Previous Article | Next Article 
Applied and Environmental Microbiology, October 1998, p. 3759-3764, Vol. 64, No. 10
0099-2240/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
Toxic Effects of Modified Fenton Reactions on
Xanthobacter flavus FB71
Fatïh
Büyüksönmez,1
Thomas F.
Hess,1,*
Ronald L.
Crawford,1 and
Richard J.
Watts2
Center for Hazardous Waste Remediation
Research, University of Idaho, Moscow, Idaho
83844,1 and
Department of Civil and
Environmental Engineering, Washington State University, Pullman,
Washington 991642
Received 9 March 1998/Accepted 21 July 1998
 |
ABSTRACT |
The toxic effects of modified Fenton reactions on
Xanthobacter flavus FB71, measured as microbial survival
rates, were determined as part of an investigation of simultaneous
abiotic and biotic oxidations of xenobiotic chemicals. A central
composite, rotatable experimental design was developed to study the
survival rates of X. flavus under various
concentrations of hydrogen peroxide and iron(II) and at different
initial cell populations. A model based on the experimental results,
relating microorganism survival to the variables of peroxide, iron, and
cellular concentrations was formulated and fit the data reasonably
well, with a coefficient of determination of 0.76. The results of
this study indicate that the use of simultaneous abiotic and biotic
processes for the treatment of xenobiotic compounds may be possible.
| |
INTRODUCTION |
Abiotic-biotic processes, used for
the destruction of recalcitrant compounds in industrial effluents and
contaminated sites, have been the subject of recent research (1,
5, 6, 11, 25, 26, 35, 38). In all of these studies, the authors investigated sequential processes by using an abiotic reaction as
pretreatment for a separate, later biological reaction. One area of
study that has received little attention, however, is the
investigation of simultaneous abiotic and biotic
transformation processes. Such coexisting reactions could have
both economic and process advantages when applied to industrial
pollution prevention schemes or to in situ remediation of hazardous
wastes. One major limitation to combining these reactions
simultaneously is the toxicity of elements of abiotic reactions to
microorganisms. Therefore, as part of an overall coexisting
abiotic-biotic transformation process study, we investigated the toxic
effects of modified Fenton reactions, a common abiotic transformation
process (27, 28, 31, 37, 44), on Xanthobacter
flavus, a xenobiotic chemical-degrading microorganism.
The Fenton reaction, a widely used abiotic transformation process, is
the catalyzed decomposition of hydrogen peroxide by transition metals,
which results in the generation of hydroxyl radicals and other species
such as superoxide and hydroperoxyl radicals (18, 19, 34).
The standard Fenton procedure involves adding dilute hydrogen
peroxide to a degassed solution of iron(II), which results in
nearly stoichiometric generation of hydroxyl radicals. However, most
environmental applications of Fenton chemistry have some modifications,
including the use of higher concentrations of hydrogen peroxide,
phosphate-buffered medium, iron(III), or heterogeneous catalysts. These
conditions, although not as stoichiometrically efficient as those in
the standard Fenton reaction, are often necessary to treat industrial
waste streams (18) and sorbed contaminants in soils and
groundwater (41).
Hydroxyl radicals generated by modified Fenton reactions react with
most environmental contaminants at near diffusion-controlled rates
(>109 M
1 s1). The degradation
of xenobiotic chemicals by hydroxyl radicals then proceeds via either
hydroxylation or hydrogen atom
abstraction: ·OH + R 
·ROH (1)·OH + RH2 ·RH + H2O (2)
Many biorefractory compounds, such as perhalogenated
alkenes, dienes, and benzenes (e.g., perchloroethylene,
hexachlorocyclopentadiene, hexachlorobenzene), are effectively
degraded by hydroxyl radicals within minutes (27, 37,
42). Based on these high transformation rates, there has been an
increased interest in oxidation processes for soil and groundwater
treatment.
Coexisting abiotic-biotic reactions may have application in in situ
soil and groundwater remediation and could possibly occur during such
efforts. Hydrogen peroxide, which is miscible and dissociates to oxygen
and water, has been commonly used as an oxygen source for in situ
bioremediation (9, 32, 33). However, in some instances, due
to rapid dissociation of the hydrogen peroxide, oxygen transfer was
found to be limited to the area close to the injection well. This quick
dissociation was later attributed to microbial enzymatic activity and
iron and copper salts present in the soil matrix (8, 9, 39).
Data from Tyre et al. (41) and Watts et al. (43)
suggest that naturally occurring iron oxyhydroxides can serve as
effective Fenton catalysts. Fenton reactions, then, were probably
taking place in the in situ bioremediation applications where hydrogen
peroxide was being used to increase dissolved-oxygen concentrations.
