bioremediation in the rhizosphere

8/11/2019 Bioremediation in the Rhizosphere

1/7

b a RITICAL RE VIEW 1

c

xamination of the pub-

lished scientific literature

reveals persuasive evi-

dence that plant roots, in

conjunction with their as-

sociated microbial commu-

ities, offer a potentially

important treatment strategy for in

situ biological remediation of chem-

ically contaminated soils. Under a

variety of environmen tal condi-

tions, vegetation has been shown to

enhance microbial degradation

rates of organic chemical residues

in soils. These findings are impor-

tant because vegetation may pro-

vide a low-cost alternative or sup-

plement to expensive, capital-

intensive technologies for soil

cleanup. Moreover, unlike technol-

ogies that merely relocate contami-

nants, vegetation promises a means

of halting legal liability for hazard-

ous

waste residues in soils because

hazardous compounds in the rhizo-

sphere [root zone) are totally de-

stroyed (mineralized).

Historically, the use of plant sys-

tems as a waste treatment technol-

ogy bas focused primarily on waste-

water ( 1 ) . This work dealt mostly

with the manipulation of opera-

tional parameters [e+, lagoon size

or

flow rate) to optimize biological

removal of unwanted chemicals.

Whether microorganisms in the root

zone of aquatic plants contribute to

improved water quality through

detoxication of hazardous organic

substances is unknown and rela-

tively unexamined.

This review will critically exam-

ine reports on the interaction of mi-

croorganisms with hazardous

or-

ganic chemicals in the terrestrial

rhizosphere. Studies

on

microbial

degradation of agricultural chemi-

cals in the rhizosphere, and recent

research on the fate of nonagricul-

tural chemicals in rhizosphere soils

are presented. Collectively these

studies provide a strong scientific

basis to support field demonstra-

tions of in situ degradation of toxi-

cants in the rhizosphere. Moreover,

investigations of the fundamental

2630

Emiron. Si.Technol.,

Vol.

27.No. 13,191

mechanisms wh

microbial degra

would provide insi

tions of the plant

for in situ remediation

The rhizosphere

The rhizosphere, first described

by Lorenz Hiltner in 1904, has been

the focus of agricultural research for

manv vears because of its imvor-

tain xenobiotic compounds in the

rhizosphere. Consequently, an in-

triguing question is whether selec-

tion for plants with supernodulat-

ing roots, proliferation of root hairs,

or other genetically determined

properties of plant roots would pos-

itively affect microbial degradation

rates of specific toxicants in the

rhizosphere.

The actual comnosition of the mi-

tanck

i o

crop productivity. ?he

rhizosphere is a zone of increased

microbial activity and biomass at

the root-soil interface that is under

the influence of the plant root 2 ) .

This zone is distinguished from

bulk soil by this root influence. Ex-

cellent comprehensive reviews on

the rhizosphere are available 2, );

therefore, only a brief description of

important rhizosphere characteris-

tics is presented below.

The overall effect of the plant-

microbe interaction is an increase

in microbial biomass by an order of

magnitude or more compared with

that of microbial populations in

bulk soils. This rhizosphere ef-

fect is often expressed quantita-

tively as the ratio of the number of

microorganisms in rhizosphere soil

to the number of microorganisms in

nonrhizosphere soil, the

WS

ratio

4).

Although WS ratios commonly

range from 5 to

20,

they can

run

as

high as

100 or

greater

5).

This in-

crease in microbial growth and ac-

tivity in the rhizosphere may be re-

s p o n s i b l e f or t h e i n c r e a s e d

metabolic degradation rate of cer-

crobial community in the rhizo-

sphere is dependent

on

root type,

plant species, plant age, and soil

type

(3,5,61,

as well as other factors

such as exposure history of the

plant roots to xenobiotics (7-10).

Generally, the rhizosphere is colo-

nized by a predominantly gram-

negative microbial community

5) .

Carbon dioxide concentrations in

the rhizosphere are generally higher

than in nonvegetated soil, and

rhizosphere soil pH may differ by

1-2 units from that of comparable

nonvegetated soil. Oxygen concen-

trations, osmotic and redox poten-

tials, and moisture content are other

parameters influenced by the pres-

ence of vegetation (2).These param-

eters are further dependent

on

the

properties of specific plant species.

The continual change at the root-

soil interface, both physical and

chemical, produces constant alter-

ations in the soil structure and mi-

crobial environment.

The interaction between plants

and microbial communities in the

rhizosphere is complex and has

evolved to the mutual benefit of

both organisms. Plants sustain large

microbial populations in the rhizo-

sphere by secreting substances such

as carbohydrates and amino acids

through root cells and by sloughing

root epidermal cells. The magni-

tude

of

rhizodeposition by plants

can be quite large 1 1 ) . Root cap

cells, which protect the root from

abrasion, may be lost to the soil at a

rate of

10,000

cells per plant per day

3). In addition, root cells secrete

mucigel, a gelatinous substance that

is a lubricant for root penetration

through the soil during growth.

