MaryJane Incorvia Mattina

Concurrent plant uptake of heavy metals and persistent organic pollutants from soil

The extent of anthropogenic environmental pollution—in the United States (Black, 1999; Glass, 1999), in the European Union (Chaudhry et al., 2002), and in the third world is well documented. For example, the Food and Agriculture Organization of the United Nations has estimated that at a minimum 10 t of unwanted pesticides are in ‘‘storage’’ in undeveloped countries, with at least 2 10 t in African countries (Chaudhry et al., 2002). The potential for negative impacts of these stocks on humans and the environment is of major concern. In situ remediation techniques, such as phytoremediation— the attenuation of pollution through the use of plants—which impose minimal environmental disturbance, offer economic, agronomic, and societal benefits to all countries. Up to the present time phytoremediation of soilborne heavy metals and of organic contaminants has been pursued as two distinct disciplines. This compartmentalized approach applies to fundamental studies of the mechanisms of action, as well as to the development of remediation technologies. Based on data from the authors’ laboratories over the preceding several years we propose that far more convergence as opposed to divergence in the underlying plant physiology and soil science impacts the soil/vegetation microcosm to attenuate both soil-borne heavy metals and organic pollutants. For example, our published research has established that zucchini (Cucurbita pepo L.) and spinach (Spinacia oleracea) bioaccumulate soil-bound persistent organic pollutants (POPs) (Mattina et al., 2002). Other published reports have shown that spinach bioaccumulates heavy metals from soil (Romer and Keller, 2001). The data which are presented here demonstrate that these two plants simultaneously bioconcentrate and translocate both categories of weathered, soil-bound pollutant. Such simultaneous uptake and translocation of heavy metal and organic pollutants, if confirmed and optimized, could have enormous implications for plant/soil interaction mechanisms, and impact on practical remediation approaches, and ultimately on risk to human health.

Influence of Citric Acid Amendments on the Availability of Weathered PCBs to Plant and Earthworm Species

A series of small and large pot trials were conducted to assess the phytoextraction potential of several plant species for weathered polychlorinated biphenyls (PCBs) in soil (105 μ g/g Arochlor 1268). In addition, the effect of citric acid on PCB bioavailability to both plants and earthworms was assessed. Under small pot conditions (one plant, 400 g soil), three cucurbits (Cucurbita pepo ssp pepo [zucchini] and ssp ovifera [nonzucchini summer squash], Cucumis sativus, cucumber) accumulated up to 270 μg PCB/g in the roots and 14 μg/g in the stems, resulting in 0.10% contaminant removal from soil. Periodic 1 mM subsurface amendments of citric acid increased the stem and leaf PCB concentration by 330 and 600%, respectively, and resulted in up to a 65% increase in the total amount of contaminant removed from soil. Although citric acid at 10 mM more than doubled the amount of PCB desorbed in abiotic batch slurries, contaminant accumulation by two earthworm species (Eisenia foetida and Lumbricus terrestris) was unaffected by citric acid at 1 and 10 mM and ranged from 11–15 μg/g. Two large pot trials were conducted in which cucurbits (C. pepo ssp pepo and ssp ovifera, C. sativus) and white lupin (Lupinus albus) were grown in 70 kg of PCB-contaminated soil. White lupin was the poorest accumulator of PCBs, with approximately 20 μ g/g in the roots and 1 μ g/g in the stems. Both C. pepo ssp ovifera (summer squash) and C. sativus (cucumber) accumulated approximately 65–100 μ g/g in the roots and 6–10 μ g/g in the stems. C. pepo ssp pepo (zucchini) accumulated significantly greater levels of PCB than all other species, with 430 μg/g in the roots and 22 μ g/g in the stems. The mechanism by which C. pepo spp pepo extracts and translocates weathered PCBs is unknown, but confirms earlier findings on the phytoextraction of other weathered persistent organic pollutants such as chlordane, p,p′-DDE, and polycyclic aromatic hydrocarbons.

Plant uptake and translocation of highly weathered, soil-bound technical chlordane residues: Data from field and rhizotron studies

