USING VEGETATION TO ENHANCE IN SITU BIOREMEDIATION

L.E. Erickson, M.K. Banks, L.C. Davis, A.P. Schwab, N. Muralidharan, and K. Reilley
Center for Hazardous Substance Research
Ward Hall
Kansas State University
Manhattan, Kansas 66506
and

J.C. Tracy

Department of Civil Engineering
South Dakota State University
Brookings, SD 57007

ABSTRACT

Vegetation can enhance in situ bioremediation processes in many applications. Microbial transformations occur in the soil external to the plant roots. Organic contaminants also enter vegetation and are transformed within plants. Research progress is reviewed with emphasis on recent experimental results and mathematical models of contaminant fate in systems where vegetation is present. Evapotranspiration by plants provides a solar driven pump-and-treat system which helps bring contaminants to the rhizosphere and helps contain them on the site.

M.K. Banks and K. Reilley are in the Civil Engineering Dept. L.C. Davis is in the Biochemistry Dept. L.E. Erickson and N. Muralidharan are in the Chemical Engineering Dept. A.P. Schwab is in the Agronomy Dept.

INTRODUCTION

Vegetation is found in the presence of hazardous contaminants in soils at many locations. A number of studies have been reported on the effects of vegetation on the transformation or stabilization of compounds (1-39). These studies show that there are many reasons to investigate the interactions that occur among hazardous compounds, microorganisms, plants, soil, air, and water. The plant root zone (the rhizosphere) has significantly larger numbers of microorganisms than soils which do not have plants growing in them (16); this appears to enhance the biodegradation of organic compounds. Two professional societies have included relevant technical sessions at their recent national meetings. The Air and Waste Management Association's symposium (1) was entitled "Beneficial Effects of Vegetation in Waste Treatment, Soil Remediation and Stabilization" while the American Chemical Society's three sessions (13) were entitled "Microbial Degradation of Organic Compounds in the Rhizosphere: Implications for Bioremediation."

Beneficial effects of vegetation have been reported in soils contaminated with metals as well as organic compounds. The application of vegetation to the stabilization, control, and remediation of soils contaminated with metals has been reviewed recently by Pierzynski et al. (28). The present review will be limited to organic compounds that may be transformed and inorganic compounds that may be beneficial to plants and microorganisms. The emphasis will be on recent developments that are not included in the reviews of Shimp et al. (30) and Anderson et al. (38).

Vegetation has been used beneficially in the in situ bioremediation of contaminated soil, as a biofilter to adsorb and biodegrade contaminants in air and water, and in buffer zones for control and treatment of leachate and surface waters (10, 12, 18, 22, 27, 30). Specific potential pollution prevention applications include the use of grasses and trees at the edges of fields along the banks of streams to capture and transform pesticides and fertilizers, grass waterways below animal feedlots to manage runoff associated with rainfall events, and vegetation at the edge of landfills to utilize and transform compounds in landfill leachate. Wetlands biofilter wastewater treatment systems have been developed to biodegrade organic compounds (30).

ADVANTAGES OF VEGETATION

There are several reasons for the increasing level of research on the beneficial effects of vegetation in contaminated soil. Plants use solar energy which is very inexpensive and widely available. Evapotranspiration may be viewed as a solar driven pump-and-treat system that helps to bring contaminants to the rhizosphere and contain them on the site. Plants can transform organic compounds that are assimilated through their roots and the rhizosphere provides an excellent environment for the adsorption and microbial transformation of organic compounds. Vegetation is aesthetically pleasing; it can provide information on the health of the site and a desirable habitat for wildlife. Plants can enhance oxygen transfer to microbial communities by transporting oxygen within the plant and by lowering the water table so that gas phase diffusion can occur in soil. Vegetation can be managed inexpensively and efficiently to produce biomass for chemical or energy applications. Since plants are often present at contaminated sites, it is desirable to understand how they interact with the contaminants.

MAJOR FINDINGS

Consumption and biodegradation of organic compounds is a natural part of the soilmicrobial system. If appropriate conditions are present for microbial transformation of the contaminants, plants may not be needed for biodegradation to occur. However, in many cases plants act to enrich the environment for microbial degradation. For compounds that are readily degraded aerobically, plants may enhance oxygen transfer to the root zone, for example. Efforts will be made to identify specific studies in which the beneficial effects of plants on degradation have been reported; however, it should be realized that excellent conditions for microbial biodegradation may often be established in other ways as well.