0013-936X/93/0927-2630 04.00/0 1993 American Chemi cal Society

T O D D

N

D

E R

S

O N

Iowa

Stote University

Ames,

IA 50011-3140

1 2

B E T H G

U

T

H

R I

E

University

ofNorth

Carolina

Chapel

Hill,

NC27599-7400

B R

B

R

T

,

W

L T

0

oakRidge

National

aboratory

OakRidge,

TN

37831-6038


2/7


3/7

This mucigel, along with other cell

secretions, constitutes root exudate

(12).

Soluble exudate includes ali-

phatic, aromatic, and amino acids

and sugars. Root cap cells and exu-

dates provide important sources of

nutrients for microorganisms in the

rhizosphere. Although modification

of the soil in the rhimsphere by plant

root exudates is an important process

that influences microbial nonula-

tions,

it

is the actual struct$e' of

the plant root that provides micro-

organisms with surface area for

colonization 2. 5, 6). The fibrous

roots of grasses provide a larger

surface area for colonization than

do taproot systems 5).

Once established in the rhizo-

sphere of plants, microbial popula-

tions may be passively nourished

by root exudation and decaying

plant matter;

or the

presence of the

microorganisms may actually in-

duce liberation of certain organic

nutrients by co-evolved biochemi-

cal signals.

Pseudomonas

putida

and Azospirillum spp. are exam-

ples of bacteria capable of inducing

nutrient release

from

the roots

13).

In the absence of bacteria and

fungi, plant exudate production

decreases (21, subsequently pro-

Sandmann and Loos 7)ound

an

increase in the number of 2.4-D

(2,4-dichlorophenoxyacetate)-de-

grading bacteria i n rhizosphere

soils of previously untreated sugar

cane but not African clover. This re-

search illustrates

a

potentially inter-

esting theme common to the litera-

ture

on

microbial degradation of

herbicides in the rhizosphere-the

nossibilitv that rhizosuhere micro-

viding fewer organic substrates to

sustain microbial

growth.

The

in-

teraction of leguminous plants

with nitrogen-fixing bacteria re-

sults in increased microbial bio-

mass, plant growth, and root

exu-

dation, perhaps because of the

increased availability of soil nitro-

gen in the presence of nitrogen-fix-

ing

bacteria. This in turn may lead

to enhanced microbial degradation

of organic compounds such asher-

bicides in the rhizosphere by these

bacteria (141.

L

lsis

1

.

dem@ trati

on

s

/

of in

situ c

Research on microbial transfor-

mations of organic compounds in

the

rhizosphere focuses mainly on

agricultural chemicals such as in-

secticides and herbicides. A num-

ber of researchers have described an

increase in pesticide degradation in

the rhizospheres of a variety of

plant species (Table 1).Occasion-

ally, this increased degrading ca-

pacity correlates with increased

numbers of pesticide-degrading mi-

croorganisms. The wide range of

chemical structures and plant types

reported in these studies suggests

the involvement of multiple species

of microorganisms ( 15 ) within a

community, that is, microbial con-

sortia, rather than a single member

of

that community.

bial communities are involved in

protecting the plant from chemical

injury. The phenoxy acid herbi-

cides, such as 2,4-D, control broad-

leaf weeds. Sandmann and

Loos

7)

suggested that the increase in 2,4-D-

degrading microorganisms in the

rhizosphere of sugar cane (a grass)

was a possible mechanism by

which the plant was protected from

the herbicidal effects of 2,4-D and

that phenolic analogues in the exu-

date contributed to selection of a

microbial community responsible

for degrading 2,4-D. Conversely,

2,4-D-degrading microbial popula-

tions in African clover, a plant sen-

sitive to 2,4-D, were not increased.

Earlier work by Abdel-Nasser and

co-workers 8) and Gavrilova et al.

10) howed elevated microbial

counts in

the rhizospheres

of

pesti-

cide-treated plants. Corn, beans, and

cotton plants treated with temik

[Z-methyl-2 methy1thio)propional-

dehyde O(methylcarbamoyl]oximel

8)bad higher microbial counts in

some instances than those in un-

treated rhizospheres. Although the

authors did not monitor degradation

of temik, they hypothesized that the

increased microbial numbers sup-

ported the idea that temik and

other pesticides were metabolized

by several types of rhizospheric

microbiota.

Gavrilova and co-workers

(10)

found >lOO-fold higher microbial

counts in the rhizosphere of

wheat, corn, and peas treated

with diazinon [O,O-diethyl O(2-

isopropyl-4-methyl-6-pyrimid-

inyl) phosphorothioate] than in

treated soils without vegetation.

