Professional Documents
Culture Documents
Contents
I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 79
II. Chemistry. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 80
III. Distribution of Arsenic . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 80
IV. Detection of Arsenic in Environmental Samples . . . . . . . . . . . . .. 84
V. Terrestrial Plants. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 85
VI. Microbial Transformations. . . . . . . . . . . . . . . . . . . . . . . . . .. 86
A. Bacterial Resistance. . . . . . . . . . . . . . . . . . . . . . . . . . . .. 86
B. Bacterial Oxidation . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 87
C. Bacterial Methylation. . . . . . . . . . . . . . . . . . . . . . . . . . .. 88
D. Fungal Methylation. . . . . . . . . . . . . . . . . . . . . . . . . . . .. 92
VII. Aquatic Transformations. . . . . . . . . . . . . . . . . . . . . . . . . . .. 94
A. Marine Environments . . . . . . . . . . . . . . . . . . . . . . . . . . . 94
VIII. Freshwater Environments . . . . . . . . . . . . . . . . . . . . . . . . . .. 99
IX. Toxicity of Arsenic. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 101
X. Stability of Organoarsenic Compounds . . . . . . . . . . . . . . . . . .. 102
XI. Global Cycle of Arsenic. . . . . . . . . . . . . . . . . . . . . . . . . . . .. 102
Summary. . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . .. 103
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 104
I. Introduction
Arsenic has both metallic and nonmetallic properties and is a member of the
nitrogen family. It occurs as a free element and combined form being widely
distributed in sulfide ores. The poisonous character of arsenic allowed for its
use as a herbicide, cattle and sheep dips, and insecticides. The ubiquity of
arsenic in the environment, its biological toxicity, and its redistribution are
factors evoking public concern. This review will cover the chemistry of arse-
nic and methods curently used to speciate the prevalent chemical forms in
various environments. The major focus of this review is on the biological
transformations of arsenic in both the terrestrial and aquatic systems.
79
80 s. Tamaki and W.T. Frankenberger
Emphasis has been placed on the link of these biotic transformations to the
global cycle of arsenic.
II. Chemistry
The arsenic cycle involves both biotic and abiotic reactions. Arsenic is a
naturally occurring element, present in soil, water, air, and all living matter. It
is a metalloid of Group VA of the periodic classification with properties that
allow it to form alloys with various metals and covalent bonds with carbon,
hydrogen, oxygen, and sulfur (Ferguson and Gavis 1972). The oxidation states
and electron orbitals are similar between arsenic and phosphorus. Arsenic is
subject to eight electron reductions and can occur in + 5, + 3, and - 3 states.
Its similarity to phosphorus and its ability to form covalent bonds with sulfur
are two reasons for arsenic toxicity. Arsenate (H 3 As0 4 ) is an analogue of the
essential mineral phosphate and is taken up via the phosphate transport
system by most organisms. Arsenate has been postulated to replace phosphate
in energy transfer phosphorylation reactions. Arsenite (AsO z -) has a high
affinity for thiol groups of proteins inactivating many enzymes.
Arsenicals Use
Feed Additives
Arsanilic acid and Roxarsone (3-nitro- Increase rate of gain and imporve feed
4-hydroxyphenyl arsonic acid) efficiency in chickens and swine,
control swine dysentery
Carbarsone and nitarsone (4- Antihistomonads in turkeys
nitro phenyl arsonic acid)
Pesticides
Herbicides (mono-disodium salts of Post emergence grass herbicides
methane arsonic acid)
Insecticides
Calcium arsenate Control boll weevil in cotton fields
Component in snail baits; used in fly
control in poultry houses, herbicide
for grass Poa annua
Lead arsenate Control codling moth, plum curculio,
cabbage worm, potato bug, and
tobacco horn worm
Fungicides
Sodium arsenite U sed to preserve railroad and
telephone posts, fungicide, and wood
preservation. Control measles and
dead arm of table grapes
10,10-0xybisphenoxarsine Fungus control in cotton sail-cloth and
vinyl films
Dessicants/deJoliants
Dimethylarsinic (cacodylic) acid Cotton defoliants
Other
Lead and calcium arsenate Control acidity in grapefruit
pH
2 4 6 8 10 12 14
As0 43
0
pE
2
-6
Reduced
8 Wale'
14
Quantitative data for total organoarsenicals are usually limited because ofthe
indirect determination calculating the differences between inorganic species
and total arsenic.
