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VIII. Soil As and Microorganisms

VIII. Soil As and Microorganisms

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183



ARSENIC IN THE SOIL ENVIRONMENT: A REVIEW



Industrial Sources



(CH&&O(OH)

(CH&AsO



Arsenical Herbicides

and Pesticldes



T



Local



Dust



I I Consumptton

iH



Oxygen present

HAs02



1



As406



I



Oxygen absent

H2A~04-



H2AS04-



HAs02



Leaching

Figure 7 Soil-air cycle (WHO, 198 1; reprinted by permission of the publisher).



63, and 32 mg kg- for Cu, Cr, As, and B, respectively) were considerably lower

than those present in Bisessar's (1982) work.

Considerable variation in tolerance to As compounds applied to the soil has been

shown by the soil microflora. Maliszewska et al. (1985) reported that As"' compounds were more toxic than As" compounds to microorganisms important to

maintaining soil fertility.Arsenite compounds were applied at 500, 1500,and 3000

mg As kg- I and As" compounds at 1000,5000, and 10,000 mg As kg- to sandy

and alluvial soils. The influence of As"' and As" compounds on the soil microflora differed, depending on the microflora and the soil type. In sandy soil, As"' depressed the growth of bacteria, whereas As" stimulated their proliferation. Overall, both As compounds had little effect on the development of actinomycetes and

fungi flora and suppressed the growth of Azotobacter sp.

Maliszewska et al. (1985) also measured a decrease of approximately 30% in

dehydrogenase activity in the soils. The decrease in activity was greatest in the

sandy soil and with the application of As"'. Dehydrogenase is an unspecific enzyme for assessing the effect of As compounds on the soil microflora; other authors have found that enzymes involved in more specific biochemical reactions are

inhibited by the addition of As to the soil environment. Tabatabai (1977) reported

that As"' greatly inhibited the urease activity of some soils at a concentration of

375 mg As"' kg- I , but the addition of As" at a similar concentration to the soil

had no effect on activity. Bardgett er al. (1 994) investigated microbial properties



Table VIII

Total As, Pb, Cd, and Cu Concentration and Counts of Sod Microflora Near a Secondary Pb SmelteP

Total heavy metal

concentration (mg kg-I)

Location

(eastofsource)



Pb



As



Cd



Total no. of colonies

Cu



Bacteria



Actinomyces



~ _ _ _ _ _ _



15 m

90 m

150 m

180 m



Control (1000 m

south)



28,000

8333

4800



3564

703



972

554

230

163

57



151



599

398

287



102

33

26



333



5



73



10.5

12

12.6

15.1

17.2



Fungi



in log soil

Nematodes



_ _ _ _ _ ~



1



1.4

1.6

2.1

2.4



“Bisessar, 1982; reprinted with kind permission from Kluwer Academic Publishers.



2.5

3.2

3.5

4.3

4.6



Earthworms



~



16

30.9

26.6

58

98



0



0

0

1.3

2.3



ARSENIC IN THE SOIL ENVIRONMENT: A REVIEW



185



of the surface (0-50 mm) of a pasture soil contaminated by runoff by preserving

liquor runoff from an adjacent timber-treatment plant. Total concentrations of Cr,

Cu, and As ranged from 86 to 1260,70 to 1233, and 79 to 1265 mg kg-', respectively. They found no significant relationship between soil As, Cu, and Cr concentrations and urease activity, whereas a significant relationship was observed between As, Cu, and Cr (? values = As, 0.923; Cu, 0.933; Cr, 0.872) and a decline

in sulphatase activity. However, many factors may influence the inhibitory effect

of metals on the soil microflora, with soil type being an important factor in determining the bioavailability of the metals (Maliszewska et al., 1985).



A. BIOTRANSFORMATION

OF As INSOILS

The biotransformation of As in soils has been recognized for many years. Two

microbial processes, oxidation and reduction, are of current interest because of

their possible application for bioremediation of contaminated soil. A number of review articles have discussed As and its transformation in various environments

(Cullen and Reimer, 1989; Ehrlich, 1996), and these articles provide a more in

depth review of the subject than is provided here.

Bacterial oxidation was first identified by Green in 1918 wh en a bacterium from

a cattle-dipping fluid was isolated. Many other heterotrophic As"' oxidizing bacteria have since been characterized, with many bacterium classified as Bacillus or

Pseudomonas spp. Studies by Osborne and Ehrlich (1976) reported that Alcaligenesfaecalis was able to oxidize As"' to As", although it was not clear if their

organism derived energy from this process. The oxidation of reduced As species

has been less widely studied than the processes of microbial reduction of As.

