides, and phosphates [21].

Miller [22] performed the classical sequential extraction by Tessier and his colleagues [23] on a laboratory prepared Pb-spiked soil that had been prepared using the same method that we used in this study and reported that approximately 17% of the Pb is expected to be bioavailable for plant root uptake. The greater percentage of Pb was concentrated in the residual and exchangeable fractions of this soil type [22, 24]. The residual fraction (fraction 5) can be thought of as what is left over after the first four fractions have been removed. It contains primary and secondary minerals which may hold trace metals within their crystal structure [23]. These metals are not expected to be released under normal environmental conditions and therefore, not bioavailable for plant uptake.

Our results indicate that Wautersia metallidurans ATCC 43123 and Pseudomonas monteilii ATCC 700476 may have facilitated the growth and Pb tissue uptake of tall fescue (Festuca arundinacea) and therefore may increase the phytoremediation efficiency especially at Pb soil concentrations less than 2000 mg Pb/kg dry soil.

Soil rhizobacteria may have also directly influenced metal solubility by changing heavy metal speciation in the rhizosphere of tall fescue, similar to what has been reported earlier by Jing et al. [25]. Study of the roles of mycorrhiza in metal speciation in the rhizosphere and the impact on increasing host plant tolerance against excessive heavy metals in soil showed that speciations of Cu, Zn, and Pb changed significantly in the rhizosphere of arbuscular mycorrhiza.

Tall fescue plants survived the Pb soil treatments of 500, 1000, and 2000 mg Pb/kg dry soil but displayed stunted growth and lower biomass especially at the highest level of soil Pb treatments. This apparently indicated that Wautersia metallidurans and Pseudomonas monteilii could protect their host plants from the phytotoxicity of excessive Pb. A similar finding was reported by Jing and his colleagues [25] who found that mycorrhiza may have played a part in protecting plants from copper, zinc and lead by changing the speciation from bioavailable to the non-bioavailable form. They further reported that copper and zinc accumulation in the roots and shoots of mycorrhiza-infected plants were significantly lower than those in the non-infected plants, which might also suggest that mycorrhiza efficiently restrict excessive copper and zinc absorptions into the host plants [25]. Our data further suggest that microbial inoculation may have increased biomass of fescue plants especially at lower (500, and 1000 mg Pb/kg dry soil) Pb soil concentrations.

There has been at least one report that EDTA alone was more effective than microbial inoculation in increasing the concentrations of all metals in corn and sunflower plants [26]. We, however, found that EDTA in combination with Wautersia metallidurans and Pseudomonas monteilii increased lead concentrations in wheat and tall fescue in both sterile and non-sterile soils that were used in this study.

Chemicals such as EDTA and acetic acid applied sequentially can access different soil components which can then bind and/or release lead when subjected to certain conditions [27-29]. While the addition of synthetic chelates has been shown to stimulate the release of metals into soil solution and enhance the potential uptake of metals into roots, it has been documented that the addition of EDTA tends to increase the risk of spreading contamination due to high solubility of Pb-chelate complex [30]. Recent research aims are to eliminate this risk by implementing alternative chelate formulations and innovative agronomic practices.

It has been shown that in plants growing in Pb contaminated soils, Pb translocation from roots to shoots was less than 30% even for the best Pb-translocating variety. Moreover, actively growing roots provide a barrier which restricts the movement of Pb to the above ground parts of the plants [31]. This point was further substantiated by previous findings of Kumar and his colleagues [32] which showed that significant Pb translocation to the shoots of Indian mustard and other species was observed only at relatively high concentrations of Pb in the hydroponic solution and only after the Pb-binding capacity of the roots was partially saturated.

Results from this study showed that the highest Pb translocation index of tall fescue was observed in non-sterile soils and at relatively high concentrations of Pb with the addition of EDTA.

CONCLUSIONS

The success of phytoextraction process depends upon both shoot biomass and shoot metal concentration. Therefore, the potential effectiveness of each plant for phytoremediation was evaluated through determination of the metal accumulation inside the plant i.e. (metal concentration x plant dry weight). The heavy metal removal by plant shoots is an important index which is useful for the practical application of treatments. Our results showed that there were significant differences in the uptake of the heavy metals exhibited by plants exposed to various treatments. Further, we found that the biomass of tall fescue shoots and roots (Figures 5-8) decreased dramatically when grown in soils spiked with 2000 mg Pb/kg dry soil.

We found no indication that the two bacteria species used in this study, Pseudomonas monteilii and Wautersia metallidurans, had an effect on the growth of tall fescue plants that were grown in sterile and non-sterile soils. While it was generally observed that the highest amounts of Pb uptake was evident in plants treated with a combination of EDTA and rhizobacteria, more research is needed to elucidate the combined effects of rhizobacteria and EDTA on uptake and growth of plants grown especially in soils contaminated with elevated levels of Pb. We conclude that further analyses and technical refinements are needed on the use of rhizobacteria in phytoextraction.

ACKNOWLEDGEMENT

Support for this research was provided by the Title III Program: Strengthening the Environmental Science Ph.D. Program in Research, a grant funded by the U.S. Department of Education--Grant No. P031B090210. Also, this publication was made possible through partial support provided by NASA through the University of Mississippi (to JSU) under the terms of grant No. NNX10AJ79H. The opinions expressed herein are those of the authors and do not necessarily reflect the views of NASA or the University of Mississippi.

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Miriam Ighoavodha, Gloria Miller, Maria Begonia, and Gregorio Begonia

Plant Physiology/Microbiology Laboratory, Department of Biology, P.O. Box 18540, College of Science, Engineering, and Technology, Jackson State University, 100 Lynch Street, Jackson, Mississippi, 39217, USA

Corresponding authors: maria.f.begonia@jsums.edu; gregorio.begonia@jsums.edu

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