Although

no

clear correlation

could be established between mi-

crobial counts and the rate of di-

azinon degradation, the authors

did isolate bacteria, fungi, and

actinomycetes from wheat rhizo-

sphere capable of degrading diaz-

inon in pure cultures. Recently,

Sat0 16) ound an eight-fold in-

crease in heterotrophic and nitri-

fying bacteria in rice rhizosphere

after the addition of benthiocarb

[S-p-chlorobenzyl diethylthiocar-

bamate). These findings implicate

the increase

in

microbial biomass

as a cause of the decreased persis-

tence of certain toxicants in the

rhizosphere and also suggest that

rhizosphere microorganisms can

protect the plants from chemical

injury

(17, 28).

Seibert and co-workers 19) b-

served an increase in atrazine ( 2 -

chloro-4-ethylamino-6-isopropyl-

amino-s-triazine) degradation at

5

ppm (mg/kg soil) by microorgan-

isms in the rhizosphere of corn fol-

lowing the harvesting of corn shoots.

This enhanced degradation was cor-

related with

an

increase in microbial

biomass in the presence of decom-

posing corn roots. The authors also

attributed the increased degradation

to higher dehydrogenase activity ob-

served in the rhizosphere soil

throughout the experimental period.

In the rhizosphere soil, the concen-

tration of unchanged atrazine was

found to be lower th natrazine con-

centrations

in

nonrhizosphere soils.

Concentrations of hydroxyatrazine

and two other hydroxylated metabo-

lites were three times

higher

in the

rhizosphere than were concentra-

tions

in nearby soils.

2632

Envimn.

Sci

Techno l.. Vol. 27,

No. 13, 1993


4/7

Gramineae Mecoprop Mixed microbial culture was capable of using compound

2,4-Db source. None of the pure cultures was capable of using the compounds.

MCPA' Wheat is tolerant to this class

01

herbicides (phenoxy acids).

2,4-Db High population of 2,4-D-degrading microorganisms in the rhizosphere 7

of sugarcane, a plant tolerant to 2 ,4-D, compared with African clover, a

plant sensitive to the herbicidal eflects of 2,4-D

Stimulated ammonium oxidalion (nitri fication) n rhizosphere soil

Increased mineralization n the rhizosphere, especially under flooded

conditions

Eightfold increase in heterotrophic bacteria in the rhizosphere of treated 16

rice plants

Baci//ussp. isolated from rice rhizosphere could grow on oil residues but 31

only in the presence of root exudates.

Rhizosphere microbial counts increased by 2 orders of magnitude

Vegetated microbial filters increased the removal of both aromatic and

aliphatic compounds.

Increased disappearance of PAHs in vegetated vs. nonvegetated soil

columns

Increase In production

of

atrazine degradation metabolites by

rhizosphere microorganisms in the presence of decomposing roots

Higher counts of microorganisms in treated vs. untreated rhizospheres

Rhizosphere trealments sgnificanlly ncreased mtia l raies of

mnera zaio noya faclo rot 1.1-1.9

Increase0 minemzatlon ot botn compodnds n Ihe rhzosphere

Descmes me rnponance 1 egunn ous p anis

tn

rec a m ng

petroleLrn contammatea sites

Mh

caJseo ennanceo nitrif callon ana m nera zation of organic

SLQstanCes n tne (h zosphere

Ammon lying.

n

tr lying and ce . J ose-oecomposing bacler a

n

tne

m

zospnere ncreaseo by 1 to

2

orders of magnitLoe

Linaceae

deza Faoaceae .ncreased oegradalon 1 TCE

n

fhizosp

ly

p ne P naceae contai

grass Gramineae

nrod Compos.tae

Soybean Faoaceae

Canads Typhaceae Sddanants Mineralizat.on

1

sdtactants was more rapid

in

the rhizosphere th

root. free sediments

2-(2-Methyl-4-chlomphenoxy)propianic acid. 42.4-Dichlorophen~xyacet i~cid. E2-Melhy l -4-~hloraphen~xyacet iccid. d2,3-Oihydro-2,2-dimelhyl-

-benzofuranyl methylcarbamate. * O,Odiethyl-O-~nilrohenyl phosphorothioate. 'S-pchiorobenzyl diethylthiocarbamate. 9 O,Odielhyl-O(Z-

isopropyl-6-melhyl-4-pyrimidinyl)

phosphorothioate. Volatik organic compounds (benzene. bi henyl. chiombenzene, dimethylphthalale. ethylbenzene,

naphthalene, pnilmloluene, oluene pxylene, bromoform, chloroform, 1.2-dohloroelhane. elrachtroethyiene.1.1.1 -tnchiomethans. ',Polycyciic aromatic

h drccarbons (benz[a]amhracene, chrysene. benzolalp rene, and dibenzla,hlanthracene.

'2-Chloro-4-ethylamino-6-iso

ropylamino-s-lnzins. 2-

hXethyl-2(methyilhio)propionaldehyde

~(methylca*amoyi~oxime. dodecyl linear alkyibenzenssulfonate. dadecyl linear aIcol?oI ethoxylats, dodecykrime-

lhylammonium chloride.

rn

Maleic hydrzide

( 1 , 2 - d i h y d r o - 3 , 6 - ~ r i d a i ~ , o ~ ) .