Transformation of Soluble and Biodegradable Compounds

Recent results have been presented from an investigation in which water saturated with toluene at 26 C and 0.5 ml/L of 93% phenol in water were fed into separate 1.8 m long and 35 cm deep laboratory chambers containing soil with alfalfa growing at the surface (10, 12, 22). The ground water was sampled at four sampling wells (ports 1-4) which were located along the flow path of each chamber. Ports 1 and 2 were 33 cm and 66 cm from the inlet, respectively; ports 3 and 4 were 66 cm and 33 cm from the outlet, respectively. The results presented in Tables 1-4 indicate that significant quantities of the toluene and phenol which enter are not present in the effluent. The results with toluene appear to indicate that microbial degradation occurs in the rhizosphere in the unsaturated zone. Adequate quantities of nitrogen appear to have been provided by the alfalfa. Gas phase measurements with FTIR show that the toluene is not present in the gas phase above the soil based on a detection concentration of 250 ppb (v/v) (10). Carbon dioxide is produced in the soil in sufficient quantities to account for the transformation of the toluene to carbon dioxide and water. It appears that some of the toluene in the saturated zone is not biodegraded; this may be due to a shortage of oxygen in the saturated zone.

The results for phenol in Tables 2 and 4 indicate that most of the phenol disappeared; the amount in the effluent was very small. Phenol was not found in the gas phase. The experimental results which include measurements of carbon dioxide evolution suggest that most of the phenol was transformed and biodegraded. Anaerobic biodegradation of phenol in the saturated zone may have taken place, also. Under conditions where all of the influent water is evapotranspired, it appears that all of the contaminant can be transformed and remediated.

A carbon mass balance on the two chambers together showed that about 50 mmoles/day of the inlet carbon appeared to be biodegraded. The measured production of CO2 was about 70100 mmoles/day with plants and the contaminants and about 2/3 as much when the contaminants were not being fed. Thus, approximately 23-33 mmoles carbon/day appears to be associated with CO2 production due to biodegradation of contaminants. This leaves 17-27 mmoles carbon/day associated with biomass formation and the incorporation of carbon into the soil. In one year, the organic carbon content of the soil would increase by about 0.001 g/g of soil based on this level of carbon incorporation. Because of root exudates and variations of soil organic carbon content with depth from 0. 3 % at the bottom to 1. 8 % near the surface, the increase in soil organic carbon due to biodegradation of the contaminants was not determined independently.

Root Exudates Provide Carbon and Energy for Microbial Growth

Contaminants that are not very soluble in water and those that require a source of carbon and/or energy for their transformation may be biodegraded more rapidly in the presence of vegetation. Polynuclear aromatic (PNA) compounds are not very soluble in water. April and Sims (6) and Reilley (29, 36) have shown that the biodegradation of PNA compounds is enhanced by plants. Table 5-7 contain results from the recent work of Reilley et al. (29, 36). Their results are in general agreement with the earlier work of Aprill and Sims. Disappearance (most likely due to biodegradation) of anthracene and pyrene is observed in experiments without plants as well as when plants are present; however, less of the contaminant remains when plants are present. Note that when vegetation is present (Tables 5 and 6), the contaminant concentration after 24 weeks for the contaminated spiked soil is of the same order of magnitude as the original concentration in the contaminated soil. In Table 7, it can be seen that the beneficial effect of root exudates is simulated by adding organic acids to the soil. This enhances the microbial populations in the soil which leads to the evolution of greater amounts of carbon dioxide from radiolabeled pyrene. Lee and Banks (16) have reported that microbial counts are significantly larger when vegetation is present in soils contaminated with PNA compounds. A mathematical model which predicts that root exudates will have a beneficial effect on the biodegradation of compounds that are not very soluble in water has been proposed by Davis et al. (11).

The uptake of anthracene and pyrene by alfalfa and fescue plants has been investigated by Al-Assi (2). He concludes that these compounds do not accumulate in these plants.

Anderson (3) has reported that the rhizosphere of growing plants has a beneficial effect on the transformation of trichloroethylene (TCE). When growing plants were present, the microbial activity, biomass, and degradation of TCE in rhizosphere soils were found to be significantly greater than corresponding nonvegetated soils (3,5,35). The presence of vegetation had a positive effect on the transformation of TCE to carbon dioxide.

Ferro et al . (37) has reported that mineralization rates of pentachlorophenol are 3 . 5 times greater in vegetated soil where Hycrest crested wheatgrass (Agropyron desertorum) is growing compared to soil without vegetation. Pentachlorophenol was also found in the plant roots and shoots. At an initial concentration of 100 mg/kg dry weight of soil, the growth of the vegetation was affected by the pentachlorophenol.

