Relationship of Protozoan Biomass To Phosphate and Nitrate Removal From Activated Sludge Mixed Liquor

Biotechnology
Journal
DOI 10.1002/biot.200900135
Biotechnol. J. 2010, 5, 304313
Research Article
Relationship of protozoan biomass to phosphate and

nitrate removal from activated sludge mixed liquor
Oghenerobor B. Akpor and Maggy N. B. Momba
Department of Environmental, Water and Earth Sciences, Tshwane University of Technology, Pretoria, South Africa
The relationship between protozoan biomass concentration and phosphate and nitrate removal
was investigated in mixed liquor using three different carbon sources as supplements. The study
was carried out using three respective initial biomass concentrations in a shaking flask environment. Samples were taken every 24 h to determine phosphate, nitrate, dissolved oxygen and chemical oxygen demand. The results revealed a direct relationship between decreases in nutrient concentrations and increases in cell densities of the isolates. Between 24 and 96 h, the increases in
the protozoan density corresponded to a phosphate decreases from initial ranges of
55.4257.36 mg/L, 50.2751.17 mg/L and 50.0150.83 mg/L to final ranges of 2.4611.90 mg/L,
0.6111.80 mg/L and 1.2913.89 mg/L, in the presence of Aspidisca, Trachelophyllum and
Peranema, respectively. Nitrate concentrations were observed to decrease from initial ranges of
23.8425.90 mg/L, 23.9425.84 mg/L and 26.1226.54 mg/L to final ranges of 0.116.32 mg/L,
0.165.60 mg/L and 0.249.04 mg/L, respectively. The study had revealed that an increase in cell
density of the test isolates produces a corresponding increase in phosphate and nitrate removal.
Received 21 June 2009

Revised 11 September 2009
Accepted 29 September 2009
Keywords: Biomass relation Protozoa Nutrient removal
1 Introduction
Wastewater may contain high levels of phosphate
and nitrate, which when excessively released to the
environment can lead to eutrophication, which is a
major drawback of activated sludge production. Although phosphate itself does not have notable adverse health effects, phosphate levels greater than
1.0 mg/L may interfere with coagulation in water
treatment plants [1]. On the other hand, nitrogen is
important in wastewater management because it
can have many effects on the environment. The
presence of nitrogen in wastewater discharge above
Correspondence: Professor Maggy N. B. Momba, Department of

Environmental, Water and Earth Sciences, Tshwane University of
Technology, P/Bag X680, Pretoria 0001, South Africa
E-mail: mombamnb@tut.ac.za
Fax: +27-12-382-6254
Abbreviations: COD, chemical oxygen demand; DO, dissolved oxygen
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2009 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim
the required limit of 10 mg/L is undesirable because

of ecological and public health impacts [2, 3].
Since the assurance of water quality has become
an integral part of environmental management today, wastewater treatment is one of the strategies
for water quality management [4]. In the past, nutrient removal from wastewater treatment was
achieved through chemical addition but since
chemical precipitation increases the volume of
sludge produced and often results in sludge with
poor settling and dewatering characteristics and a
depression of the pH, biological treatment is now
advocated [3, 5].
Because large amounts of waste products are
passed through our sewage treatment systems on a
daily basis, biological nutrient removal is critical for
the preservation of our lakes, streams and other receiving water bodies [6]. Although biological nutrient removal in wastewater systems have been attributed mainly to bacteria, some studies have reported the efficiency of protozoa species in the
mineralization of nutrients like carbon, nitrogen
Biotechnol. J. 2010, 5, 304313
and phosphorus in terrestrial and aquatic environments [710].A few studies have also reported their
role in phosphate and nitrate removal from activated sludge mixed liquor [11, 12].
Previous investigations have shown the role of
carbon sources in nutrient removal from wastewater [1214]. In the past, the relationship of bacterial biomass with phosphate removal had been
reported [15, 16]. Although the relationship of pro-
www.biotechnology-journal.com
tozoan biomass to nutrient removal in activated

sludge mixed liquor has been investigated in the
presence of acetate as carbon source [17], detailed
reports on the relationship between phosphate and
nitrate removal by protozoan biomass in activated
sludge mixed liquor in the presence of carbon
sources other than acetate are lacking.This study is
therefore aimed at investigating this relationship in
the presence of acetate, glucose and sucrose as carbon sources in activated sludge mixed liquor.
Materials and methods
The present study was carried out between October

