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VIII. Current Phytoremediation Research and Development

VIII. Current Phytoremediation Research and Development

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rally, they are not common constituents of most soils and may be resistant to

biodegradation primarily because of their insolubility, molecular size, toxicity,

and/or inherent chemical bond energies and configuration. Although use of these

compounds as pesticides or industrial chemicals has dramatically decreased or

ceased in many countries, their persistence has contributed to their continued

detection in the environment and occurrence at hazardous waste sites. Despite this

persistence, the degradation of some chlorinated hydrocarbons has been shown to

be enhanced in the rhizosphere or by microorganisms from rhizosphere soil

compared to nonvegetated soils.

Pentuchlorophenof (PCP) is a widespread chlorinated hydrocarbon contaminant, especially in soil around wood treatment plants. At high concentrations,

PCP is often quite persistent due to its toxicity to a variety of soil organisms. One

approach to remediation of PCP-contaminated soil has been inoculation with

microorganisms capable of metabolizing PCP (Crawford and Mohn, 1985);however, survivability of inoculated organisms is often limiting. Ferro and coworkers ( 1994) explored the possibility of using rhizosphere microorganisms to

accelerate PCP degradation. Crested wheatgrass (Agropyron desertorurn) was

tested for the ability to enhance mineralization of 14C-PCP in a flow-through

soil-plant system in the laboratory. Mineralization of 1%-PCP in the vegetated

system was 22% of the applied 14C after 155 days, whereas only 6% of the 14CPCP was mineralized in the nonvegetated system. A significant portion of the

I4C-PCP and/or metabolites (36%)was taken up by the plants. Leaching of 14CPCP and/or metabolites was greater in the nonvegetated system. Overall, the

vegetated soil had lower levels of PCP-derived material than the nonvegetated

soils at the conclusion of the experiment. Thus, vegetation was beneficial in

increasing mineralization of PCP as well as reducing leaching of PCP and its

metabolites.

Trichloroethylene ( I , I ,2-trichloroethylene) (TCE) is one of the most common

substances found at hazardous wastes sites and in contaminated groundwater.

Walton and Anderson (1990) previously observed accelerated degradation of

TCE in slurries of rhizosphere soil collected from four plant species at a former

solvent disposal site and enhanced mineralization of I4C-TCE in rhizosphere soil

samples. However, the authors speculated that the absence of a living plant may

have lead to conservative estimates of degradation for TCE, and in subsequent

experiments utilizing soil-plant systems composed of soil and vegetation from

the same contaminated field site showed significant mineralization of 14C-TCE.

In this study, specially designed Erlenmeyer flasks were used to monitor the fate

of “T-TCE in the soil-plant systems. In addition to the vegetated samples,

nonvegetated and sterile soil samples were included as separate treatments for

each experiment. The flasks were sealed by coating a nonreactive silicone rubber

sealant between the plant stem and the flask. At 24-hr intervals, headspace within

the flasks was flushed through a series of traps for removing IT-volatile com-



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pounds and W02.Analysis of the I4CO2traps from the experiments showed

that I4CO2production in the vegetated soils was elevated compared with both the

nonvegetated soil and the sterile control soil. In the experiments with soils

containing Lespedeza cuneatu and Pinus tuedu, I4CO2production at the conclusion of the experiment was significantly greater than I4CO, production in nonvegetated and sterile (autoclaved) control soils (Anderson and Walton, 1992,

1995). Most of the 14C02produced from 14C-TCE in the vegetated soils evolved

during the initial 3 days of the experiment. This is in agreement with earlier

observations on the initially rapid disappearance of TCE from the headspace

above aqueous slurries of rhizosphere soil (Walton and Anderson, 1990). In

addition, comparisons of the percentage of I4C-TCE mineralized in the whole

plant systems with previous data on “T-TCE mineralization in L . cuneata rhizosphere soil appeared to confirm the hypothesis that the mineralization rates based

on rhizosphere soil samples gave conservative estimates of mineralization that

would occur in soil containing a living plant.