It has been observed that plants are susceptible to uptake from soil and in planta transport of technical chlordane, in spite of its hydrophobicity and sequestration within the soil matrix due to weathering. Field and rhizotron studies were conducted with Cucurbitaceae planted in highly weathered, chlordane-contaminated soil to investigate details of soil-to-plant contaminant uptake. In the field-work, Cucurbita pepo L. (zucchini) was grown in soil at four levels of chlordane contamination: Clean (<limits of quantitation, 5 ng/g), low (average, 370 ng/g), medium (average, 1,951 ng/g), and high (average, 4,572 ng/g). The analysis of plant tissues (root, stem, leaf, and fruit) resulted in the detection of chlordane consistently at the highest concentration in the root tissue at each level of soil contamination. As the soil chlordane concentration increased, the average chlordane concentration in the root tissue increased as follows: Clean, 370 ng/g; low, 8,130 ng/g; medium, 21,800 ng/g; high, 29,400 ng/g. Further analysis of the field-grown plants showed distinct differences in both the proportional distribution of chlordane among the plant tissues and the pattern of the chlordane residues in each tissue type. These differences are attributed to plant uptake from soil versus uptake from air. In the rhizotron studies, uptake of chlordane residues by C. pepo L. was compared with that of another Cucurbitaceae, Cucumis sativus L. (cucumber). Xylem sap from the rhizotron-grown plants was collected and analyzed for chlordane, in addition to determination of chlordane residues in soil, roots, and aerial plant tissue. Component fractions and enantiomer fractions of both chiral and achiral chlordanes were followed through soil, root, xylem sap, and aerial tissue compartments. They indicate that the xenobiotic residues translocate enantioselectively from the soil matrix into and through the plant environment with genera-specific patterns. The determination of chlordanes at ng/g concentration explicitly for the first time in the xylem sap of plants grown in contaminated soil confirms the presence of a soil-sequestered and highly hydrophobic organic contaminant within the aqueous plant environment.

Phytoextraction of weathered p,p'-DDE by zucchini (Cucurbita pepo) and cucumber (Cucumis sativus) under different cultivation conditions.

ABSTRACT Previous studies have shown that zucchini (Cucurbita pepo) and cucumber (Cucumis sativus) under field conditions are good and poor accumulators, respectively, of persistent organic pollutants from soil. Here, each species was grown under three cultivation regimes: dense (five plants in 5 kg soil); nondense (one plant in 80 kg soil); and field conditions (two to three plants in approximately 789 kg soil). p,p′-DDE and inorganic element content in roots, stems, leaves, and fruit were determined. In addition, rhizosphere, near-root, and unvegetated soil fractions were analyzed for concentrations of 11 low-molecular-weight organic acids (LMWOA) and 14 water-extractable inorganic elements. Under field conditions, zucchini phytoextracted 1.3% of the weathered p,p′-DDE with 98% of the contaminant in the aerial tissues. Conversely, cucumber removed 0.09% of the p,p′-DDE under field conditions with 83% in the aerial tissues. Under dense cultivation, cucumber produced a fine and fibrous root system not observed in our previous experiments and phytoextracted 0.78% of the contaminant, whereas zucchini removed only 0.59% under similar conditions. However, cucumber roots translocated only 5.7% of the pollutant to the shoot system, while in zucchini 48% of the p,p′-DDE in the plant was present in the aerial tissue. For each species, the concentrations of LMWOA in soil increased with increasing impact by the root system both within a given cultivation regime (i.e., rhizosphere > near-root > unvegetated) and across cultivation regimes (i.e., dense > nondense > field conditions). Under dense cultivation, the rhizosphere concentrations of LMWOAs were significantly greater for cucumber than for zucchini; no species differences were evident in the other two cultivation regimes. To enable direct comparison across cultivation regimes, total in planta p,p′-DDE and inorganic elements were mass normalized or multiplied by the ratio of plant mass to soil mass. For cucumber, differences in total p,p′-DDE and inorganic element content among the cultivation regimes largely disappear upon mass normalization, indicating that greater uptake of both types of constituents in the dense condition is due to greater plant biomass per unit soil. Conversely, for zucchini the mass normalized content of p,p′-DDE and inorganic elements is up to two orders of magnitude greater under field conditions than under dense cultivation, indicating a unique physiological response of C. pepo in the field. The role of cultivation conditions and nutrient availability in controlling root morphology, organic acid exudation, and contaminant uptake is discussed.

Tracking chlordane compositional and chiral profiles in soil and vegetation

The cycling of chlordane and other persistent organic pollutants through the environment must be comprehensively elucidated to assess adequately the human health risks posed from such contaminants. In this study the compositional and chiral profiles of weathered chlordane residues in the soil and vegetative compartments were investigated in order to provide details of the fate and transport of this persistent pesticide. Zucchini was planted in a greenhouse in three bays containing chlordane-contaminated soil. At harvest the vegetation and soil were extracted and analyzed for chlordane content using chiral gas chromatography/ion trap mass spectrometry. Both achiral and chiral chlordane components were quantified. The chlordane concentration in the rhizosphere (soil attached to roots) was significantly less than that in the bulk soil. However, the enantiomeric ratio of the chiral components and overall component ratios had changed little in the rhizosphere relative to the bulk soil. Significant levels of chlordane were detected in the vegetation, the amount varying in different plant tissues from a maximum in roots to a minimum in fruit. In addition to the chlordane concentration gradient in plant tissues, significant shifts in compositional profile, as indicated by the component ratios, and in chiral profile, as indicated by the enantiomeric ratio, of the contaminant were observed in the plant tissues. The data indicate that abiotic processes dominate the transport of the chlordane components through the soil to the plant. This is the first report of the effect of rapid biotic processes within the plant compartment on chlordane compositional and chiral profiles.