Additionally, interest in abiotic remediation technologies has led to
the recent commercialization of modified Fenton reaction systems for
use in situ (3). Both abiotic and bioremediation
technologies may ultimately benefit from coexisting abiotic-biotic
reactions.
The elements of Fenton reactions, such as hydrogen peroxide, hydroxyl
radicals, and other radical species, are highly toxic to living
organisms. The toxicity of the reactive oxygen species comes from their
ability to oxidize a large number of cellular constituents. Toxicity
mechanisms include DNA disruption (2, 40), oxidation of
proteins and amino acids (7, 47), and lipid peroxidation of
membrane fatty acids (30). While the toxicity of hydrogen
peroxide to microorganisms has been the subject of many investigations
(2, 10, 15, 20, 46), there has been no attempt to quantify
the toxic effects of the radicals involved in modified Fenton reactions
on similar biological systems.
The purpose of this research was to investigate the toxic effects of
modified Fenton reactions on Xanthobacter flavus FB71, a
hazardous-compound-degrading bacterium. Survival of bacterial populations was modeled statistically for various combinations of the
treatment parameters: (i) H2O2 concentration,
(ii) Fe(II) concentration, and (iii) initial cell number. The effect of
treatment conditions on the activities of selected microbial enzymes
was also determined.
| |
MATERIALS AND METHODS |
Bacterial growth conditions and strain determination.
We
isolated a strain of bacterium that utilized dichloroacetic acid from
waste activated sludge of a sewage treatment plant in Pullman, Wash.,
as the sole carbon and energy source. Isolation and growth media
contained, per liter of distilled water, 200 mg of dichloroacetic acid
sodium salt (98%; Aldrich), 15 g of Noble Agar (Difco), 3.4 g of Na2HPO4, 1.5 g of
KH2PO4, 0.25 g of NaCl, 0.5 g of
NH4Cl, 0.12 g of MgSO4, 5.55 mg of
CaCl2, 2 ml of Wolfe's mineral solution (17),
and 2 ml of vitamin supplement stock solution containing (per liter) 50 mg each of biotin, thiamine HCl, and nicotinic acid (Sigma). The
organism was identified, with a similarity index of 0.909, as X. flavus by cell wall fatty acid analysis (Acculab).
Following microbial isolation, the carbon source within the above
defined growth medium (minus Noble Agar) was switched to pyruvic acid
sodium salt (98%; Aldrich) to promote rapid growth. A number of
authors have reported that the appearance of the microbial enzymes
involved in the detoxification of reactive oxygen species is dependent
upon the timing within the growth stage (22, 23, 29, 36,
45). Therefore, to ensure the consistency of harvested cells
and enzyme activities, cells were grown in a 1.5-liter volume at
steady state in a continuous-flow chemostat (New Brunswick Scientific
BioFlo-III) with 1.0 liter of fresh growth medium per day at 30°C and
with stirring at 200 rpm and aerated with 3 liters of sterile air per
min.
H2O2 acclimation.
Cells were
acclimated to high levels of H2O2 (Fisher
Scientific) under similar chemostat-growth conditions to those detailed above, with the addition of increasing concentrations of peroxide. The
H2O2 was added to the fresh medium during
operation of the chemostat at concentrations of 100 mg/liter for the
first day, 200 mg/liter for the second day, and 300 mg/liter for the
third day. After the third day, the medium was maintain at an
H2O2 concentration of 300 mg/liter.
Cell extracts.
Cells harvested from the chemostat were
recovered by centrifuging at 4°C and 10,000 × g for
10 min with a Beckman centrifuge (model J2-MC). The cells were
resuspended in 0.05 M phosphate buffer and then lysed by being passed
through a French press three times under cell pressure of 11,000 lb/in2. Debris-free extracts were obtained by centrifuging
the lysate at 4°C and 15,000 × g for 30 min and
recovering the supernatant, which was used for protein and enzyme
analyses.
Protein assay.
Total cellular protein was assayed
spectrophotometrically (Hewlett-Packard model 8453) by monitoring the
shift of maximum absorbance from 465 to 595 nm as the Brilliant blue
G-250 dye bound to protein (Bio-Rad) (4).
Enzyme assays.