Analyses by AAS or leAP do not allow direct determination of arsenate in
environmental samples. Recently a method was developed for the direct
determination of arsenate in aqueous soil extracts by single-column ion
chromatography (SCIC) at trace levels (Mehra and Frankenberger 1988).
Separation is carried out on a low-capacity anion-exchange resin column
being quantified by conductometric detection. Trace amount measurements of
arsenate (detection limit, 92 J.Lg L -1) were made in the presence of other
oxyanions, N0 3 -, P0 4 3 -, and SO/-.
v. Terrestrial Plants
Terrestrial plants growing on shores bordering arsenic contaminated water
show relatively little arsenic content despite the fact that sediments may
contain levels as high as 200 J.Lg As g - 1 (Reay 1972). Furthermore resistance to
arsenic can be increased by acclimating plants to successively higher
concentrations of arsenic. Little bluestem, Andropogon scoparius Michx. can
survive in soil containing up to 41,200mg kg- 1 of arsenate (Wauchope 1983).
The soil matrix plays an important role in the availability of arsenic to
plants. Retort oil shales have high concentrations of arsenic but plants grown
on these soils show little accumulation ranging from 0.03 to 0.44 mg kg- 1
(Kilkelly and Lindsay 1982). Plant toxicity to arsenic is often reached
prior to accumulation of levels which would be toxic to wildlife ingesting
the plants.
In studies of arsenate uptake by barley, it was reported that uptake is
temperature dependent increasing with increasing temperatures (Asher and
Reay 1979). Arsenate is preferentially taken up 3 to 4 times the rate of arsenite.
The presence of phosphate inhibits the uptake of arsenate while arsenate only
mildly inhibits phosphate uptake. In terrestrial plants as in most other
systems, arsenate and phosphate are thought to compete for the same uptake
system but there appears to be a higher affinity for phosphate (Asher and Reay
1979). The discriminate ratio between phosphate and arsenate is approxi-
mately 4: 1.
In corn, peas, melons, and tomatoes, absorbed arsenate is rapidly reduced
to arsenite. Terrestrial plants do not synthesize lipid-soluble arsenic com-
pounds. Methylation of the arsenite occurs under phosphate deficient
conditions and increases substantially when plants are also made nitrogen
deficient. The methylated compounds accumulate to approximately 6 times
greater concentration in the leaves than in the roots. Plants which show high
levels of arsenic methylation are atypical and are considerably deformed due
to the nutrient deficient growth conditions (Nissen and Benson 1982).
Synthesis of methylated arsenic compounds by terrestrial plants is not
necessarily a detoxification mechanism.
86 S. Tamaki and W.T. Frankenberger
on their presence and is stimulated 5-fold by the addition of arsenite and 50-
fold with the addition of antimonate (Rosen et al. 1988).
The ArsA protein is mainly cytosolic but a portion is found sedimented
within the cell membrane and is thought to complex with ArsB. ArsB is found
in the inner membrane of E. coli and has been postulated to be the portion of
the pump responsible for the export of anions from the cell. The deduced
amino acid sequence of ArsB reveals several regions of the protein which are
potentially transmembrane. The 16 kd ArsC polypeptide modifies the ArsA-
ArsB complex allowing the pumping of arsenate. ArsC is not required for the
effiux of arsenite or an timon ate (Chen et al. 1986). The plasmid-encoded
resistance for arsenate/arsenite is highly specific for oxyanions. It fails to
protect E. coli cells from concentrations of 0.1 mM phenylarsine oxide or 10
mM Na cacodylate (Mobley et al. 1983) but is highly selective in preventing
the export of phosphate from the cell (Mobley and Rosen 1982).