1,1.2-trichloroethyiene.

Source:

Reference 15.

Similar results were recently re-

ported (20) for atrazine studied at

high concentrations characteristic

of waste sites. Rhizosphere soils

from grasses collected near the

boundaries of a pesticide-contami-

nated site mineralized

60

of atra-

zine added at 100 ppm 0.46

mM

after eight days, although a

lag

pe-

riod of three days was observed.

However, nonrhizosphere soil col-

lected within the site mineralized

280

of the atrazine within two to

three days, in some cases without a

lag period. Nonetheless,

60 miner-

alization of atrazine at

100

ppm in

rhizosphere soils of grasses collected

near the site boundary

has

mportant

implications for sites contaminated

with pesticide wastes.

served a rhizosphere effect on deg-

radation similar to that observed by

Seibert

(19)

using atrazine. Only

5.5%

of the C-parathion evolved

as 14C0, from unplanted soils,

whereas 9.2% evolved from rhizo-

spheres under nonflooded condi-

tions. Converselv, 22.6% of the ra-

Reddy and Sethunathan (21)con-

ducted fate studies of 14C-parathion

0,

diethyl-0-p-nitrophenylphos-

phorothioate) using rice and ob-

diocarbon evolved as %O, under

flooded conditions, which favor

rice growth. Reddy and Sethu-

nathan

21)

rgued that the proxim-

Environ SCLTechno1,VoI.

27,

No. 13. 1993 2693


5/7

ity of the aerobic-anaerobic inter-

degrade and grow on mecoprop as mbial degradation of agriculturally

face in the rice rhizosphere under

the sole carbon and energy

source.

related organic compounds in the

flooded conditions favored the ring This microbial community also de- rhizosphere of a variety of plant spe-

cleavage of parathion. Increased mi- graded

2,4-D

and MCPA (2-methyl+ cies. Recent studies also indicate that

crobial deeradation rates in the ChloroDhenoxvaceticacidhMoreover.

the

dkDDt?aranCe of nonaericultural

rhizospherlmay also have been the

result

of

greater

0,

concentration

provided by the rice

roots 22,23).

Thus, root exudates provide mi-

croorganisms with a wide range of

organic substrates for use as carbon

and energy sources. Because both

parathion and the structurally

re-

lated pesticide, diazinon, appear to

be degraded initially by cometa-

bolic attack 24,251, su and Bartha

(26)

hypothesized that the rhizo-

sphere would be especially favor-

able for cometabolic transforma-

tions of pesticides. Cometabolism

is a process whereby microorgan-

isms biochemically transform a

substance while growing

on

an-

other substrate (5). The microor-

ganism neither derives energy

from the cometabolized substance

nor is incorporated into microbial

biomass; however, the chemical

structure of the cometabolized

compound is changed.

Using radiolabeled diazinon

and parathion, Hsu and Bartha

were able to show accelerated

mineralization of these two insec-

ticides in the rhizosphere of the

bush bean, Phaseolus vulgocis.

Beans were chosen because of

their recognized inability to me-

tabolize diazinon

(25).

Approxi-

mately 18 of the parathion and

13% of the diazinon were miner-

alized in the bean rhizospheres

compared with

7.8

and

5.0

in

the root-free soil for parathion

and diazinon, respectively.

Gun-

ner

and co-workers

25)

revi-

I

I

Anderson et

h. 15)

oncluded that

mimbia l consortia, rather th n indi-

vidual microbial species,

are

likely to

be involved in

the

degradation of

nu-

memus toxicants in the rhizosphere.

Overall, these studies indicate the

complexity of plant-microbe-

toxicant interactions and the com-

plications that may hamper elucida-

tion of the mechanisms by which

toxicants are degraded in the rhizo-

n

i

esehch

ith

usly found similar results w

diazinon, although they did not

provides

substantial

evidence for the

~

P d

u

Moremediation

f surface soils. i

b

i

observe an increase in microbial bi-

omass in the rhizosphere after ap-

plication of diazinon. Rather, a mi-

crobial isolate capable

of

diazinon

metabolism proliferated.

The rhizosphere may also provide

a habitat in which microbial consor-

tia capable of growth

on

organic con-

taminants may flourish. Lappin et al.