2007 and February 2008. Medium used for this
study was mixed liquor obtained from the anaerobic zone of the Daspoort wastewater treatment
plant in Pretoria, South Africa and was supplemented as described previously [1517].
Three protozoan isolates (Aspidisca sp., Trachelophyllum sp. and Peranema sp.), which have previously been screened for phosphate and nitrate removal efficiency [11, 12], were used for this study.
They were isolated from the aerobic zone of the
Daspoort wastewater treatment plant. The carbon
sources, sodium acetate, sucrose and glucose were
used for this investigation; these have previously
been ascertained to enhance nutrient removal from
mixed liquor in the presence of the protozoan isolates [12].
The densities of protozoan cells in mixed liquor
were estimated using the direct microscopy technique as described elsewhere [17]. In this study,
three different initial biomass concentrations (101,
102 and 103 cells/mL) of the test protozoan isolates
were used.
The design of the study was as described previously [17]. Standard methods [18] were used for the
determination of total phosphate, nitrate-nitrogen
and chemical oxygen demand (COD), using the
ascorbic acid, salicylate and close-reflux methods,
respectively. Dissolved oxygen (DO) was determined using a DO meter. All experimental setups
were conducted in triplicate.
Results
3.1 Nutrient removal and growth of Aspidisca

in mixed liquor
Figure 1. Relationship between nutrient (phosphate and nitrate) removal

and growth of Aspidisca sp. in the presence of acetate as carbon source at
the different initial biomass concentration.
As shown in Fig. 1, in the presence of acetate as

carbon source, there was a relationship between
the decrease in phosphate or nitrate content and
the growth of Aspidisca. For the first 24 h, no re-
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markable removal of phosphate or nitrate was

noted, and there was no specific increase in
Aspidisca density. A drastic decrease in phosphate
and nitrate contents occurred with a progressive
increase in Aspidisca density. This trend was
observed at all initial biomass concentrations. At
the end of 96 h of incubation, the population of
Aspidisca increased from 101 to 2.5 102 cells/mL,

and growth of Aspidisca sp. in presence of the glucose as carbon source at
different initial biomass concentration.
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from 102 to 5.4 103 cells/mL and from 103 to

5.8 104 cells/mL. Also, the phosphate concentrations decreased from 56.63 to 9.46 mg/L, from 55.92
to 5.43 mg/L and from 55.61 to 2.46 mg/L, while initial biomass concentrations of 101, 102 and 103
cells/mL progressively increased in number
(Fig. 1). Similarly, nitrate concentrations decreased
from 23.83 to 3.29 mg/L, from 23.88 to 0.33 mg/L
and from 24.02 to 0.26 mg/L, as the population the
initial biomass concentrations of Aspidisca increased (Fig. 1).
In the presence of glucose as carbon source, the
growth of Aspidisca was observed to be directly related to the decrease in phosphate and nitrate concentration. At initial biomass concentrations of 101
and 102 cells/mL only slight decreases in phosphate and nitrate concentrations were noted for
the first 24 h, and there was no remarkable increase
in the density of Aspidisca (Fig. 2). As the population of Aspidisca increased progressively with time,
corresponding decreases in phosphate and nitrate
contents were observed. After 96 h of incubation,
the population of Aspidisca had increased from 101
to 3.0 102 cells/mL, from 102 to 5.4 103 cells/mL
and from 103 to 3.4 104 cells/mL (Fig. 2). Between
24 and 96 h of incubation, the concentrations of
phosphate decreased from 50.79 to 10.54 mg/L,
from 50.66 to 5.14 mg/L and from 50.27 to
2.07 mg/L, as the initial biomass concentrations of
Aspidisca increased progressively (Fig. 2). In addition, nitrate concentrations after 96-h incubation
decreased from 25.76 to 5.23 mg/L, 25.84 to
1.58 mg/L and from 25.73 to 0.16 mg/L, with progressive increases in the population of Aspidisca.
The decreases in phosphate and nitrate concentrations with corresponding increase in Aspidisca
density were irrespective of initial biomass concentration (Fig. 2).
When sucrose was used as carbon source, there
was also a direct relationship between the growth
of Aspidisca and the decrease in phosphate and nitrate contents.Within the first 24 h, only a slight increase in Aspidisca density was observed, with no
remarkable decrease in phosphate and nitrate concentrations. Remarkable decreases in phosphate
and nitrate concentrations were only observed after 24 h, when a drastic increase in cell density
occurred (Fig. 3). Between 24 and 96 h the cell
density of Aspidisca increased from 101 to
2.4 102 cells/mL, 102 to 5.6 103 cells/mL and from
103 to 3.6 104 cells/mL.These increases in biomass
corresponded to phosphate decrease from 50.83 to
9.83 mg/L, from 50.61 to 5.33 mg/L and from 50.57
to 1.81 mg/L (Fig. 3). Similarly, nitrate concentrations decreased from 26.43 to 9.04 mg/L, from 26.12
to 1.16 mg/L and from 26.21 to 0.57 mg/L (Fig. 3).
Biotechnol. J. 2010, 5, 304313
3.2 Nutrient removal and growth of