Polychlorinated biphenyls (PCBs)provide another research story of particular

interest in the relationships between rhizosphere microorganisms and plants.

While the use of microorganisms for remediation of PCB-contaminated environments has been the focus of research for the last 10 years, recently the use of

vegetation for enhancing microbial degradation has also been explored (Donnelly

et a / ., 1994; Donnelly and Fletcher, 1995; Brazil et a / ., 1995).

The use of ectomycorrhizal fungi for bioremediation is a potential technology

for overcoming some of the survival limitations of soil inoculation. The symbiotic relationship of plant-ectomycorrhizal systems may give the fungus a better

chance to compete against indigenous soil microflora and subsequently increase

PCB metabolism in contaminated soils. Donnelly and Fletcher (1995) explored

the metabolism of a PCB stock solution containing 10 or 11 different PCB

congeners (2-6 C1) by ectomycorrhizal fungi in culture flasks over 5 days. Of the

21 fungal species tested, 14 were capable of some PCB metabolism. The number

of congeners metabolized ranged from 0 to 7 and varied among the fungal

species. As expected, the lower-chlorinated congeners were more easily metabolized. Radiigera atrogleba and Cautieria crispa metabolized the most PCB congeners. An interesting note familiar to many in the bioremediation area is that

there was no correlation between taxonomically related species and metabolism

of structurally similar congeners.

Donnelly and co-workers (1994) have also been exploring the use of PCBdegrading bacteria in combination with plants. Previous research from the group

at General Electric (Bedard et a / . , 1986) identified several aerobic bacteria

capable of PCB metabolism. However, success with these organisms in the field

has been limited by the requirement of biphenyl as a cosubstrate. The need to

find other compounds which stimulate the growth of PCB-degrading bacteria led

Donnelly and co-workers to hypothesize that naturally occurring compounds



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produced by plants may be useful. The growth of three bacterial strains shown to

degrade PCB was tested using several known plant compounds including flavonoids and coumarins. Growth on biphenyl served as a control. Several of the

plant compounds supported growrh of the bacterial strains as well as or better

than biphenyl. In addition, bacterial strains grown on the plant compounds

retained the ability to metabolize certain PCB congeners. Results of these studies

suggest that certain plant species or stages of plant growth might be valuable for

enhancing PCB degradation in soil.

Plants can select for different rhizosphere microbial communities. It remains

unproven, however, whether this selection affects degradative rates in the field.

Whether this selection potential translates into differences in the rates of microbial degradation of organic compounds remains to be proven. It is on this premise, however, that recent research by Fletcher et al. (1995) has screened and

selected plants for specific exudate patterns and has examined the rate and timing

of the release of these compounds into the rhizosphere environment.



2. Remediation in Plantu

As mentioned above, research on pesticides has shown that plants have four

known types of reactions which result in the breakage of the C-Cl bound. These

reactions include: (1) monoxygenases, (2) glutathione (or homoglutathoine)

S-transferases, (3) (anti)auxin cell receptor binding (that converts a C-Cl to a CS protein), and (4) a nonenzymatically catalyzed replacement of a C1 to an OH

(in certain aromatic configurations, e.g., triazines). Other mechanisms of C-Cl

bond breakage undoubtedly exist; however, they have not been actively researched.

The capacity of plants to metabolize PCBs has been studied by Groeger and

Fletcher (1988). The extensive screening on whole plant showed a number of

differences in metabolic capacity between plants. To ascertain whether this was

plant metabolism or a microbial-plant community, Groeger and Fletcher went

further and produced and screened plant tissue culture (free from microbial

associations) for PCB metabolism. Cell cultures of rose (Rosa sp., cv. Paul’s

Scarlet) were found to have among the best ability to metabolize PCBs, but the

completeness of metabolism was dependent upon specific PCB congeners.