Catalase, peroxidase, and superoxide
dismutase (SOD) enzymes were assayed spectrophotometrically
(Hewlett-Packard model 8453) by the methods described in the
Worthington Enzyme Manual (48). The catalase
activity was assayed by monitoring the disappearance of hydrogen
peroxide at 240 nm. One unit of catalase activity was defined as the
decomposition of 1 µM H2O2 per min at 25°C and pH 7.0. The peroxidase activity assay was based on the absorbance increase at 510 nm resulting from the decomposition of hydrogen peroxide with 4-aminoantipyrine used as a hydrogen donor. One unit of
peroxidase activity resulted in the decomposition of 1 µM
H2O2 per min at 25°C and pH 7.0. The SOD
activity was assayed by monitoring the inhibition of the reduction
of nitroblue tetrazolium at 540 nm. One unit was defined as the amount
of enzyme causing half-maximal inhibition of nitroblue tetrazolium
reduction. The unit activities of the enzymes were normalized as
specific activities by using the total cellular protein assay.
Toxicity study.
Toxicity studies were performed by
enumerating the cells after incubation in 40 ml of medium (as described
above minus carbon and nitrogen), containing Fe(II),
H2O2, and cells at the concentrations given in
Table 1. Cultures were placed on a rotary
platform shaker at 30°C and 200 rpm for 60 min. Hydrogen peroxide was
added to the medium first, followed by cells that had been harvested
from the steady-state chemostat. The concentrations of harvested cells were determined by measuring the optical density at 600 nm (0.1 unit
108 cells/ml), and the medium was diluted accordingly
to obtain the desired initial cell populations. The experiments were
initiated by the addition of a previously prepared ferrous iron stock
solution. The ferrous iron stock solution (40 mM) was prepared in the
presence of excess chelating agent, i.e., 400 mM nitriloacetic acid
(NTA), and under anaerobic conditions to prevent autooxidation of the ferrous iron to ferric iron (13).
View this table:
[in this window]
[in a new window]
|
TABLE 1.
Experimental matrix for the investigation of response
surfaces describing the toxic effects of modified Fenton reactions
on X. flavus by measuring organism survival considering
the experimental variables of hydrogen peroxide, iron(II), and
cell population
|
|
Cell populations were enumerated at the end of the toxicity studies by
the spread plate technique with nutrient agar (
24).
Tenfold
serial dilutions prior to plate spreading were made in
the carbon- and
nitrogen-free growth medium. Such sample handling
eliminated the need
for pretreatment of cells since any adverse
effects of the sampled
media or carryover of the chemicals were
decreased substantially by
dilution.
Experimental design.
Toxicity experiments were based on a
central composite, rotatable design as outlined by Cochran and Cox
(12) to decrease the number of experiments while increasing
the statistical significance of the results. The three-level design,
shown in Table 1, included the initial cell population and
H2O2 and Fe(II)-chelate concentrations as
experimental variables. The percent cellular survival, based on spread
plate enumerations, was the response measured. The design contained
three blocks of experiments based on a second-order design: Block 1 was
a 23 factorial design that formed the first-order portion
of the design; block 2 was the "star" points that provided the
second-order portion of the design; and block 3 was defined as the
center of the experimental design, which allowed analysis of the error
of the measurements.
Response surface methodology is a technique used to demonstrate the
effects of independent variables on an experimental response.
The
method allows researchers to analyze the effects of multiple
variables
with a minimal number of experiments while keeping statistical
significance (
12) and has gained popularity as an effective
research tool. Hess et al. (
21) used the technique to
investigate
the effects of process variables on dissolved-oxygen
removal from
a water treatment technology, while Watts et al.
(
42) demonstrated
the effects of treatment variables on
remediation of hexachlorobenzene-contaminated
soils.
| |
RESULTS AND DISCUSSION |
Adaptation to H2O2 stress.
The purpose
of our research was to investigate the toxic effects of modified Fenton
reactions on bacteria, rather than the effects of hydrogen peroxide,
which is itself toxic to microorganisms. Conversely, it has been
well established that microorganisms can be acclimated to high
concentrations of H2O2 by pretreatment with sublethal concentrations (15, 22, 46). Therefore, to
eliminate the toxic effects of H2O2, we
initially acclimated cells to high concentrations of
H2O2.
The effect of H
2O
2 acclimation was investigated
by comparing the survival rates of acclimated and nonacclimated cells
in the
medium used for the toxicity study after 1 h of incubation
with
various concentrations of H
2O
2. The
H
2O
2-acclimated cells showed
high survival
rates (>80%), while nonacclimated cells showed high
susceptibility to
H
2O
2 stress (Fig.
1), with an overall decline
in cell
number of more than 90%. During this study, it was observed
that the
time required to produce replicates from the same dilution
significantly decreased the number of colonies formed for the
nonacclimated cells. This situation, while resulting in a high
standard
deviation from the mean for final cell populations, affected
neither
the percent survival rate nor its standard deviation.
A similar
phenomenon was not encountered for the acclimated strain.
View larger version (13K):
[in this window]
[in a new window]
|
FIG. 1.