Beneficial Transformations Occur in Plants

Some compounds are taken up by plants and transformed within the plants. Licht (18), Nair et al. (25, 26), Nair and Schnoor (23, 24), and Paterson and Schnoor (27) have reported that atrazine and nitrates are taken up and transformed by plants in the riparian zone. Poplar trees and associated vegetation have been shown to significantly reduce the concentrations of nitrate in riparian zones. This agricultural pollution prevention application is being investigated further by Licht and coworkers.

Bedell (9) and Mueller et al. (20, 21), have investigated the late of explosive compounds such as di-and trinitrotoluenes (DNT and TNT) in the presence of plants. The results show that uptake and biotransformation of nitrated toluenes occurs when Jimson weed (Datura innoxia) and Lycopersicon peruvianum, a wild tomato species, are grown in soils containing DNT and TNT. Radiolabeled TNT was transformed to aminobenzyl alcohols, aminobenzaldehydes, and aminobenzoic acids. When plants were grown in soils containing 500, 750, and 1000 ppm of TNT, there was evidence of phytotoxic effects at 1000 ppm of TNT. The Lycopersicon peruvianum and the Datura quercofolia showed signs of stress which included yellowing and loss of leaves and flowers; however, the Datura innoxia looked quite healthy in soils with 1000 ppm of TNT (21) .

Genetic Engineering and Bioaugmentation

Genetic modifications of plants and microorganisms to enhance contaminant biodegradation or to improve growth characteristics may be cost effective in selected applications. Kingsley et al. (15) reported on the beneficial effects of bioaugmentation of soil by adding to the rhizosphere competent bacteria capable of degrading the herbicide 2,4-D. Inoculation with the bacteria allowed wheat seed germination and plant growth in soils which had an otherwise phytotoxic concentration of the compound. Similar results have been reported for radish seeds by Short et al. (31).

Vegetation Can Be Beneficial in Landfill Covers

Licht (19) has reported on the advantages of densely rooted trees for water management on landfill covers. An Ecolotree Cap design is being investigated on the Lakeside Reclamation Landfill, Beaverton, Oregon. In April, 1990, 7455 poplar trees (Populus spp.) were planted on a 0.6 acre prototype plot covering a recently finished cell of the landfill. The trees grew well with the average heights being 2.07 m in 1990, 3.86 m in 1991, and 6.17 m in 1992. During the second growing season, the trees were able to transpire water from the soil covers at rates greater than precipitation. Licht (19) points out that the tree covered cap is porous, and that the landfill reacts more like a bioreactor. More rapid stabilization of the buried material is expected.

Mathematical Modeling

Mathematical models to describe water movement and contaminant fate in the rhizosphere of growing plants have been reported by Davis et al. (11). Tracy et al. (33, 34) have presented simulation results for two different cases; the beneficial effects of vegetation in the management of landfill leachates containing low levels of an organic compound are presented in the earlier study (34). Rate limiting factors are investigated using sensitivity analysis in the most recent work. The model is applicable to both unsaturated and saturated soil. Balances are included for water in the soil, water in the roots, the contaminant, root exudates, microbial biomass, and oxygen. The kinetic model includes microbial growth on root exudates as well as the contaminant.

CONCLUDING REMARKS

Degradation of contaminants may occur in plants as well as in microorganisms. The rhizosphere is rich in microbial numbers and microbial diversity. Contaminants may be degraded more rapidly when plants are present because of root exudates supplied by the plants; contaminants may also be taken up into the plants and transformed. Recent results are very encouraging. Additional research is needed to more fully understand the beneficial interactions which occur.

ACKNOWLEDGMENT

This research was partially supported by the U.S. EPA under assistance agreements R-815709 and R-819653 to the Great Plains-Rocky Mountain Hazardous Substance Research Center for regions 7 and 8. It has not been submitted to the EPA for peer review and therefore may not necessarily reflect the views of the agency and no official endorsement should be inferred. The U.S. Department of Energy, Office of Restoration and Waste Management, Of fice of Technology Development and the Center for Hazardous Substance Research also provided partial support.

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TABLE 1. Dimensionless Concentration of Toluene in the Saturated Zone
at Five Axial Positions on Four Different Days.