Recent work on trichloroethylene in hybrid poplar trees has shown that the

plant is relatively insensitive to the presence of the compound and shows no ill

growth effects at 100 mg/liter TCE (many times higher than the level deemed

safe in drinking water). The TCE is taken into the plant and has two detectable

fates: it is either metabolized or bound. The metabolic process produces 2,2,2trichloromethanol and di- and trichloroacetic acid compounds, which would

suggest the presence of an active TCE metabolizing P450 enzyme (Strand et al.,

1995). In addition, a large fraction of the TCE taken up by the plant roots



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becomes bound and unavailable to chemical solvent extraction. More work on

this fraction is also needed from a mechanistic as well as an ecotoxicological

perspective. Based on previous results, this bound fraction may also be unavailable to animals, microbes, and other environmental receptors. Binding pollutants

into the woody tissue of long-lived trees may prove to be an acceptable phytostabilization strategy. A field test of these poplar trees has recently been installed by these same researchers.



C. PESTICIDES

The widespread use of pesticides during the last 40 years has facilitated the

growth of retail agrochemical dealerships. Unfortunately, many of these dealerships have experienced soil and water contamination problems from normal

operating procedures and accidents. At pesticide-contaminated sites, a potential

limitation to using vegetation exists because of the presence of mixtures of

herbicide contaminants. Nonetheless, herbicide-resistant plants exist at these

sites, and rhizosphere soils from these plants have previously shown the ability to

degrade mixtures of herbicides (Anderson et u l . , 1994). In addition, previous

studies on the herbicide-degradative capability of rhizosphere soils of other plant

species (Sandmann and Loos, 1984; Lappin et a[., 1985) help support the use of

vegetation in remediating pesticide-contaminated sites. The use of plants in the

remediation process for these materials is also a logical extension of ongoing

research in the landfarming (surface tilling and fertilization) of these same materials (Felsot and Shelton, 1993).

1. Rhizosphere Degradation



Anderson and co-workers have conducted studies utilizing soils and plants

from pesticide-contaminated sites. Preliminary studies indicated increased degradation of atrazine, trifluralin, and metolachlor in rhizosphere soil from Kochia

scoparia. a herbicide-resistant plant, compared with nonvegetated soil (Anderson et a l . , 1994). Subsequent experiments indicated that mineralization of 1%atrazine in soil treated with a mixture of atrazine and metolachlor at concentrations typical of point-source contamination (50 x g/g each) was significantly

greater in rhizosphere soil from Kochia scoparia than in nonvegetated and control soils (Perkovich et a l . , 1995). Soils were collected from an agrochemical

dealership contaminated with several herbicides, including atrazine, metolachlor, trifluralin, and pendimethalin at concentrations well exceeding the field

application rates. Mineralization rates of ring-labeled atrazine in both rhizosphere and nonvegetated soils were quite high (>47% of the initial 14C applied

after 36 days) compared to literature values. Based on the relatively rapid miner-



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alization half-lives of atrazine in both soils, it does not appear that the presence

of metolachlor at 50 pg/g had a negative influence on the degradation. This

research supports the use of rhizosphere microorganisms associated with

herbicide-resistant plants to enhance microbial degradation of atrazine in soil at

contaminated sites. Naturally occurring plants, such as K . scoparia, appear to

have the capacity to be used as in sifu agents of bioremediation by facilitating the

proliferation of microorganisms in surface soil with the ability to mineralize high

concentrations of atrazine.

Anderson and Coats (1995) have also screened other rhizosphere soils from

waste areas for their ability to degrade atrazine and metolachlor. Several soil

samples exhibited the ability to mineralize high concentrations of I4C-atrazine.