Comparison of survival rates of
H2O2-acclimated ( ) and nonacclimated ( )
cells of X. flavus for various H2O2
concentrations after 1 h of incubation. Error bars represent
standard errors of measurements.
|
|
We also investigated the effect of H
2O
2
acclimation on cellular enzyme activity. Although there were a
number of possible
enzymes that might be involved in the
detoxification of H
2O
2,
we selected the three
most likely enzymes: catalase, SOD, and
peroxidase. The results,
summarized in Table
2, show the
effect
of H
2O
2 acclimation on these three
enzymes. No measurable peroxidase
activity was observed in either the
H
2O
2-acclimated or nonacclimated
cells.
However, adaptation by feeding the chemostat with medium
containing 300 mg of H
2O
2 per liter resulted in an
approximately
23-fold increase in the specific activity of catalase,
whereas
the specific activity of SOD increased less than 2-fold. Izawa
et al. (
22) obtained similar results for catalase induction
due to H
2O
2 acclimation.
The large increase in the specific activity of catalase demonstrates
its role in H
2O
2 adaptation. The elevated
survival rate
of H
2O
2-acclimated cells in the
presence of H
2O
2 is evidence of
successful
acclimation to H
2O
2, a necessary step for the
following
experiments.
Toxic effects of modified Fenton reactions.
The toxic effects
of Fenton reactions on microorganisms results from
H2O2, ·OH, and other reactive
oxygen species. Because our goal was to investigate the toxic effects
of only radical species generated via modified Fenton reactions,
H2O2-acclimated cells were used throughout the
experiments. The toxic effects were investigated as a function of
initial cell population and both reaction elements, i.e.,
H2O2 and Fe(II). Experiments were based on a
central composite, rotatable design (12), chosen to minimize
the number of experiments while keeping a high degree of statistical
significance in the results. The experimental design, with all
calculated H2O2 and Fe(II) concentrations and
cell population values, together with resulting cellular survival (as a
percentage), is shown in Table 1.
Analyses of the experimental results, by a second-order equation,
(
12,
14) resulted in the following quadratic equation
of the
response surface for the percent cellular survival with
the three
variables of H
2O
2, Fe(II), and initial cell
population:
S = 122.6892 (±15.0632)
0.251 ×
H (±0.1033)
14.7437 ×
F
(±3.0993)
5.1721 ×
C (±1.1721) + 0.0006 ×
H2 (±0.0003) + 1.1315 ×
F2 (±0.2961), where
S is percent
cellular survival,
H is H
2O
2
concentration
(milligrams per liter),
F is Fe(II)
concentration (millimolar),
and
C is the initial cell
population (log
10 per milliliter). Numbers
in
parentheses are uncertainties (95% confidence level) associated
with
each variable in the model. The terms that were determined
by a
t test (
14) as being insignificant at a
P of 0.10 were
excluded from the equation. The above
equation was given with
four significant figures because of the drastic
effect on the
model due to the
H2 term. It
should be noted that experiment 7, block 1 (Table
1),
was rerun due to
an experimental error, yet a sensitivity analysis
on the point showed
that the results of experiment 7 had an insignificant
effect on the
overall model equation (data not shown). Finally,
it should be
remembered that the validity of the model is limited
to use
within the tested boundaries.
The statistical analysis of variance (ANOVA) of the data is shown in
Table
3 (
14). Regression of
the experimental data
values against estimated values from the model
was performed and
is shown in Fig.
2. The
corresponding coefficient of correlation
(
R2)
was 0.76, an acceptable value when considering the errors inherent
in
enumeration of microbial populations. Furthermore, based on
ANOVA of
the results (Fig.
2; Table
3), the second-order response
equation
appeared to adequately fit the data: comparison of the
mean squares for
lack of fit and error terms (Table
3) showed
values of approximately
equal size, indicating adequate model
fit (
12).
View larger version (12K):
[in this window]
[in a new window]
|
FIG. 2.
Regression plot of observed data values against
estimated values from the second-order response surface model.
|
|
The utility of any response surface model for describing a biological
system comes from its ability to accurately predict
the response. Our
proposed model was shown to accurately predict
observed values from the
experimental design, based on the coefficient
of determination
statistic. The model also appeared valid in describing
observed values
from the separate experiment in Fig.
1. When these
data were added to
those in Fig.
2, the plot of observed survival
against predicted
survival, they fit within the overall experimental
error and actually
increased the coefficient of determination
to 0.83 from 0.76 (data not
shown).
Response surface plots of the second-order model, generated by
keeping one of the variables constant at the center point of
the
experimental design, are shown in Fig.