Trachelophyllum in mixed liquor
In the presence of acetate as carbon source, Trachelophyllum growth showed a direct relationship
with the decrease in phosphate and nitrate con-

and growth of Aspidisca sp. in the presence of sucrose as carbon source at
tents. For the first 24 h, when no remarkable increase in Trachelophyllum density was noted, there
was no remarkable decrease in phosphate concentrations at initial biomass concentrations of 101 and
102 cells/mL. At all initial biomass concentrations,
remarkable decreases in nitrate concentrations
were only observed after 24-h incubation when
there was specific increase in Trachelophyllum
density (Fig. 4). Between 24 and 96 h of incubation,
the Trachelophyllum population increased from 101
to 2.5 102 cells/mL, from 102 to 5.8 103 cells/mL
and from 103 to 5.7 104 cells/mL (Fig. 4). Corresponding phosphate concentrations decreased
and from 55.56 to 4.30 mg/L, respectively (Fig. 4).
The nitrate concentrations decreased after 96-h incubation from 25.21 to 6.32 mg/L, from 22.26 to
3.38 mg/L and from 24.07 to 0.13 mg/L, respectively, which corresponded to the increase in Trachelophyllum biomasses as noted above (Fig. 4).
As observed in the presence of acetate, the
growth of Trachelophyllum in the presence of glucose as carbon source was also observed to have a
direct relationship with phosphate and nitrate decrease. At initial biomass concentrations of 101 and
102 cells/mL, remarkable decreases in phosphate
and nitrate concentrations were only observed after the first 24 h, when specific increases in Trachelophyllum density were noted (Fig. 5). A progressive growth in the population of Trachelophyllum
resulted in biomass increases from 101 to 2.1 102
cells/mL, from 102 to 5.2 103 cells/mL and from 103
to 5.4 104 cells/mL. This biomass increase between 24 and 96 h resulted in phosphate concentrations decrease from 50.53 to 7.31 mg/L, from
50.66 to 2.69 mg/L and from 50.27 to 0.61 mg/L, respectively (Fig. 5). Nitrate concentrations also decreased, from 25.07 to 5.05 mg/L, from 24.02 to
1.46 mg/L and from 24.70 to 0.56 mg/L, respectively, for the different initial population numbers of
Trachelophyllum as noted above (Fig. 5).
The trend in growth of Trachelophyllum and nutrient removal in the presence of sucrose as carbon
source is shown in Fig. 6. A direct relationship was
observed between Trachelophyllum growth and
phosphate or nitrate removal. Between 24 and 96 h,
the population of Trachelophyllum increased from
101 to 2.1 102 cells/mL, from 102 to 5.4 103
cells/mL and from 103 to 5.4 104 cells/mL.The corresponding phosphate concentration decreases
were from 50.14 to 7.92 mg/L, from 50.27 to
5.81 mg/L and from 50.70 to 2.15 mg/L, respectively. The decreases in nitrate concentrations were
and from 26.32 to 0.36 mg/L, respectively (Fig. 6).
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and growth of Trachelophyllum sp. in the presence of acetate as carbon
source at different initial biomass concentration.
3.3 Nutrient removal and growth of Peranema