These included rhizosphere soils from lambsquarters (Chenopodium berlundieri), foxtail barley (Hordeumjubatum), witchgrass (Panicum capillare), catnip

(Nepeta cataria), and musk thistle (Carduus nutans). Of the 14 species (eight

families) tested, the greatest mineralization of 14C-atrazine was observed in

rhizosphere soils from musk thistle (33.1-1.7%) and catnip (24.1-1.2%). However, none of the 14 rhizosphere samples tested exhibited a positive response for

14C-metolachlormineralization.



2. Remediation in Plan@

Actually, modern pesticides, and in particular herbicides, are an ideal target

for phytoremediation. The materials are designed for application on soil and

plant systems. Herbicides which are designed to be applied to the bare soil at

planting, or prior to planting, are specifically designed to move through the soil

to the plant root, be taken up by the plant roots, and be metabolized by the

tolerant species. In one sense, phytodecontarnination occurs in many farmers’

fields, as an overapplication of a pesticide may require more than one cropping

cycle to reduce its bioactivity down to a level where sensitive species can be

grown. The phenomena of “carry-over” is often considered good by farmers who

grow successive monocultures of the same crop (as it reduces their need for

reapplication), but bad by farmers who try to replant with sensitive rotational

crops.

Many farmers will relate stories of altering crop management schemes to

accommodate a spill or miss-application (due to incorrect dilution procedures or

malfunctioning equipment). One farmer, who had planted corn into a triazine

spill a decade earlier, thought the Ph.D.’s “concept of phytoremediation of pesticides” was “about half a bucket of common sense” and then went on to inquire

what we did for a living. The mechanism of triazine uptake, degradation, and

characterization is exhaustively studied in the literature, and also apparently

practiced with some skill in the field. It is not, however, a soil decontamination

method approved by most regulatory authorities.



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D. BIOTECHNOLOGICAL

IMPROVEMENTS

IN PHYTOREMEDIATION

Over the last decade, the transformation and regeneration of microbes and

plants has advanced greatly. Genes are now commonly moved between microbial

genera, and genes cloned from a wide variety of viral, microbial, plant, and

animal sources are now routinely expressed in some plants. Genetic engineering

for enhanced phytoremediation is in its infancy, yet progress is being made.

Progress has been made in finding and cloning potentially useful genes, transforming and regenerating appropriate species, altering plant characteristic

morphology, changing plant metabolism, and adding degradative capacity to the

rhizosphere.



1. Degradative Genes

A wide variety of microbial genes that can metabolize xenobiotics have now

been cloned. A small portion of these have been expressed in plant tissue. The

primary purpose behind most of this work to date has been to increase the

tolerance of a crop plant to a particular herbicide. Such altered plants may

increase the sales of the associated herbicides. Examples of this include: ( 1 )

Alzodef tolerance conferred on tobacco by the introduction of the cah gene from

the fungus Myrothecium verrucaricr (Maier-Greiner et ul., 199l ) , ( 2 ) Glofosinate

tolerance in tobacco and potato with the bar gene from Strepromyces hyet al., 1989), and ( 3 ) a glyphosate metabolism system that

g r o s c o p i c ~(DeGreef

~

may be used in conjunction with the altered tolerance genes (again a microbial

source) in “Round-up ready” germplasm developed by Monsanto. In addition to

these, P450s have been cloned from microbial, plant, and mammalian tissues.

Some of these, including mammalian genes, also have been expressed in plants

(Saito et al., 1991). Many molecular labs are now in the process of isolating the

genes responsible for a specific metabolic activity in microbial, plant, or animal

systems. Insect populations resistant to specific insecticides have even provided a

source of novel glutathione S-transferase activity (Thompson er a l . , 1994). These

genes are being cloned and eventually expressed in plant tissues. In some cases,

the molecular strategy has needed some adjustment (e.g., whole-plant, constitutive expression of a gene coding for the metabolism of a PCB is unlikely to

succeed as PCBs are a lipophilic contaminant that, if available, are tightly bound

into the outer layers of the plant root). Although the molecular biology may be of

intrinsic interest, justifying the project on the basis of phytoremediation potential

is difficult. The best use of molecular biological tools is as part of an integrated

phytoremediation team. To a large degree, the limiting factors in phytoremediation are unknown and hence difficult to target with molecular biological skills.