Resistance to arsenic is inducible and a fourth gene has recently been
identified which regulates the arsenic resistance operon. Plasmid encoded
resistance results from the activation of an anion-translocating ATPase with
high selectivity for arsenate, arsenite, and antimonate (Rosen et al. 1988).
Plasmid-encoded resistance for arsenate/arsenite is widespread among
different bacterial species (Nakahara et al. 1977; Smith 1978; Dabbs and Sole
1988). Hybridization studies indicate that a number of arsenate resistant
strains of Klebsiella pneumoniae and E. coli possess sequences homologous to
the plasmid encoded genes. However, genes involved in arsenic resistance are
not completely conserved among different bacterial strains. In Staphylococcus,
three genes are also involved in conferring resistance to arsenic, however,
sequence analysis indicates only ArsB, the gene encoding the transmembrane
protein, shares homology with sequences of R773 (Silver and Misra 1988).
Furthermore, strains of E. coli, K. pneumoniae, and Klebsiella oxytoca that are
resistant to arsenic have been isolated which lack sequences homologous with
ArsA, ArsB, or ArsC genes. One significant feature of the epidemiology of
bacterial arsenic resistance is the fact that it is often associated with other types
of heavy metal and antibiotic resistances (Smith 1978).
Arsenite is much more toxic to aquatic microbiota of agricultural drainage
water and evaporation pond sediments than any other As species (Huysmans
and Frankenberger 1990a). The addition of As(V), methanearsonic acid and
dimethylarsinic acid (0.1 to 1000 mg L - 1) to culture medium had no effect on
colony-forming units from water samples while As(III) (> 1.0 mg L - 1) in-
hibited the population. The As-resistant bacteria showed a high tolerance to
other trace elements (e.g., Co, Cu, Pb, Ni, Mo, Cr, Se(IV), Se(VI), Sb, Sn, and
Ag) and antibiotics.
B. Bacterial Oxidation
Bacteria are approximately lO-fold more resistant to arsenate than arsenite.
Bacillus and Pseudomonas species have been isolated which can oxidize
88 S. Tamaki and W.T. Frankenberger
C. Bacterial Methylation
~
Penicillium brevicaule Trimethylarsine Bread crumbs spiked Challenger et al. (1933)
a.
....
(Scopulariopsis with As 20 3 or '<
0
....,
brevicaulis) methyl arsenate or
cacodylate >
....
<l>
Penicillium notatum Trimethylarsine Sodium methylarsonate Bird et al. (1948) ::s'"
Penicillium chrysogenum Trimethylarsine and sodium cacodylate
o
Aspergillus niger Trimethylarsine
Aspergillus glaucus Trimethylarsine Bread crumbs treated Bird et al. (1948)
with arsenous and
methyl arsonic acids
Lenzites trabea Volatile As derivative Medium containing Merril and French (1964)
with garlic odor As trioxide
(probably trimethylarsine)
(Continued)
00
'-0
\0
o
Table 2. (Continued)
sodium arsenate, a
~
methanearsonic and, ~
~
dimethylarsinic acids ::l
0-
Candida humicola Trimethylarsine Substrate was chromate Cullen et al. (1984a) ~
copper arsenate ~
(wood preservative) ...'I1
po
::l
GliocIadium roseum Trimethylarsine Methanearsonic and Cox and Alexander (1973a,b, 1974) i><"
n
Pencillium sp. dimethylarsinic acids ::l
<J
Aeromonas sp. Trimethylarsine Nutrient broth, containing Chau and Wong (1978) ...n
(JQ
OH CH3-B'2 B'2 CH 3
2
+51 8 3 '- ~ +31
HO- As-OH ~ A; - OH _-"----"'.L'--, HO- As-OH
I I ~
o o o
arsenate arsenite methylarsonic acid
CH 3 CH 3
+1 1 ~ -31
r
28
HO- As -CH3
~
o
~ As-CH 3
H
I
dimethylarsinic dimethylarslne
acid
Fig. 2. Anaerobic biomethylation pathway for dimethylarsine production by
Methanobacterium sp. (McBride and Wolfe 1971).