Average flow rate	Dimensionless Concentration C*
(liters/day)		C* = concentration C/inlet concentration

Inflow 	Outflow 	Port 1	Port 2	Port 3	Port 4	Port 5#

1.0	0.4		0.89	0.97	0.99	0.81	1.06
1.0     0.4		0.80	0.76 	0.83 	0.91    0.87
1.5     0.8      	0.82 	0.87 	0.75 	0.69 	0.96
1.5     0.85     	0.83 	0.92 	0.90 	0.81 	0.97

*Inlet flow was water saturated with toluene. The input concentration
was about 515 mg/liter. From Muralidharan et al. (22).

# Port 5 was connected to the outflow container.

TABLE 2. Dimensionless Concentration of Phenol at Five Axial
Positions on Four Different Days.*

Average flow rate        Dimensionless Concentration C*
(liters/day)       	C* = concentration C/inlet concentration

Inflow 	Outflow 	Port 1 	Port 2 	Port 3 	Port 4 	Port 5#

1.0	0.1             0.89    0.91    0.66    0.98    0.02
0.6     0.0             0.77    0.76    0.24	---	---
0.6     0.0             0.85    0.79    0.25    ---	---
1.4     0.0             0.96    0.89    0.82    0.77    0.02+
1.2     0.3             0.99    0.89    0.84    0.77    0.03

* Inlet flow was water with 0.5 ml/L of 93 % phenol. From Muralidharan
et al. (22).
+ No measurable effluent flow.
# Port 5 was connected to the outflow container.
--- No sample was collected. All values for inflow = 0.6 liters/day
were from the same day.

TABLE 3. Fractions of Input Water and Toluene which do not Leave in
the Effluent.

| Average flow rate |                 C*          Fraction of         Fraction of
(liters/day)                                     toluene lost        water lost

Inflow 		Outflow 	Port 5

1.0             0.40                1.06            0.58                 0.6

1.0             0.40                0.87            0.65                 0.6

1.5             0.80                0.96            0.49                0.47

1.5             0.85                0.97            0.45                0.43

From Muralidharan et al. (22).


TABLE 4. Fractions of Input Water and Phenol which do not Leave in
the Effluent.

Average flow rate                 C*	Fraction of	Fraction of
(liters/day)                            phenol lost	water lost

Inflow 		Outflow 	Port 5

1.0             0.1              0.02	0.99		0.90
0.6             0.0              ---    1.00		1.00
0.6             0.0              ---    1.00		1.00
1.4             0.0              0.02   1.00		1.00
1.2             0.3              0.03   0.99		0.75

From Muralidharan et al. (22).

Table 5. Concentration of Anthracene (mg/kg) in Contaminated
Spiked Soil for 100 mg/kg of Added Anthracene.*

Vegetation                          Time

                        4 weeks             24 weeks
No Plants               1.704 (0.205)        1.145 (0.100)
Alfalfa                 0.883 (0.190)        0.587 (0.322)
Fescue                  1.371 (0.453)        0.753 (0.152)
Switch Grass            1.040 (0.281)        0.788 (0.237)
Sudan Grass             1.649 (0.155)        0.737 (0.145)

* Values in parentheses are standard deviations from four replicates.
The measured concentration of anthracene in the contaminated soil
before spiking was 0.6 mg/kg. From Reilley (29).


Table 6.

Concentration of Pyrene (mg/kg) in Contaminated Spiked Soil for 100
mg/kg of Added Pyrene.*

Vegetation                          Time

                  4 weeks               24 weeks
No Plants      12.646 (0.237)        2.363 (0.245)
Alfalfa         9.887 (0.164)        1.655 (0.187)
Fescue         10.152 (0.436)        1.490 (0.597)
Switch Grass   10.828 (0.464)        1.325 (0.318)
Sudan Grass    10.685 (0.261)        1.484 (0.564)


* Values in parentheses are standard deviations from four replicates.
The measures concentration of pyrene in the contaminated soil before
spiking was 1.4 mg/kg.  From Reilley (29).


Table 7.

Comparison of Cumulative Amount of l4CO2 Evolved from Transformation of
Pyrene for Organic Acid Enriched Rhizosphere Soil (RA), Rhizosphere
Soil (RW), NonRhizosphere Soil (NW), and Autoclaved Soil (C)*.


Time (days)	RA (dpm) 	RW (dpm) 	NW (dpm)	C (dpm)
       5         5,803           5,143           5,081             336
      10         9,908           8,197           7,976           1,051
      30        14,194          10,844          10,932           2,403
      50        16,875          12,209          12,673           3,271

From Reilley (29).