27)ound that a microbial commu-

nity isolated from wheat roots could

grow

on

the herbicide mecoprop

[2-(2-methyl-4-chlorophenoxy)

ro-

pionic acid]

as

the sole carbon and

energy source

The authors isolated

five species of microorganisms, none

of which could individually m w

n

sphere. The following critical

areas

need to be investigated

further:

the influence of the size and

structure

of

plant roots

on

toxicant

degradation,

the dynamic aspects of root turn-

over, including the possible release

of toxicants to the soil during decay

processes,

the potential for roots to release

surfactant compounds that may sol-

ubilize xenobiotics, and

the role of rhizosphere microbial

communities in humification pro-

cesses that may reduce bioavailabil-

ity of toxicants through stabiliza-

tion with soil omanic matter.

mecoprop, not even when 6ultures

included a readilv available carbon

-

Of hazardous

waste

source for cometibolism. However,

two or more species together could

The studies reviewed above pro-

vide evidence for the accelerated mi-

chemic& is accelerated

l

the root

zone. Collectively, these studies

show results comparable to the work

with

pesticides: specifically, the deg-

radation of a variety of nonagricul-

tur l chemicals and the capability of

rhizosphere microorganisms to de-

grade them. The following target toxi-

cants were examined in this research:

polycyclic aromatic hydmcarbons in

prairie g s rhizospheres 281, the en-

hanced degradation of 1,1,2-kichlo-

roethylene (TCE)

in soils

collected

from the rhizosphere (291,and in-

creased TCE mineralization in

whole plant-soil systems

(30).Also

documented in these studies are in-

creased degradation of

oil

residues

by microorganisms isolated from

oil-polluted rice rhizospheres 311,

increased mineralization of surfac-

tants

by microorganismsassociated

with cattail roots

(32),

urfactant

mineralization in intact rhizo-

spheres

331,

and removal of a vari-

ety of EPA priority pollutants in

nonvegetated filters and filters

planted with the common reed,

Ph gm it es communis (34).Several

of these studies are discussed be-

low.

Rasolomanana and Balandreau

31)

observed enhanced microbial

degradation of oil by rhizosphere

microorganisms. These observa-

tions were serendipitously dis-

covered during the study of the

improved growth of rice in soil to

which oil residues had been ap-

plied. Rasolomanana and Balan-

dreau, hypothesizing that the in-

creased growth was brought about

by the initial removal of the oil

residues from the rhizosphere by

specific microorganisms, isolated a

Bacillus

sp. that could grow on the

oil residues only in the presence of

rice root exudates.

April1 and Sims

28)

valuated

the persistence of four PAHs-

benz[alanthracene, chrysene, ben-

zo[alpyrene, and dibenz[a,h]an-

thracene-in the root zone of a

mixture of eight prairie grasses in

soil column studies. Residue analy-

sis of the columns revealed that

PAH disappearance was consis-

tently greater in the vegetated than

in the unvegetated controls. Al-

though sterile soil controls were not

included in the experiments, the

authors speculated that microbial

degradation of

the

PAHs accounted

for the increased disappearance of

2634

Environ. Sci.

Technol..

Vol. 27, No. 13, 1993


6/7

PAHs from the vegetated soil col-

umns. However, the rhizosphere ef-

fect may have been obfuscated by

the addition of manure to all soil

columns during PAH addition. In

other words, the difference in dis-

appearance rates of the PAHs be-

tween the vegetated and the

non-

vegetated columns may have been

much greater had the manure not

been added to both columns.

In addition, April1 and Sims spec-

ulated that humification of the PAHs

may have accounted for increased

disappearance in the vegetated col-

umns. Furthermore,

the

possibility

for root uptake and metabolism of the

PAHs was not considered in these

experiments, although the metabolic

capabilities of vegetation are well

documented 35, 36, 37) and plant

uptake and metabolism of organic

compounds may contribute to en-

hanced degradation of these materi-

als at waste sites

(38).

Nonetheless,

this study does provide evidence for

the accelerated disappearance of haz-

ardous organic compounds in the

rhizosphere even though the cause of

the disappearance was not estab-

lished experimentally.

Walton and Anderson observed

accelerated degradation of TCE in

slurries of rhizos here soils and

mineralization of C-TCE in rhizo-

sphere soil samples collected from

four plant species at a former sol-

vent disposal site

(29).

These stud-

ies were conducted to provide a

foundation for more rigorous

whole-plant studies in which in-

creased mineralization of C-TCE

was also demonstrated 30).The

plants tested represented a variety

of root types: fibrous, tap, legumi-

nous, and mycorrhizal. Two le-

gumes, Lespedezo

cuneoto

and Gly-

cine mox (soybean), enhanced soil

microbial mineralization of 14C-

TCE, although only L. cuneoto is in-

digenous to the contaminated site.

In addition, enhanced mineraliza-

tion was observed in soil containing

loblolly pine

(Pinus

toedo

seed-

lings, which have root-ectomycor-

rhizal associations. This raises the

question of whether mycorrhizae

contribute to the degradation of

TCE and other hazardous organic

compounds in the rhizosphere.

Recently Donnelly and Fletcher

(39)described the ability of ectomy-

corrhizal fungi to degrade certain

congeners of polychlorinated bi-

phenyls (PCBs) in vitro. In addition,

Katayama and Matsumura 40) have

recently shown that a rhizosphere-

competent fungus, Trichoderma

horzionum

was able to degrade a

variety of organochlorine com-

pounds, including pentachlorophe-

nol,

endosulfan, and DDT.