3,
along with discrete
data values. As can be seen in the plots, there was
a decline
in cellular survival with increasing hydrogen peroxide and
Fe(II)
concentrations. This was to be expected, since the extent of
formation
of products of Fenton reactions was dependent on the
concentrations
of both species (
13). A further observation
was the apparent
anomaly of lowered bacterial survival with increasing
initial
cell number for similar peroxide concentrations, as seen in
Fig.
3A and C. This, too, can be explained if the cell number is
thought
of as another reactive species with Fenton reaction products,
and then high cell concentrations lead to high reaction rates,
or
cellular death, and low survival percentages. If coexisting
abiotic-biotic processes are to be used for treatment purposes,
a
significant number of cells must be present to effect a useful
kinetic
degradation rate. Even though the experiment with an initial
cell count
of 10
7/ml (block 2, experiment 6 [Table
1]) showed only
2% survival,
the remaining 2 × 10
5 cells/ml may be
enough for a successful abiotic-biotic remediation
scheme.
View larger version (15K):
[in this window]
[in a new window]
|
FIG. 3.
Response surface plots for percent microbial survival
(contour lines) under different experimental conditions. (A)
Ferrous iron concentration of 5 mM. (B) Initial cell number
of 104.5 cells/ml. (C) Hydrogen peroxide concentration of
150 mg/liter. Symbols: *, observed data;  , mean value for center
point data.
|
|
The results (Fig.
3B and C) showed that the addition of Fe(II)
decreased cellular survival rates. Addition of ferrous iron
to
the reaction mixture resulted in the generation of various
oxygen
radical species, especially hydroxyl radicals, which were
more reactive
than H
2O
2. The first-order reaction rates of
catalase
with H
2O
2 and hydroxyl radicals are
1.7 × 10
7 and >1 × 10
10
M
1 s
1, respectively (
19).
Although the primary detoxification enzyme
involved in both cases
was catalase (
47), the increased toxicity
seen in
our experiments may be explained by the increased reactivity
of
products of Fenton reactions.
Data from Fig.
3A and B show that the elevated hydrogen peroxide
concentrations resulted in higher survival rates. This phenomenon
may
be attributed to (i) experimental errors (the increases in
survival
rates are within the experimental error range) or (ii)
the formation of
other reactive oxygen species, in the presence
of excess hydrogen
peroxide, which are possibly less toxic or
can be detoxified by
enzymatic means other than by catalase. Pignatello
and Sun
(
34) showed that ferric iron catalyzed excess hydrogen
peroxide, yielding water, oxygen and hydroperoxyl radical (equations
3 to 6). Halliwell and Gutteridge (
19) reported another
possible
reaction between ferric iron and hydrogen peroxide, yielding
superoxide
radical (equation 7), readily detoxified in microorganisms
by
SOD.
|
(3)
|
|
(4)
|
|
(5)
|
|
(6)
|
|
(7)
|
Another observation from this study concerned the possible
toxicity of Fe(II)-NTA. Figure
3 shows that there was still
significant
toxicity in the absence of H
2O
2 and
that it was attributable to
either (i) in vivo generation of
H
2O
2 during the reduction of
molecular
oxygen (
16,
33), with concomitant generation of
hydroxyl or
other oxygen radicals, or (ii) high concentrations
of NTA. Therefore,
we further investigated the possible contribution
of NTA to the
observed results of the study of the toxic effects
of the products of
the Fenton reaction. To this extent, cells
were exposed to NTA for
1 h under the same conditions at which
the toxic effects of
the Fenton reaction were investigated. The
results (Fig.
4) showed that high NTA concentrations
may have
contributed up to 25% of the overall toxic effects
of Fenton reactions
when the Fe(II) concentration was 10 mM.
View larger version (11K):
[in this window]
[in a new window]
|
FIG. 4.
Effect of various concentrations of NTA on the survival
rates of X. flavus after 1 h of exposure. Error
bars represent standard errors of measurements.
|
|
In conclusion, the results of this research showed that there are toxic
effects of Fenton reactions on peroxide-acclimated
bacteria that are
exclusive of the toxicity of any of the individual
reactants. These
toxic effects was attributed in this study to
the production of
hydroxyl and other oxygen radicals. The cellular
protective
mechanism against peroxide and oxygen radical toxicity
was shown
to be an increase in catalase activity. Finally, a model
describing toxicity, as related to cellular survival, was developed
on
the basis of concentrations of Fenton reaction species and
initial cell
number. The model was shown to be a statistically
significant
description of the process and could be used to predict
the survival of
the bacteria within the ranges of variables used.