Various bacteria, fungi, and algae organisms that are able to reduce As compounds have been identified. The reduction of AsV to As"' has been reported to be

carried out by Pseudomonasjuorescens under anaerobic conditions, wine yeast,

rumen bacteria, and cyanobacteria (Cullen and Reimer, 1989). Cheng and Focht

( 1979) have also identified that Pseudornonas and Alcaligenes were able to produce arsine gas directly from As" solutions in glucose and urea-enriched soils under anaerobic conditions. The ability of organisms to reduce inorganic As species

directly has only been reported so far for bacteria. The bacterial methylation of inorganic As has been extensively studied in methanogenic bacteria. Methanogenic

bacteria are a morphologically diverse group that produce methane as their primary metabolic end product under anaerobic conditions (Tamaki and Frankenberger, 1992). McBride and Wolfe (1971) reported that cell extracts of whole cells

of the Methanobacterium strain MOH, growing anaerobically, reduced and methylated As" to dimethylarsine. Anaerobic biomethylation of As only proceeds to dimethylarsine, which is stable in the absence of 0, but is rapidly oxidized under

aerobic conditions (Cullen and Reimer, 1989). The pathway of As" methylation



186



E. SMITH ETAL.



initially involves the reduction of AsVto As"', with the subsequent methylation of

As"' to dimethylarsine by coenzyme M (Frankenberger and Losi, 1995).

In addition to bacteria, several fungi species have the ability to reduce As

species. It is well known that fungi and algae are able to methylate As. Toxic

trimethylarsine gas is volatilized, and the liberalization of this gas by molds growing on wallpaper decorated with As pigments led to a number of poisoning incidents in the 1800s in England and Germany (Challenger, 1945). Cox and Alexander (1973a) reported that three fungal species, Candida humicola, Gliocladium

roseurn, and Penicilliurn sp. were capable of transforming methylarsonic and dimethylarsonic acids to trimethylarsine. Further work by Cox and Alexander

(1973b) showed that other anions, notably phosphate, inhibited the formation of

trimethylarsine from inorganic As and methylarsonic acid.

The extent to which microbial activity is involved in the transformation and

movement of As in the soil is difficult to quantify. Woolson (1977) detected the generation of alkyarsines, notably dimethyarsine and trimethylarsine, in both anaerobic and aerobic conditions in the laboratory. Furthermore, the rate of formation of

volatile compounds from the three As compounds applied to the soil (74As-sodium

arsenate, I4C-MSMA, and 14C-cacodylicacid) was fastest under aerobic conditions, with the nature of the As compounds influencing the rate of formation. Hassler el al. (1984) suggested that, in addition to methylating As compounds, microbiological mobilization of As may occur under certain soil conditions. Woolson and

Kearney (1973) found that the loss of 14C-cacodylicacid, applied to a range of soils

and incubated over several months, was influenced by soil type, concentration of

cacodylic acid applied, and soil moisture levels. Losses were attributed to the production of methylarsines and were greatest at the higher rates of cacodylic applied

(100 mg As kg-I) in anaerobic conditions and in sandy soils.

Few studies have investigated the long-term effects of microbial transformations of As species. In many instances, microbial influences on As sorption and

desorption processes have been largely ignored in laboratory studies. Under shortterm laboratory studies and with previously uncontaminated soils, the microorganisms may have little influence on sorption processes in soils. However, there

may be important implications for long-term studies, or where the soil microflora

and microfauna have been predisposed to As when studying As sorption-desorption processes in laboratory situations.



M.CONCLUSIONS

Arsenic is widely distributed in nature, with traces of As in the soil almost universal. The behavior of As in the soil is dominated by As speciation. In soil solutions the inorganic As species predominate, either as AsV or As"'. Under moderately oxidizing conditions (> + 100 mV) AsV will predominate, whereas under



ARSENIC IN THE SOIL ENVIRONMENT: A REVIEW



187



moderately reducing conditions As111will predominate. The conversion of As from

one oxidation state to another in soils is also affected by other soil parameters, including pH and microbial activity. The importance of microbial activity in controlling As species present in soil environments is well acknowledged, but the

pathways and kinetics of the microbial processes are not well understood.

An understanding of the physiochemical behavior of As in the soil is important

for quantifying the persistence and bioavailability of As in the environment. The

sorption of As onto soil surfaces plays an important role in mediating the availability of As in the environment. Iron, Al, and to a lesser extent Mn oxides are important soil constituents in controlling soil solution concentrations of As. Soil pH

has a major influence on the availability of As. Arsenic is apolyprotic acid, and pH

has a major influence on the valence charge of the As ion in soil solution and hence

on the As adsorbed.

In general, bioaccumulation of As to hazardous levels for human and animal

consumption in the edible portions of plants seldom occurs because of the phytotoxic effects before such hazardous levels are reached. Plants accumulate the highest concentrations of As in plant roots. Unlike other elements such as P, As is not

generally translocated to other parts of the plant. However, some plant species have

been found to translocate As to a greater extent than others.

Future research of As in soils is needed to understand factors controlling the nature of As species in the soil solution, as well as the role of microbes in controlling As speciation. Although adsorption processes have been well studied, further

work is needed in understanding desorption processes and the factors that influence the kinetics of these processes. Scope also exists for studies on both plant and

microbial uptake of As and the possible use of plants as low-cost, long-term means

of remediation of As-contaminated sites.



ACKNOWLEDGMENTS

We would like to thank Primary Industries for South Australia and the Co-operative Research Centre for Soil and Land Management for their support.



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