D. Fungal Methylation
It is well establishsed that fungi are able to transform inorganic and organic
arsenic compounds into volatile methylarsines. The volatilized arsenic
dissipates from the cells effectively reducing the arsenic concentration the
fungus is exposed to. The importance of fungal metabolism of arsenic dates
back to the early 1800s where a number of poisoning incidents in Germany
and England were caused by a volatile methyl arsine gas. The victims lived in
musty rooms with a characteristic garlic-like odor. Trimethylarsine was
identified as the toxic compound (Challenger 1945). Molds growing on
wallpaper decorated with arsenical pigments (Scheele's green and Schweinfiir-
ter green) produced the toxic trimethylarsine gas. Since then, several species of
fungi have been identified that are able to volatilize arsenic (Cox and
Alexander 1973a). The fungus, Penicillium brevicaule (Scopulariopsis brevi-
caulis) produces trimethylarsine when grown on bread crumbs containing
either methanearsonic acid or dimethylarsinic acid. A biochemical pathway
for trimethylarsine production has been proposed by Challenger (1945)
(Fig. 3).
In recent studies, three different fungal species Candida humicola, Glioc-
ladium roseum, and Penicillium sp. were capable of converting methanearsonic
and dimethylarsinic acids to trimethylarsine (Cox and Alexander 1973a). In
addition, C. humicola used arsenate and arsenite as substrates to produce
trimethylarsine. Cell-free homogenates of C. humicola transformed arsenate
OH OH OH OH OH OH
I I I I I I
HO-As-OH - HO-As-OH -HO-As-CH3 - HO-As-CH3 - H3C-As-CH3 -H3C-As-CH3
II I I
0 I
NH2
y y (-.AN
0-1 y Oy N-lN)
H3 H3 CH 3
O-ts-CH2COOH
C1 H3 ~ CH3
dimethyloxarsylacetic acid
yH 3
---
O=ts- CH2CH20H H3C- ~- CH 2COOH
CH3 "
yH 3
CH 3
Fig. 3. Fungal methylation pathway for the formation oftrimethylarsine (Craig 1986
[modified after Challenger, 1945]).
Biochemistry of Arsenic 93
mM (KH 2 PO 4)' The addition of carbohydrates and sugar acids to the minimal
medium suppressed trimethylarsine production. The amino acids, pheny-
lalanine, isoleucine, and glutamine promoted trimethylarsine production with
an enhancement ranging from 10.2- to 11.6-fold over the control without
amino acid supplementation.
Methylation of arsenic is thought to occur via transfer ofthe carbonium ion
from S-adenosylmethionine (SAM) to arsenic. Incubation of cells with an
antagonist of methionine inhibits production of arsines thus supporting the
role of methionine as a methyl donor (Cullen et al. 1977). The addition of either
methanearsonic acid or dimethylarsinic acid to cell-free-extracts yields
trimethylarsine oxide (Cullen et al. 1979). Further reduction oftrimethylarsine
oxide to trimethylarsine requires the presence of intact cells (Pickett et al.
1981). Various arsenic thiols (cysteine, glutathionine, and lipioc acid) are
thought to be involved in the reduction step of trimethylarsine oxide to
trimethylarsine (Cullen et al. 1984b,c). The final reduction step is inhibited by
several electron transport inhibitors and uncouplers of oxidative phosphoryl-
ation (Zingaro and Bottino 1983; Pickett et al. 1981). Preincubation of cells
with trimethylarsine oxide increases the rate of conversion to trimethylarsine
suggesting an inducible system (Pickett et al. 1981). In addition, the rate of
transformation of arsenate to trimethylarsine is increased by preconditioning
the cells with dimethylarsinic acid (Zingaro and Bottino 1983). The com-
pounds isolated during the reduction of arsenate by C. humicola are consistent
with the intermediates reported in the pathway for methylation of arsenic as
proposed by Challenger (1945).
Soil fungal species may play a major role in the transformation and
movement of arsenic chemicals used in agriculture. The methylation of
arylarsonic acids is important because of their wide use as food supplements
for swine, turkeys, and poultry. Candida humicola is capable of methylating
benzenearsonic acid to produce volatile dimethylphenylarsine (Cullen et al.