The results of this
research indicate that coexisting abiotic-biotic
processes may be
possible, in part, because of toxicity avoidance
mechanisms in the
bacteria. Although applications of single bacterial
strains are
limited in practice, a single-strain system was selected
based on
the analytical simplifications to clearly elucidate the
interactions
between chemical and biological processes. Knowing
how such chemical
and biological processes interact will aid in
subsequent development
and optimization of coexisting abiotic-biotic
processes.
| |
ACKNOWLEDGMENTS |
This research was supported by National Science Foundation grant
9613258 from a joint program of the National Science Foundation and
United States Environmental Protection Agency.
We thank A. Paszcynski for help with experimental procedures and
A. L. Teel for thoughtful discussion.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Center for
Hazardous Waste Remediation Research, University of Idaho, Moscow, ID
83844-0904. Phone: (208) 885-7461. Fax: (208) 885-7908. E-mail:
tfhess{at}uidaho.edu.
Publication 98303 of the Idaho Agricultural Experiment Station.
| |
REFERENCES |
| 1.
|
Anagiotou, C.,
A. Papadopoulus, and M. Loizidou.
1993.
Leachate treatment by chemical and biological oxidation.
J. Environ. Sci. Health Part A
28:21-35.
|
| 2.
|
Ananthaswamy, H. N., and A. Eisenstark.
1977.
Repair of hydrogen peroxide-induced single-strand breaks in Escherichia coli deoxyribonucleic acid.
J. Bacteriol.
130:187-191[Abstract/Free Full Text].
|
| 3.
| Andrews, T., D. Zervas, and R. S. Greenberg.
1997. Oxidizing agent can finish cleanup where other systems taper
off. Soil Groundwater Cleanup 1997 (July):39-42.
|
| 4.
| Bio-Rad Laboratories. Bio-Rad protein assay.
Bio-Rad Laboratories, Richmond, Calif.
|
| 5.
|
Bowers, A. R.,
S. H. Cho, and A. Singh.
1991.
Chemical oxidation of aromatic compounds: comparison of H2O2, KMnO4 and O3 for toxicity reduction and improvements, p. 11-25.
In
W. W. Eckenfelder, A. R. Bowers, and J. A. Roth (ed.), Biodegradability in chemical oxidation technologies for the nineties. Technomic Publishing Company, Lancaster, Pa.
|
| 6.
|
Bowers, A. R.,
P. Gaddipati,
W. W. Eckenfelder, and R. M. Monsen.
1989.
Treatment of toxic or refractory wastewaters with hydrogen peroxide.
Water Sci. Technol.
21:477-486.
|
| 7.
|
Brot, N.,
L. Weissbach,
J. Wearth, and H. Weissnach.
1981.
Enzymatic reduction of protein-bound methionine sulfoxide.
Proc. Natl. Acad. Sci. USA
78:2155-2158[Abstract/Free Full Text].
|
| 8.
|
Brown, R. A., and R. D. Norris.
1994.
The evolution of a technology: hydrogen peroxide in in-situ bioremediation, p. 148-162.
In
R. E. Hinchee, B. C. Alleman, R. E. Hoeppel, and R. N. Miller (ed.), Hydrocarbon bioremediation. Lewis Publishers, Boca Raton, Fla.
|
| 9.
|
Brown, R. A.,
R. D. Norris, and R. L. Raymond.
1994.
Oxygen transport in contaminated aquifers with hydrogen peroxide, p. 441-450.
In
Proceedings of the NWWA/API Conference on Petroleum Hydrocarbons and Organic Chemicals in Groundwater. Prevention, detection and restoration. National Water Well Association, Worthington, Ohio.
|
| 10.
|
Buchmeier, N. A.,
S. J. Libby,
Y. Xu,
P. C. Loewen,
J. Switala, and D. G. Guiney.
1995.
DNA repair is more important than catalase for Salmonella virulence in mice.
J. Clin. Invest.
95:1047-1053.
|
| 11.
|
Carberry, J. B., and T. M. Benzing.
1991.
Peroxide pre-oxidation of recalcitrant toxic waste to enhance biodegradation.
Water Sci. Technol.
23:367-376.
|
| 12.
|
Cochran, W. G., and G. M. Cox.
1992.
Experimental designs, 2nd ed.
John Wiley & Sons, Inc., New York, N.Y.
|
| 13.
|
Cohen, G.
1987.
The fenton reaction, p. 55-64.
In
R. A. Greenwald (ed.), CRC handbook of methods for oxygen radical research. CRC Press, Inc., Boca Raton, Fla.
|
| 14.
|
Diamond, W. J.
1989.
Practical experimental designs for engineers and scientists, 2nd ed.
Van Nostrand Reinhold, New York, N.Y.
|
| 15.
|
Fiorenza, S., and C. H. Ward.
1997.
Microbial adaptation to hydrogen peroxide and biodegradation of aromatic hydrocarbons.