in mixed liquor
In the presence of acetate as a carbon source, there
was a direct relationship between the growth of
Peranema and the decrease in phosphate and nitrate concentration. At all initial biomass concentrations, no remarkable decrease in phosphate and
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Biotechnol. J. 2010, 5, 304313

and growth of Trachelophyllum sp. in the presence of glucose as carbon
nitrate concentration were observed during the

first 24 h, as there was no noticeable increase in
Peranema density (Fig. 7). Between 24 and 96 h, the
population of Peranema increased from 101 to
5.1 102 cells/mL from 102 to 3.1 103 cells/mL and
from 103 to 5.1 104 cells/mL. At these biomass increases, phosphate concentrations were observed
to decrease from 57.14 to 15.26 mg/L, from 56.76 to
11.70 mg/L and from 57.36 to 7.19 mg/L, respectively. Nitrate concentrations decreased from 25.56
Biotechnol. J. 2010, 5, 304313

and growth of Peranema sp. in presence of acetate as carbon source at
and growth of Trachelophyllum sp. in the presence of sucrose as carbon
to 3.25 mg/L, from 24.27 to 1.14 mg/L and from

25.90 to 0.11 mg/L, respectively (Fig. 7).
As shown in Fig. 8, in the presence of glucose as
a carbon source, a direct relationship was again ob-
served between the growth of Peranema and the

decrease in phosphate and nitrate content. No remarkable decrease in phosphate and nitrate concentration was observed for the first 24 h, and there
was no remarkable increase in Peranema density.
Noticeable decreases in phosphate and nitrate
contents were observed with progressive increase
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Biotechnol. J. 2010, 5, 304313
In the presence of sucrose as a carbon source, a

direct relationship was seen between the growth of
Peranema and the decrease in phosphate and nitrate content. During the first 24 h, as no specific increase in cell density was observed, there was no
noticeable decrease in phosphate and nitrate contents. Phosphate and nitrate concentrations were
observed to decrease progressively with increase
in Peranema density between 24 and 96 h (Fig. 9).
During this period, Peranema population increased
from 101 to 2.7 102 cells/mL, from 102 to 5.3 103
cells/mL and from 103 to 5.6 104 cells/mL. These
biomass concentrations triggered the decrease
in phosphate concentrations from 50.44 to
to 1.29 mg/L, respectively. Nitrate concentrations
decreased from 26.41 to 5.43 mg/L, from 26.44 to
1.24 mg/L and from 26.54 to 0.24 mg/L, respectively, for the three initial Peranema populations
(Fig. 9).
3.4 COD and DO concentrations in mixed liquor

As shown in Table 1, there was no observed reduction in COD concentrations of mixed liquor containing sodium acetate as carbon source. At the end
of the 96-h incubation, the COD concentration had
increased by over 50%, irrespective of the protozoan and initial biomass concentration used for inoculation. In mixed liquor containing glucose as
carbon source, after 96-h incubation, COD concentrations in mixed liquor decreased by 62.0985.33%,
65.5484.38% and 58.7772.16%, in liquor containing Aspidisca sp., Trachelophyllum sp. and Peranema sp., respectively (Table 1). In the presence of su-

and growth of Peranema sp. in the presence of glucose as carbon source
at different initial biomass concentration.
in Peranema density. Between 24 and 96 h, the population of Peranema increased from 101 to
2.7 102 cells/mL, from 102 to 5.3 103 cells/mL and
from 103 to 5.6 104 cells/mL. Phosphate concentrations also decreased from 50.87 to 11.80 mg/L,
from 50.40 to 8.32 mg/L and from 51.17 to
5.38 mg/L, respectively, for the three initial biomass
concentrations (Fig. 8). Similarly, nitrate concentrations were observed to decrease from 26.41 to
to 0.24 mg/L, respectively (Fig. 8).
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Table 1. Percentage COD increase/decrease in mixed liquor containing

the protozoan isolates after 96-h incubationa)
Aspidisca sp. Trachelophyllum sp. Peranema sp.