Because elevated %O, produc-

tion was observed in the soils con-

taining soybean germinated from

commercially available seeds, pro-

longed exposure of the plant or soil

microorganisms to the toxicant of

interest may not be a requirement

for enhanced degradation. How-

ever, prolonged exposure of soil mi-

croorganisms to the toxicant may

speed degradation through the se-

lective enrichment of those species

in

the microbial community that

can survive and degrade the xenobi-

otic substrate. The relative impor-

tance of several variables in biode-

grading TCE and other organic

compounds in the rhizosphere is

not well understood. These vari-

ables include the morphology or

surface area of the root system (e.g.,

tap vs. fibrous], the selective influ-

ence of the root exudates, and the

nature of microbe and root associa-

tions present (e.g., nitrogen-fixing

and mycorrhizal).

Other beneficial effects

An important consideration for

the use of vegetation in remediating

contaminated surface soils is the

potential transport of the parent

compound

or

hazardous metabo-

l i te(~)rom soil into plant tissue.

Root uptake of organic compounds

from soil solution depends largely

on physicochemical properties of

the compounds, environmental

conditions, and plant characteris-

tics 411. Because movement of

chemicals into plants presents an-

other potential route of exposure for

humans and wildlife at contami-

nated sites, plant residue analysis is

critical in addressing plant uptake

of hazardous organic contaminants.

A number of recent reviews 42-46)

summarize the uptake and accumu-

lation of organic chemicals from

soil by vegetation. Overall, plant

uptake is usually favored for small

and low molecular weight polar

compounds, whereas large and high

molecular weight lipophilic com-

pounds tend to be excluded from

the root. Some researchers have

proposed the use of vegetation in

terrestrial environments to accumu-

late inorganic contaminants such as

nitrates 471and metals ( 4 8 )as well

as for removal of organic com-

pounds from soils 38).

Conclusions

The research discussed in this re-

view provides substantial evidence

r .

I

Todd

A.

Anderson is

o

member of the

gmduote faculty and

o

research ossoci-

ate in the Pesticide Toxicology Lobom-

tory

ot I owa

State University.

H e

re-

ceived a B.S. degree in biological

science from Peru Stote College NE

and

M.S.

degree and Ph.D. in environ-

mental toxicology rom the Universityof

Tennessee. His reseorch interests in-

clude the environmental fate and effects

of Industrial chemicals and pesticides

ond bioremediation

of

contominoted

sites.

. --*

- - I

ElizabethA. Guihrie is

o

graduatestu-

dent in the Deportment

of

Environmen-

tal Sciences and Engineeringot the Uni-

versity of North Carolina. She received

her B.S. degree in biology from Emory

University ond served as

a

Peoce Corps

volunteer in Gabon Centml Africa. Her

research interestsore the movement and

effectsof chemical Contaminants in ter-

restrial ecosystems and biologicol reme-

diotion

of

contominoted sites.

Barbam

T.

Walton is

o

senior scientist

in the Environmental Sciences Division

of Oak Ridge Notional Laboratory She

is on adjunct professor in the Deport-

ment of Environmental Sciences ond

Engineering at the Universityof North

Carolina and holds adjunct faculty op-

pointments in ecology ond environmen-

to1 toxicology

t

the Universityof Ten-

nessee. She is o former president of he

Society of Environmental Toxicology

and Chemistry and a post officerof the

Americon Board

of

Toxicology.

Environ. Sci. Technol..

Vol. 27,

No.

13, 1993

26


7/7

for the potential role of vegetation

in facilitating microbial degradation

for in situ bioremediation of surface

soils contaminated with hazardous

organic compounds. Support for

this concept comes from the funda-

mental microbial ecology of the

rhizosphere, documented accelera-

tion of microbial degradation of ag-

ricultural chemicals in the root

zone, and recent research address-

ing degradation of nonagricultural

hazardous organic compounds in

the rhizosphere. Further under-

standing of the critical factors influ-

encing the plant-microbe-toxicant

interaction in soils will permit more

rapid realization of this new ap-

proach to in situ bioremediation.

Especially promising areas for

fur-

ther research are the following: the

species-specific properties of the

plant, such as root morphology and

plant physiology; ecological and

physiological characteristics

of

the

microbial communities associated

with plant roots; and the role of root

exudates in selection of those com-

munities. Microbially mediated hu-

mification processes in the rhizo-

sphere may have an important

influence on the persistence and bio-

availability of toxicants in surface

soils. Also important may be the role

of nonbacterial plant associations in

the rhizosphere, such as the presence

of mycorrhizae

or

the influence of

abiotic factors such as nutrient addi-

tions, aeration, and multiple chemi-

cal stresses. A better understanding

of the mechanistic interactions be-

tween plant roots and their

sur-

rounding microbial communities

will favor successful field demon-

strations and permit effective selec-

tion and management of vegetation

to achieve in situ bioremediation.

Acknowledgments

T h e a u t h o r s t h a n k A . M . H o y lm a n a n d

C . W . G ehr s , O akR i dge N a t i ona l L abor a-

t o r y , O ak R i dge , T N ;

T.