J. Ind. Microbiol. Biotechnol.
18:140-151[Medline].
|
| 16.
|
Fridovich, I.
1978.
The biology of oxygen radicals.
Science
201:875-880[Abstract/Free Full Text].
|
| 17.
|
Gherna, R.,
P. Pienta, and R. Cote.
1992.
Catalogue of bacteria and phages, 18th ed.
American Type Culture Collection, Rockville, Md.
|
| 18.
|
Haber, F., and J. Weiss.
1934.
The catalytic decomposition of hydrogen peroxide by iron salts.
Proc. R. Soc. London
147A:332-351[Free Full Text].
|
| 19.
|
Halliwell, B., and J. M. C. Gutteridge.
1985.
Free radicals in biology and medicine
Clarendon Press, Oxford, United Kingdom.
|
| 20.
|
Hassan, H. M., and I. Fridovich.
1978.
Regulation of the synthesis of catalase and peroxidase in Escherichia coli.
J. Biol. Chem.
253:6445-6450[Free Full Text].
|
| 21.
|
Hess, T. F.,
J. D. Chwirka, and A. M. Noble.
1996.
Use of response surface modeling in pilot testing for design.
Environ. Technol.
17:1205-1214.
|
| 22.
|
Izawa, S.,
Y. Inoue, and A. Kimura.
1996.
Importance of catalase in the adaptive response to hydrogen peroxide: analysis of acatalasaemic Saccharomyces cerevisiae.
J. Biochem.
320:61-67.
|
| 23.
|
Jamieson, D. J.,
S. L. Rivers, and D. W. S. Stephen.
1994.
Analysis of Saccharomyces cerevisiae proteins induced by peroxide and superoxide stress.
Microbiology
140:3277-3283[Abstract/Free Full Text].
|
| 24.
|
Koch, A.
1994.
Growth measurement, p. 248-277.
In
P. Gerhardt, R. G. E. Murray, W. A. Wood, and N. R. Krieg (ed.), Methods for general and molecular bacteriology. American Society for Microbiology, Washington, D.C.
|
| 25.
|
Koyama, O.,
Y. Kamagata, and K. Nakamura.
1994.
Degradation of chlorinated aromatics by Fenton oxidation and methanogenic digester sludge.
Water Res.
28:885-899.
|
| 26.
|
Lee, S. H., and J. B. Carberry.
1992.
Biodegradation of PCP enhanced by chemical oxidation pretreatment.
Water Environ. Res.
64:682-690.
|
| 27.
|
Leung, S. W.,
R. J. Watts, and G. C. Miller.
1992.
Degradation of perchloroethylene by Fenton's reagent: speciation and pathway.
J. Environ. Qual.
21:377-381.
[Abstract/Free Full Text] |
| 28.
|
Li, Z. M.,
P. J. Shea, and S. D. Comfort.
1997.
Fenton oxidation of 2,4,6-trinitrotoluene in contaminated soil slurries.
Environ. Eng. Sci.
14:55-66.
|
| 29.
|
Loewen, P. C.
1984.
Isolation of catalase-deficient Escherichia coli mutants and genetic mapping of katE, a locus that affects catalase activity.
J. Bacteriol.
157:622-626[Abstract/Free Full Text].
|
| 30.
|
Mead, J. F.
1976.
Free radical mechanisms of lipid damage and consequences for cellular membranes, p. 51-68.
In
W. A. Pryor (ed.), Free radicals in biology. Academic Press, Inc., New York, N.Y.
|
| 31.
|
Murphy, A. P.,
W. J. Boegli,
M. K. Price, and C. D. Moody.
1989.
A Fenton-like reaction to neutralize formaldehyde waste solutions.
Environ. Sci. Technol.
23:166-169.
|
| 32.
|
Norris, R. D., and K. D. Dowd.
1994.
In situ bioremediation of petroleum hydrocarbon-contaminated soil and groundwater in a low permeability aquifer, p. 457-474.
In
P. E. Flathman, D. E. Jerger, and J. H. Exner (ed.), Bioremediation: field experience. Lewis Publishers, Boca Raton, Fla.
|
| 33.
|
Pardieck, D. L.,
E. J. Bouwer, and A. T. Stone.
1992.
Hydrogen peroxide use to increase oxidant capacity for in-situ bioremediation of contaminated soils and aquifers: a review.
J. Contam. Hydrol.
9:221-242.
|
| 34.
|
Pignatello, J. J., and Y. Sun.
1993.
Photo-assisted mineralization of herbicide wastes by ferric ion catalyzed hydrogen peroxide, p. 77-84.