1983). In addition, methylphenylarsinic acid and dimethylphenylarsine oxide
are also reduced by C. humicola to dimethylphenylarsine. Arsanilic acid, which
contains an amino group at the para position of phenylarsonic acid was not
converted to a volatile arsine but it has been reported that soils treated with
arsanilic acid can lose their arsenic component.
94 S. Tamaki and W.T. Frankenberger
OH
~2.
29 ~+ I
H2As v0 4 - ~SIIlO(OHr CH 3-As v=O
I
O'
arsenate reduction arsenite methylation methanearsonic
acid
O' CH 3
~2. I ~+ I
CH3-As"'=O CH 3-Asv=O
I
O'
methanearsonous dimethylarsinic
anion acid
CH3 CH 3
I
2.L_~t I
CH3-As"'-O'
~+ CH 3-Asv=O
I
CH 3
dimethylarsinous trimethyiarsine
anion oxide
CH 3
~2' I
: ASIII- CH 3
I
CH 3
trimethylarsine
2. Marine Invertebrates and Fish. Fish and invertebrates are parts of the
higher trophic levels in the food web of marine environments. The primary
producing phytoplankton and macro algae can accumulate arsenic and
transform inorganic forms into complex organic molecules that may be
converted into water-soluble or lipid-soluble arsenic compounds. Consump-
tion of primary producers by a higher trophic level metabolizes the
organoarsenic compounds into other forms. Fish and marine invertebrates
retain 99% of the arsenic in the organic form. The concentration of inorganic
arsenic rarely exceed 1.0mgkg- 1 in their tissues (Maher 1983). Generally,
arsenic concentrations are higher in crustacean and mollusk tissues compared
to fish (LeBlanc and Jackson 1973; Maher 1983).
Chemical structures have been determined among several of the predomi-
nate water-soluble arsenic compounds in invertebrates and fish. Giant clams
of the genera Tridacna and Hippopus concentrate arsenic in their kidneys to
levels greater than 1,000 mg kg- 1 dry wt (Benson and Summons 1981). The
arsenic is obtained from symbiotic unicellular algae, zooxanthellae, which
transforms arsenate in seawater to organic compounds that are passed to the
host clam. In Tridacna maxima kidney tissue, two organoarsenic compounds
were isolated and identified as trimethylarsoniumlactate and 0-
glycerophosphoryl- trimethylarsoniumlactate accounting for the majority of
the cellular arsenic (Benson and Summons 1981). The most predominant
organoarsenic species, however, was not identified but was also thought to be
a lactate derivative. The synthesis of arsenolipids are proposed as an
adaptation by the clams to reduce the cellular arsenic concentration. The
arsenolipids protrude from the gill membranes into the surrounding marine
waters and become accessible to bacteria which oxidize the lipids and release
the arsenic moiety as dimethylarsinic acid (Benson and Nissen 1982).
Dimethylarsinic acid and minor amounts of methanearsonic acid are also
present in clam tissue (Benson and Summons 1981).
The unequivocal identification of the water-soluble lactate compounds in
clam kidney tissue is subject to dispute (Edmonds and Francesconi 1987).
98 s. Tamaki and W.T. Frankenberger
Edmonds and Francesconi (1982) isolated and determined the X-ray crystal
structure of two water-soluble arsenic compounds present in the kidneys of T.
maxima. These two compounds accounted for 80% of the total arsenic in the
kidneys and were identical to the dimethylarsenosugars isolated from E.
radiate (Edmonds and Francesconi 1981 b). Arsenosugar synthesis is not
unique to E. radiata and its presence in clams was thought to be due to the
arsenosugar synthesis by the symbiotic algae with passage to the host
accumulating in the kidneys. However, current evidence suggests that the
arsenosugars were misidentified as arsonium lactate compounds by Benson
and Summons (1981) and thus any reference in the literature to arsonium-
lactate compounds must be carefully evaluated.