C. Hazen of the

S a v a n n a h R i v e r S i t e , A i k e n , S C; a n d

F .

K . P f a e n d e r , U n i v e r s i t y o f N o r t h

Carol ina , Chape l Hi l l , for helpful cont r i -

bu t i on s t o t h i s w or k . T he O f f ice o f T ech-

no l ogy D eve lo men t an d t he O f f ice o f

E n v i r o n m e n t a f R e s t o r at i o n

and

W ast e

M a n a g e m e n t , U . S . D e p a r t m e n t

of

E n-

e r g y, s u p p o r t e d t h i s w o r k . O a k R i d g e

Nat ional Laboratory

is

managed by Mar -

t i n Mar i e t ta E ne r gy S ys t ems , I nc . , under

con t r ac t D E - A C 05- 840R 21400 w i t h t he

U . S . D e p a r t m e n t o f E n e r g y . E n v i r o n -

mental S c i e n c e s D i v i s i o n P u b l i c a t i o n

N o. 4142.

References

(1)

(2)

Walton, B.

T.;

Anderson, T. A. Curr.

Opin . Bio technol .

1992,3, 67-70.

Curl , E. A ,; Truelove, B.

Th e Rh i z o -

sphere; Springer-Verlag: Berl in and

Heidelberg,

1986.

Campbell, R. Plant Microbiology; Ed-

ward Arnold: B alt imore, MD, 1985.

Katznelson,

H.

Soil

Sci. 1946, 62,

343-54.

Atlas , R . M. ; Bsr tha , R. Microbial

Ecology: Fundamentals and Applica-

t i o n s ; B enj ami nIC ummi ngs : Menl o

Park, CA, 1992.

Bolton, H.; Fredrickson,

J.

K.; Elliot,

L. F. In Soil Microbial Ecology; Met-

t ing, F. B., Ed.; Marcel Dekker: New

York, 1993; p . 27-64.

Sandmann, E.R.I.C.; Loos, M. A.

Chemosphere 1984, 23, 1073-84.

Abdel-Nasser,

M.;

Makaw i, A. A.; Ab-

del-Moneim, A. A. Egypt . J.Microbiol.

Abuyev a, A. A, ; Bagayev, V. B.

Iz-

vestiya Timiiryazevsk. Skh . Ak ad .

1979, 4, 37-44.

1975,2, 27-30.

(10)Gavrilova, E.A,; Kruglov, Y. V.; Ga-

rankina, N. G. T r . V s e s . N a u c h n o -

Issled. Instit. Skh. Mikrobiologii.

(11)Paul E.A.; Clark , F. E.

Soil

Microbiol-

o g y a n d B i o c h e m i s t r y ;

A c a d e m i c

Press: New York, 1989.

(12)

Rovira, A. D.; Foster, R. C.; Martin,

J . K. In

Th e S o i l - Ro o t I n t e r f a c e ;

Harley, J . L.; Russell, R.

S.,

Eds.; Aca-

demic Press : New York, 1979; p p .

(13) rikryl,

Z.;

Vancura, V. Plant Soil

(14)Liu, C.-M. et al. App l. Environ. Micro-

biol.

1991, 7, 1799-1804.

(15)Anderson, T. A.; White,

D.

C.; Wal-

ton, B. T. In Biotransformations:

Mi-

crobial Degradation of Health-Risk

Co mp o u n d s ;

Singh, V., Ed.; in press.

(16) ato, K. In

Interrelat ionships between

Microorganisms and Plants in

Soil;

Vancura, V.; Kun c, F ., Eds.; Elsevier:

New York, 1989; p. 335-42.

(17)Herring, R.; Bering, C. L. Bull . Envi-

ron.

Contam. Toxicol . 1988, 40,

(18)Krueger, J. P.; Butz, R. G.; Cork, D. J. J.

Agric. Food Chem. 1991,39,1000-03.

(19)Seibert, K.; Fuehr,

F.;

Cheng, H. H. In

Th e o r y a n d Pr a ct ic a l Us e

of

Soi l -

Appl ied Herbic ides Sympos ium;

Eu-

ropean Weed Resource Society: Paris,

1981; p . 137-46.

20 ) Mandelbaum, R. T.; Wackett , L. P.;

Allan, D. L. App l . Environ.

Microbiol.

(21)Reddy, B. R.; Sethu natha n, N. Ap p l .

Environ. Microbiol. 1983, 5, 26-29.

(22)

an Raalte, M. H.

Hortus Botanicus,

Bogorien sia, Javu Syoku bu u-1h

o

(23)Luxmo ore, R. J.; Stolzy, L. H.;etey,

J.

Agron. J 1970, 2,322-29.

(24) Daughton , G. G.; Hsieh, D.P.H. Ap p l .

Environ. Microbiol. 1977, 4, 175-84.