Relatively few recombinant plants have been made specifically for the purpose

of phytoremediation, however the microbial genes chlorocatechol 1,2-dioxyge-



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nase, catechol 2,3-dioxygenase (Gordon et al., 1990), and chlorophenol hydroxylase (Stomp el al., 1994) have all been engineered into plants for that

purpose.



2. Other Targets

Much is known about the plant metabolic pathways that produce bioactive

compounds. Of particular interest is the regulation of pathways that determine

the plant’s production of microbial signal molecules, antibiotics, pigments, and

xenobiotic pollutant analogs. The biosynthesis of many of these molecules is

increasingly well understood (Kubasek ef al., 1992), and in some cases genes

(e.g., PAL pathway genes) have been isolated and cloned into vectors appropriate for phytoremediation work. Work at this level would be more likely to

produce research tools than to actually produce field plants at the moment;

however, the prospects are intriguing. Producing paired plants differing in only

one trait (e.g., 100-fold difference in tannin or phenolic exudation) would provide phytoremediation with much needed tools. Other targets of biotechnology

might include altered lignin production or incorporation into cell walls (for

increased phytostabilization), increased lipid concentration or quality in the roots

(for all forms of phytoremediation), altered root permeability, and altered infectivity by mycorrhizae.



3. Plant Transformation

Unfortunately, not all species of plants are equally amenable to transformation

and regeneration. After nearly a decade’s worth of work, monocots and many

trees are still proving difficult to transform and regenerate on a routine basis.

Since many of the target plants for phytoremediation include these types of

plants, we believe continued effort in plant transformation will eventually prove

useful to phytoremediation. In one species, now in trials, altered rooting

morphology was obtained by Agrobucferium rhizogenes transformation (Han et

af., 1993). The resulting trees had greatly increased root mass, surface area, and

soil/root contact. This shows that some tree species are indeed amenable to

molecular techniques, and schemes for their improvement in phytoremediation

have been proposed (Stomp ef al., 1994).



4. Microbial Biotechnology

Not all biotech efforts in phytoremediation are directed to the plant component. Efforts at creating “biased rhizospheres” where microbes have additional

degradative capacities are ongoing in a number of labs working with biocontrol

of plant pests, nitrogen fixation, plant-growth promotion, and myconhizae.



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Few workers have attempted to combine molecular biology, microbial competition in the rhizosphere, and microbial degradation of xenobiotics. One exception is research by Brazil and co-workers (1995). They have inserted the genes

(bph) encoding the biphenyl degradative pathway into the chromosome of two

rhizosphere pseudomonads. Results of tests on the genetically engineered organism demonstrate that growth rate, bph gene expression and stability, and colonization potential of the rhizosphere were not seriously affected. It may therefore

be possible to genetically engineer rhizosphere competent pseudomonads without compromising their competence. Importantly, expression of the bph genes

was detected in rhizosphere soil microcosms. The authors suggest that expanding

the degradative capabilities of rhizosphere-competent microorganisms might be a

good method for generating useful strains for bioremediation applications.



IX. CONCLUSIONS

Phytoremediation is an exciting nascent technology. Its development represents an opportunity for cross-discipline research teams to produce a new, and

much needed, technology to remediate environmental contamination. Research

at all levels is needed. We lack many of the fundamental understandings on the

interactions between the system components (plants, their microbial communities, contaminants, and soil, water, and the atmosphere) and field and engineering installation and equipment development. The ability to use natural ecosystems to remediate the environmental damage done by industrial and urban

activites has generated excitement among technologists, owners of contaminated

sites, regulators, and the popular press. Delivering a widely applicable technology, acceptable to the scientific, regulatory, and political communities, is the

current challenge before the research community.



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