Causes and control of filamentous ...

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Biotechnology Advances 24 (2006) 115–127
www.elsevier.com/locate/biotechadv
Research review paper
Causes and control of filamentous growth in aerobic granular
sludge sequencing batch reactors
Yu Liu
*
, Qi-Shan Liu
Division of Environmental and Water Resources Engineering, School of Civil and Environmental Engineering,
Nanyang Technological University, 50 Nanyang Avenue, 639798 Singapore
Received 8 May 2005; accepted 9 August 2005
Available online 16 September 2005
Abstract
Poor long-term stability of aerobic granules developed in sequencing batch reactors (SBRs) remains a limitation to widespread
use of aerobic granulation in treating wastewater. Filamentous growth has been commonly reported in aerobic granular sludge
SBR. This review attempts to address the instability problem of aerobic granular sludge SBR from the perspective of filamentous
growth in the system. The possible causes of filamentous growth are identified, including long retention times of solids, low
substrate concentration in the liquid phase, high substrate gradient within the granule, dissolved oxygen deficiency in the granule,
nutrient deficiency inside granule, temperature shift and flow patterns. Because of cyclic operation of aerobic granular sludge SBR
and peculiarities of aerobic granules, various stresses can be present simultaneously and can result in progressive development of
filamentous growth in aerobic granular sludge SBR. Overgrowth of filamentous bacteria under stress conditions appears to be a
major cause of instability of aerobic granular sludge SBR. Specific recommendations are made for controlling filamentous growth.
D
2005 Elsevier Inc. All rights reserved.
Keywords: Aerobic granule; Sequencing batch reactor; Filamentous growth; Solids retention time; Kinetic selection
Contents
1. Introduction. ..................................................... 116
2. Main factors causing filamentous growth in the activated sludge process . . . ................... 116
2.1. Wastewater composition............................................ 116
2.2. Low substrate availability ........................................... 116
2.3. Dissolved oxygen concentration........................................ 116
2.4. Solids retention time (SRT) .......................................... 117
2.5. Nutrient deficiency .............................................. 117
2.6. Temperature .................................................. 117
3. Presence of filamentous bacteria in aerobic granules................................. 117
4. Outgrowth of filamentous bacteria in aerobic granular sludge SBR ......................... 117
5.
Possible causes of overgrowth of filamentous bacteria in aerobic granular sludge SBR ............... 119
* Corresponding author.
E-mail address: cyliu@ntu.edu.sg (Y. Liu).
0734-9750/$ - see front matter
D
2005 Elsevier Inc. All rights reserved.
doi:10.1016/j.biotechadv.2005.08.001
 116
Y. Liu, Q.-S. Liu / Biotechnology Advances 24 (2006) 115–127
5.1. Long SRT in aerobic granular sludge SBR .................................. 119
5.2. Substrate concentration and concentration gradients .............................. 120
5.3. Dissolved oxygen deficiency in aerobic granule ................................ 121
5.4. Nutrient deficiency in aerobic granule ..................................... 123
5.5. Temperature shift in aerobic granular sludge SBR............................... 123
5.6. Flow patterns in aerobic granular sludge SBR................................. 123
6. Propagation patterns of filamentous growth in aerobic granular sludge SBR . .................... 124
7. Control strategy for filamentous growth ....................................... 125
8. Concluding remarks.................................................. 125
References ......................................................... 126
1. Introduction
2. Main factors causing filamentous growth in the
activated sludge process
Aerobic granulation as a novel environmental bio-
technology has been extensively reported in sequenc-
ing batch reactors (SBR) and is tailored for treating a
wide variety of wastewaters
et al., 1999; Tay et al., 2001; Lin et al., 2003; Yang et
al., 2003; Arrojo et al., 2004; de Kreuk and van
Loosdrecht, 2004; McSwain et al., 2004; Schwarzen-
beck et al., 2004, 2005; Zhu et al., 2004
). Similar to
anaerobic granulation, aerobic granulation is believed
to be a microbial self-immobilization process that is
driven by selection pressures in SBR
2004; Qin et al., 2004; Hu et al., 2005; Liu et al.,
2005a
).
Compared to continuous microbial culture, the
unique feature of a SBR is its ability to be used in
a cyclic operation. A cycle may comprise filling,
aeration, settling, idling and sludge discharge. In stud-
ies of aerobic granulation in SBR, idling phase is
often not a part of the operation. The major technical
problem encountered in operating aerobic granular
sludge SBR relates to instability of aerobic granules.