Acetate
101 cells/mL
102 cells/mL
103 cells/mL
Glucose
101 cells/mL
102 cells/mL
103 cells/mL
Sucrose
101 cells/mL
102 cells/mL
103 cells/mL
a)Values
50.58
56.99
52.40
53.79
52.23
55.59
60.18
67.91
54.43
62.09
75.82
85.33
65.54
80.90
84.38
58.77
71.41
72.16
64.16
61.57
73.35
61.12
65.13
79.79
49.39
52.57
75.56
represent % increase (bold) or decrease and are averages of

triplicate analyses. 101, 102 and 103 cells/mL represents the initial biomass of protozoa used for inoculation
Biotechnol. J. 2010, 5, 304313
Table 2. Percentage DO decrease in mixed liquor containing the

protozoan isolates after 96-h incubationa)
Aspidisca sp. Trachelophyllum sp. Peranema sp.

Acetate
101 cells/mL
102 cells/mL
103 cells/mL
Glucose
101 cells/mL
102 cells/mL
103 cells/mL
Sucrose
101 cells/mL
102 cells/mL
103 cells/mL
96.60
93.68
94.97
95.99
95.25
93.25
96.44
96.86
97.02
96.13
91.46
94.73
92.56
94.29
95.89
97.26
97.61
97.75
96.05
95.24
96.20
90.88
93.87
90.93
96.98
96.97
97.02
a)Values
represent % decrease and are the average of triplicate analysis

101, 102 and 103 cells/mL represents the initial biomass concentrations
used for inoculation.
As shown in Table 2, DO concentration in mixed

liquor did not follow any particular trend. After
96-h incubation, remarkable decreases in DO
concentrations were observed in mixed liquor inoculated with the protozoan isolates. This observation was irrespective of the isolates and initial
biomass concentrations used for inoculation. In all
mixed liquors containing the isolates, DO decreases
of over 90% were observed in presence of the respective carbon sources.

and growth rates of Peranema sp. in presence of sucrose as carbon source
at different initial biomass concentration.
crose as carbon source, COD concentrations were

also observed to decrease by 64.1673.35%,
61.1279.79% and 49.3975.56%, in mixed liquor
containing Aspidisca sp., Trachelophyllum sp. and
Peranema sp., respectively (Table 1). In the presence of glucose, in all the isolates, the lowest and
highest COD decrease were observed at initial biomass concentrations of 101 and 103 cells/mL, respectively.
Discussion
In the present study, a progressive increase in

growth was observed in all the three isolates
throughout the period of incubation.This trend was
irrespective of carbon source and initial biomass
concentration used as an inoculum. An increase in
protozoan growth triggered a corresponding increase in phosphate and nitrate removal. This
trend was also irrespective of carbon sources used.
A higher protozoan growth was seen with a higher
initial biomass concentration and this was common
in the three protozoan isolates. A similar observation has been reported by Sherr and co-workers
[19]. During their investigation on growth rate and
nitrogen mineralization by a flagellate, they observed a linear relationship between growth rate
and initial biomass. A progressive increase in the
population of protozoa with time has been reported by Petropoulos and Gilbride [20]. The present
investigation also confirms the study by Stauss and
Dodds [21], who also noted similar observations.
Some authors (when working with bacteria)
have, however, reported that excessive quantities of
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phosphates are only accumulated when growth is