(25)

Gunner, H. B. et al. Plant

Soil 1966,

(26)Hsu,

T.

S.;

Bartha, R. Ap pl . Envi ron.

Microbiol. 1979, 7, 36-41.

(27)Lapp in, H. M.; Greaves, M. P.; Slater,

J.

H. App l . Environ. Microbiol. 1985,

49,429-33.

28)Aprill, W.; Sims,

R.

C. Chemosphere

1990,20,253-65.

(29)Walton, B. T.; Anderson, T. A. Ap p l .

Environ.

Microbiol.

1990,

56,

012-16.

(30)Anderson, T. A,; Walton, B. T. Com-

1983,52,67-70.

1-4.

1980,57,69-83.

62 -3

2 .

1993,59,1695-1701.

1943, (2603), 5-34.

25, 49-64.

parative Plant Uptake and Microbial

Degradation of Trichloroethylene in

the Rhizospheres

of

Five Plant Spe-

cies: Implications for Bioremediation

of Contaminated Surface Soils; Oak

R i d g e N a t i o n a l L a b o r a t o r y : O a k

Ridge, TN,

1992; RNLITM-12017.

(31)

Rasolomanana,

J.

L.; Balandreau,

J.

Rev. Ecol. Biol.

Sol.

1987, 24, 43-57.

(32) ederle, T. W.; Schwab, B.

S.

Ap p l .

Environ. Microbiol.

1989,

55,

(33)Knaebel, D. B.; Vestal,

J .

R. Can. J. Mi-

crobiol. 1992, 8, 643-53.

(34)W o l v e r t o n , B. C . ; McD ona l d - Mc-

Caleb, R.

C.

J. Miss . Acad . Sc i . 1986,

(35)Harms, H. H. Pestic. Sci. 1992, 35,

(36)KomoDa, D.; ennity, I.; S ander mann ,

H.,

Jr.

Pest ic. Biochem. Physiol .

1992,

(37)

KomoDa, D.; andermann H.,

Jr .

Pes-

t ic. Biochem. Physiol .

1992, 43,

(38)Bell, R. M. Higher Plant Accumula-

t i o n

of

O r g a n i c P o l l u t a n t s f r o m

Soils;

U.

S.

Environmental Protec-

t ion Agency: Cincinnat i , OH, 1992;

(39)Donnelly, P. K.; Fletcher, J. S. In Ab -

stracts of the 23th Ann ual M eeting of

the Society of Environmental Toxicol-

ogy

and Chemis t ry; Cincinnati , OH,

1992;

.

103.

(40)Katayama, A.; Matsumura, F. Envi-

Ton. Toxicol . Chem. 1993, 22,

(41)Walton, B. T.; dwards, N . T. In Land

Treatment: A Hazardous Waste Man-

a g e me n t A l t e r n a t i v e ; Loehr , R . C. ;

Malina, J .

F.,

Jr., Eds; Universi ty of

Texas: Austin, 1986; p . 73-86.

(42)

Devine, M. D.; Vand en Bo rn, W.

H.

In

Environmental Chemis t ry o f Herbi -

cides, Vol . II;

Grover, R.; Cessna, A. J.

Ed s. ; CRC Press : Boca Ra ton, FL,

1991, p . 119-40.

(43)Hance, R. J. In Environmental Chem-

istry

of Herbicides: Vol . I; Grover, R.,

Ed.; CRC Press : Boca Raton , FL,

1988,

pp. 1-19.

(44)Ryan, J. A. et al. Chemosphere 1988,

(45) aterson,

S.

t al. Chemosphere 1990,

(46)Walton, B.

T.;

oylman, A. M. Up-

take, Translocation, and Biochemical

Trans form ations of Polycyclic Aro-

matic Hydrocarbons by Vegetation;

Elect r ic Power Research Ins t i tute :

Palo Alto, CA,

1992;

PRI Report TR-

101651.

(47)Licht, L. A. Ph.D. Thesis, University

of Iowa, Iowa City, IA, 1990.

(48)Cunningham, S.D.; Berti, W. D. Ph y-

toremediation of Contaminated Sites:

Progress and Promise; Abstracts of

the 205th Meet ing o f the Amer ican

Chemical Society;

Denver, CO, 1993.

(49)Ramakrishna, C.; Sethunath an, N.

Appl. Environ. Microbiol . 1982, 44,

(50)Ampova, G. Bulgarski Tyutyun 1971,

(51)Gud in, C.

In

Proceedings of the Inter-

nat ional Sympos ium

on

Ground Wa-

ter Pol lu tion b y Oi l Hydrocarbons;

Prague, Czechoslovakia ,

1978;

p p .

2092-94.

31, 79-89.

2

-81.

43,85-94.

95-102.

EPA/600/R-92/138.

1059-65.

27,2299-2323.

22,297-331.

1-4.

16, 9-43.

411-17.

2636 Environ.

Sci.

Technol.,

Vol.

27, o

13,

993

bioremediation in the rhizosphere

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