Arsenobetaine has been isolated and purified from the Australian rock
lobster, Panulirus longipes (Cannon et al. 1981; Edmonds et al. 1977) and the
dusky shark, Carcharhinus obscurus (Cannon et al. 1981; Kurosawa et al.
1980;). In flounder, sole, lemon sole, dab, and shrimp, the major arsenic species
was recovered as arsenobetaine (Luten et al. 1983). The concentrations of
arsenic ranged from 0.45 to 31.4 j1g g - 1 dry wt. In shark, arsenobetaine is the
predominant arsenic species in both muscle and liver tissues (Kurosawa et al.
1980). In the muscle, 80% of arsenic was detected in the aqueous fraction, 10%
in the residue and almost none in the lipid fraction. In contrast, in the liver,
40% of the total arsenic was found in the aqueous fraction while 45%
in the lipid fraction. In shrimp, arsenobetaine constitutes two-thirds
of the arsenic pool while the remainder has tentatively been identified
as arsenocholine (Norin and Christakopoulos 1982; Norin et al.
1983). However, other investigators have been unable to confirm the
presence of arsenocholine in other shrimp species (Luten et al. 1983;
Shiomi et al. 1984).
It is unclear how arsenosugars and arsenolipids are transformed into
arsenobetaine within the higher trophic levels of the marine environment. The
American lobster, Homarus americanus, retains arsenic in its muscle tissue as
arsenobetaine (Edmonds and Francesconi 1981a), but is unable to synthesize
arsenobetaine from organoarsenic compounds obtained from ingested algae
(Cooney and Benson 1980). The generation of arsenobetaine from arseno-
sugars requires cleavage at the C 3 -C 4 bond of the sugar residue and the
subsequent oxidation of the C 4 carbon. Furthermore, reduction and methyl-
ation of the arsenic atom must occur to form the quaternary (tetraalkylated)
arsonium compound of arsenobetaine (Edmonds and Francesconi 1987).
Dimethylarsinoylethanol (see Fig. 4 for chemical structure), a product of
anaerobic bacterial decomposition of arsenosugars in Ecklonia, has been
proposed as an intermediate in the formation of arsenobetaine (Edmonds et al.
1982). However, the process in which dimethylarsinoylethanol is transformed
into arsenobetaine is unclear. There is no evidence that suggests bacteria have
the potential to carry out the necessary quaternary methylation (Edmonds
and Francesconi 1987). Thus the pathway involved in the synthesis of
arsenobetaine remains largely undetermined.
Biochemistry of Arsenic 99
form. Both inorganic and organic arsenic compounds accumulate in the liver
and are secreted with the bile into the lumen. Inorganic arsenic is thought to be
methylated by the intestinal microflora in the gastrointestinal tract and then
preferentially reabsorbed into the body of the fish. Two organic arsenic
compounds were detected in trout and were clearly distinct from arseno-
betaine. There is no clear evidence that fish are capable of directly convert-
ing inorganic arsenic into methylated species.
,,'::""
.- .- .- .-
.- .-
.- ,. ,. ,.
;'
,. ,. ,. ,.
;'
;' ;'
"
""/ "Vapor
"
I I 210
I I . - -.......-.1
I I
Emissions
621 158.3
I I
\ \
\ \
\
,
\
\ \
"
I \ _ _ _.........-
\ FOssil
" Fuels
\ 158.3,
Mini~OI "
,,
SuKide Ores ,
and " " Sediments
Cement, '
Manufacturing 250,000,000,000
621 " ,,
Loss
1,129
Fig. 5. Global biogeochemical cycle of arsenic. Reservoir masses and fluxes are
expressed in units of 108 and 108 gjyr, respectively (Mackenzie et ai., 1979).
Summary
Microorganisms are involved in the redistribution and global cycling of
arsenic. Arsenic can accumulate and can be subject to various biotransform-
ations including reduction, oxidation, and methylation. Bacterial methylation
of inorganic arsenic is coupled to the methane biosynthetic pathway in
methanogenic bacteria under anaerobic conditions and may be a mechanism
for arsenic detoxification. The pathway proceeds by reduction of arsenate to
104 S. Tamaki and W.T. Frankenberger
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