arrested due to a lack of some nutrients [22]. In the
present study, nutrient (phosphate and nitrate) removal was negligible within the initial 24 h of incubation. This could be attributed to the probable adjustment of the protozoan cells prior to the onset of
cell division. A similar finding has been reported by
Cloete and Steyn [23]. Reports have shown that significant increases in nutrient removal can only be
observed after biomass has adjusted itself to the
new environments [24]. During the period of cell
adjustment, microbial cells are known to synthesize cellular components, enzymes and metabolic
intermediates needed for cell synthesis [25].
The present study also revealed a faster nutrient removal at higher initial biomass concentration, with a corresponding increase in protozoan
biomass concentration. This trend was irrespective
of the different carbon supplements. A similar observation was reported by Akpor and co-workers
[17] in a similar investigation in the presence of acetate as carbon supplement. The increase in nutrient removal at higher initial protozoan concentration could be due to a probable protozoan activity.
Studies have shown that there is a direct relationship between protozoan population and bioactivity
in activated sludge systems [24]. For effective phosphate and nitrate removal to take place in such systems, it has been reported that the returned sludge
must provide sufficient concentration of biomass in
the reactor [26].Working with bacteria, Momba and
Cloete [15] reported rapid phosphate uptake at
higher initial biomass concentration with a corresponding growth of cells. Although not observed in
the present study, Momba and Cloete [16] reported
that at low initial biomass concentration, there was
an initial phosphate release during active growth
and removal when cells reach the logarithmic or
stationary phase of growth. Phosphate release during active growth has been reported by some authors and this is associated with the competition
between nucleic acid synthesis and polyphosphate
for intracellular phosphate [27, 28]. Comeau and
co-workers [29] reported phosphate release in the
presence of acetate. The present study revealed no
phosphate release in the presence of any of the
carbon sources. This observation was irrespective
of the protozoan isolates and initial biomass concentration. Deinema [30] has attributed phosphate
release to carbon compounds other than acetate.
Although not observed in the present study,
Kern-Jespersen and Henze [31] have reported that
in wastewater treatment plants, biological phosphorus removal reduces the rate and capacity of
denitrification. This is because some of the organic
matter taken up by the phosphorus-accumulating
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organisms is not utilized for denitrification, but is

oxidized with oxygen.
The pattern of nutrient removal in this study
varied slightly among the protozoan isolates in the
presence of the different carbon supplements. This
was irrespective of initial biomass concentration.
Rates of nutrient removal, empirically described as
a simple hyperbolic function of ambient nutrient
concentrations, are not necessarily fixed for respective organisms, but variable depending on nutrient conditions where cells are growing. This
could suggest that nutrient removal/release is
maintained by regulatory mechanism [32].
The increase in COD in the presence of acetate
as carbon source in mixed liquor has been reported elsewhere [16, 17]. The present study showed a
decrease in COD in the presence of glucose or sucrose. The decrease in COD in the presence of glucose or sucrose was observed to depend on the initial biomass concentration. COD in mixed liquor
was observed to decrease mostly at an initial biomass concentration of 103 cells/mL.
The present study revealed a drastic decrease in
DO concentration of mixed liquor inoculated with
the protozoan isolates. A similar finding has been
reported by Akpor and co-workers [16, 17].This decrease in DO concentration in mixed liquor could
be attributed to the progressive increase in growth
of the isolates. It has been suggested that cell density increase during growth rate can lead to an increase in oxygen uptake [20].
In conclusion, the present study revealed a relationship between protozoan biomass and enhanced phosphate and nitrate removal and also an
increase in protozoan growth. The study revealed
that increases in population density of the test isolates produced corresponding decreases in the
concentrations of phosphate and nitrate, which are
the two major eutrophic nutrients in wastewaters.
At high initial biomass concentrations, phosphate
and nitrate removal by the protozoan isolates was
higher than at low initial biomass concentration.
An increase in protozoan growth produced a corresponding increase in nutrient removal and a decrease in DO concentration in mixed liquor. Growth
rates of the protozoan isolates in mixed liquor were
dependent on the initial biomass concentration
used as inoculum. Also, COD removal in mixed
liquor was dependent on carbon source and initial
biomass concentrations of the protozoan isolate in
mixed liquor. Overall, the study shows the need to
create an environment for the proliferation of the
test protozoan isolates in activated sludge systems,
which has not been clearly documented previously.
Biotechnol. J. 2010, 5, 304313
However, it is recommended that further work is

done using the findings of the present study for
scaling-up reactors and in situ. This will help in
evaluating the possibility of creating an environment for the proliferation of these protozoan fauna
in activated sludge systems.This will enhance their
use in full-scale treatment of wastewater influents
to obtain optimum effluent standards, thus helping
to enhance effective biological nutrient removal.
The authors wish to thank the National Research
Foundation (NRF) of South Africa and Tshwane
University of Technology for sponsoring this investigation.
The authors have declared no conflict of interest.
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