In
D. W. Tedder, and F. G. Pohland (ed.), Emerging technologies in hazardous waste management. III. American Chemical Society, Washington, D.C.
|
| 35.
|
Ravikumar, J. X., and M. D. Gurol.
1991.
Effectiveness of chemical oxidation to enhance the biodegradation of pentachlorophenol in soils: a laboratory study, p. 211-221.
In
R. D. Neufeld, and L. W. Casson (ed.), Hazardous and industrial wastes. Proceedings of the Twenty-Third Mid-Atlantic Industrial Waste Conference. Technomic Publishing Company, Lancaster, Pa.
|
| 36.
|
Sak, B. D.,
A. Eisenstark, and D. Touati.
1989.
Exonuclease III and the catalase hydroperoxidase II in Escherichia coli are both regulated by the katF gene product.
Proc. Natl. Acad. Sci. USA
86:3271-3275[Abstract/Free Full Text].
|
| 37.
|
Sato, C.,
S. W. Leung,
H. Bell,
W. A. Burkett, and R. J. Watts.
1993.
Decomposition of perchloroehylene and polychlorinated biphenyls with Fenton's reagent, p. 343-356.
In
D. W. Tedder, and F. G. Pohland (ed.), Emerging technologies in hazardous waste management. III. American Chemical Society, Washington, D.C.
|
| 38.
|
Scott, J. P., and D. F. Ollis.
1995.
Integration of chemical and biological oxidation processes for water treatment: review and recommendations.
Environ. Prog.
14:88-103.
|
| 39.
|
Spain, J. C.,
J. D. Milligan,
D. C. Downey, and J. K. Slaughter.
1989.
Excessive bacterial decomposition of H2O2 during enhanced biodegradation.
Ground Water
27:163-167.
|
| 40.
|
Storz, G.,
M. F. Christman,
H. Sies, and B. N. Ames.
1987.
Spontaneous mutagenesis and oxidative damage to DNA in Salmonela typhimurium.
Proc. Natl. Acad. Sci. USA
84:8917-8921[Abstract/Free Full Text].
|
| 41.
|
Tyre, B. W.,
R. J. Watts, and G. C. Miller.
1991.
Treatment of four biorefractory contaminants in soils using catalyzed hydrogen peroxide.
J. Environ. Qual.
20:832-838.
[Abstract/Free Full Text] |
| 42.
|
Watts, R. J.,
S. Kong,
M. Dipre, and W. T. Barnes.
1994.
Oxidation of sorbed hexachlorobenzene in soils using catalyzed hydrogen peroxide.
J. Hazard. Mater.
39:33-47.
|
| 43.
|
Watts, R. J.,
M. D. Udell, and R. M. Monsen.
1993.
Use of iron minerals in optimizing the peroxide treatment of contaminates soils.
Water Environ. Res.
65:839-844.
|
| 44.
|
Watts, R. J., and S. E. Dilly.
1996.
Evaluation of iron catalysts for the Fenton-like remediation of diesel-contaminated soils.
J. Hazard. Mater.
51:209-224.
|
| 45.
|
Werner-Washburne, M.,
E. Braun,
G. C. Johnston, and R. A. Singer.
1993.
Stationary phase in the yeast Saccharomyces cerevisiae.
Microbiol. Rev.
57:383-401[Abstract/Free Full Text].
|
| 46.
|
Winquist, L.,
U. Rannug,
A. Rannug, and C. Ramel.
1984.
Protection from toxic and mutagenic effects of H2O2 by catalase induction in Salmonella typhimurium.
Mutat. Res.
141:145-147[Medline].
|
| 47.
|
Wolff, S. P.,
A. Garner, and R. T. Dean.
1986.
Free radicals, lipids and protein degradation.
Trends Biochem. Sci.
11:27-31.
|
| 48.
|
Worthington, V.
1993.
Worthington enzyme manual: enzymes and related biochemicals
Worthington Biochemical Corp., Freehold, N.J.
|
Applied and Environmental Microbiology, October 1998, p. 3759-3764, Vol. 64, No. 10
0099-2240/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
This article has been cited by other articles:
-
Marchesi, J. R., Weightman, A. J.
(2003). Comparing the Dehalogenase Gene Pool in Cultivated {alpha}-Halocarboxylic Acid-Degrading Bacteria with the Environmental Metagene Pool. Appl. Environ. Microbiol.
69: 4375-4382
[Abstract]
[Full Text]
-
Büyüksönmez, F., Hess, T. F., Crawford, R. L., Paszczynski, A., Watts, R. J.
(1999). Optimization of Simultaneous Chemical and Biological Mineralization of Perchloroethylene. Appl. Environ. Microbiol.
65: 2784-2788
[Abstract]
[Full Text]
Top
Abstract
Introduction