Characterization of substances released from crumb rubber material used on artificial turf fields

Crumb rubber material (CRM) used as infill on artificial turf fields can be the source of a variety of substances released to the environment and to living organisms in the vicinity of the CRM. To assess potential risks of major volatilized and leached substances derived from CRM, methods were developed to identify organic compounds and elements, either in the vapor phase and/or the leachate from CRM. A qualitative method based on solid phase micro-extraction (SPME) coupled with gas chromatography/mass spectrometry (GC-MS) was developed to identify the major volatile and semi-volatile organic compounds out-gassing from CRM samples under defined laboratory conditions. Direct vapor phase injection into the GC-MS was applied for the quantitative analysis. Ten organic compounds were identified in the vapor phase by the SPME method. Volatile benzothiazole (BT) was detected at the highest level in all commercial CRM samples, in the range 8.2-69 ng g(-1) CRM. Other volatile PAHs and antioxidants were quantified in the vapor phase as well. A decrease of volatile compounds was noted in the headspace over CRM samples from 2-years-old fields when compared with the virgin CRM used at installation. An outdoor experiment under natural weathering conditions showed a significant reduction of out-gassing organic compounds from the CRM in the first 14 d; thereafter, values remained consistent up to 70 d of observation. Zinc was the most abundant element in the acidified leachate (220-13000 microg g(-1)), while leachable BT was detected at relatively low amounts.

Plant uptake and translocation of air-borne chlordane and comparison with the soil-to-plant route.

In order to assess fully the impact of persistent organic pollutants (POPs) on human health, pollutant exchange at the interface between terrestrial plants, in particular food crops, and other environmental compartments must be thoroughly understood. In this regard, transfers of multicomponent and chiral pollutants are particularly informative. In the present study, zucchini (Cucurbita pepo L.) was planted in containerized, uncontaminated soil under both greenhouse and field conditions and exposed to air-borne chlordane contamination at 14.0 and 0.20 ng/m(3) (average, greenhouses), and 2.2 ng/m(3) (average, field). Chiral gas chromatography interfaced to an ion trap mass spectrometer was used to determine the chiral (trans-chlordane, TC, and cis-chlordane, CC) and achiral (trans-nonachlor, TN) chlordane components in vegetation, air, and soil compartments. The chlordane components of interest were detected in all vegetation tissues examined--root, stem, leaves, and fruits. When compared with the data from a soil-to-plant uptake study, the compositional profile of the chlordane components, i.e. the component fractions of TC, CC, and TN, in plant tissues, showed significantly different patterns between the air-to-plant and soil-to-plant pathways. Changes in the enantiomer fractions of TC and CC in plant tissues relative to the source, i.e. air or soil, although observed, were not markedly different between the two routes. This report provides the first comprehensive comparison between two distinct plant uptake routes for POPs and their subsequent translocation within plant tissues.

Factors affecting the phytoaccumulation of weathered, soil-borne organic contaminants: analyses at the ex Planta and in Planta sides of the plant root

Persistent Organic Pollutants (POPs) in the soil–plant system were tracked from their origin in the bulk soil, into the rhizosphere soil pore water, to the xylem sap, and up to the aerial plant tissue. Specifically, the profiles of both chiral and achiral components of technical chlordane along this continuum were examined in detail for members of the Cucurbitaceae family: Cucurbita pepo L. subsp. pepo (“Black Beauty” true zucchini), Cucurbita pepo L. intersubspecific cross (“Zephyr” summer squash), and Cucumis sativus (“Marketmore” cucumber). The experiments were based on the use of mini-rhizotrons for collection and analysis of rhizosphere soil pore water for organic pollutants, as well as for low molecular weight organic acids (LMWOAs). In addition, the xylem sap and aerial plant tissue for intact, homografted, and heterografted C. pepo “Black Beauty” and C. sativus “Marketmore” plants were compared. The data indicate that profiles of the chlordane components in the pore water show no alteration in chiral patterns from those in the bulk soil and may be interpreted by physicochemical partitioning coefficients. Low molecular weight organic acids (LMWOAs) in the rhizosphere were observed to have a minor impact on bioavailability of the pollutants. However, once the pollutants cross the root membrane, major distinctive uptake and enantioselective patterns are apparent in the xylem sap, which are maintained in the aerial tissue. These in planta patterns are based on plant genotype. Specifically, grafting experiments with compatible heterografts of C. pepo and C. sativus establish that the chiral patterns are fully dependent on the plant root. The genotypic dependence of the data suggests possible mechanisms for phytoaccumulation.