Filamentous growth has been commonly observed in
aerobic granular sludge SBR (
2003; McSwain et al., 2004; Wang et al., 2004;
Schwarzenbeck et al., 2005
). Once filamentous growth
dominates the reactor, settleability of aerobic granules
becomes poor and subsequent biomass washout and
eventual disappearance of aerobic granules occurs.
Thus, filamentous growth leads to instability of aero-
bic granules. Instability of aerobic granules is a sig-
nificant bottleneck in applying this useful technology
for treating wastewater. Unfortunately, the factors that
encourage filamentous growth and its control are not
entirely clear. This review attempts to address the
following points: 1. the operating conditions that
might result in filamentous growth; 2. the major
causes of filamentous growth in aerobic granular
sludge SBR; and 3. strategies for controlling filamen-
tous growth.
Activated sludge processes experience sludge bulk-
ing problems because of overgrowth of filamentous
microorganisms. Many factors and their combinations
cause filamentous growth, as discussed in the following
sections.
2.1. Wastewater composition
It is believed that carbohydrates such as glucose,
citric acid and other readily biodegradable organics
favor the growth filamentous organisms (
1985; Bitton, 1999; Eckenfelder, 2000; Richard and
Collins, 2003
).
2.2. Low substrate availability
Filamentous microorganisms are slow-growing, i.e.
they have very low Monod affinity constant (K
s
) and
maximum specific growth rate (A
max
). According to
the kinetic selection theory, at low substrate concen-
tration, filamentous organisms would achieve a high
substrate removal rate compared with that of the floc-
forming bacteria that prevail at high substrate concen-
tration
. It is
reported that the growth of Microthrix parvicella and
the settling problems of the activated sludge resulting
from excessive growth of this filamentous species
always appear in modern municipal wastewater treat-
ment plants having BOD
5
-sludge loading rates of less
than or equal
to 0.1 kg kg
1
day
1
(
Kunst, 1998
).
2.3. Dissolved oxygen concentration
The growth of certain filamentous bacteria, such as
Sphaerotilus and Haliscomenobacter hydrossis, is fa-
vored by relatively low dissolved oxygen concentra-
tions
(
Bitton,
1999; Eckenfelder,
2000
). Other
Y. Liu, Q.-S. Liu / Biotechnology Advances 24 (2006) 115–127
117
filamentous bacteria, e.g. M. parvicella can grow over a
wide range of oxygen concentrations (
2005
). Deficiency of dissolved oxygen is believed to be
one of the major causes responsible for most filamen-
tous growth in activated sludge processes.
by the kinetic selection theory developed by
et al., (1973)
.
3. Presence of filamentous bacteria in aerobic
granules
2.4. Solids retention time (SRT)
Successful aerobic granulation has been reported in
SBRs only. Compared to continuous microbial culture,
SBR is a fill-and-draw process that is fully mixed
during the batch reaction step. The sequential steps of
aeration and clarification in a SBR occur in the same
tank (
. The operation of nearly
all aerobic granular sludge SBR systems comprises four
steps: feeding, aeration, settling and discharge. Com-
pared to operation of suspended sludge SBR
and Eddy, 2003
), there is no idling phase during the
operation of aerobic granular sludge SBR.
Evidence shows that filamentous bacteria dominate
glucose-fed aerobic granules, while non-filamentous
bacteria prevail in aerobic granules grown on acetate
(
)
). However,
even in aerobic granules grown on acetate, low-levels
or moderate-levels filamentous bacteria can still be
observed and they likely serve as a backbone that
strengthens the structure of aerobic granule (
.
Filamentous bacteria have also been found in phenol-
fed aerobic granules (
and in dairy effluent-
fed aerobic granules (
.
Because filamentous bacteria are slow-growing, a
long SRT favors their growth compared to growth of
floc forming microorganisms. For a typical filamentous
bacterium such as M. parvicella the maximum specific
growth rate is 0.38 to 1.44 day
1
Tandoi et al., 1998; Rossetti et al., 2005
).
2.5. Nutrient deficiency
Nutrient deficiency can cause the growth of filamen-
tous bacteria. This indeed is in line with the kinetic
selection theory for filamentous growth (
1973
). Filamentous bacteria have high surface-to-vol-
ume (A / V) ratio than non-filamentous bacteria. This
high A / V ratio enables them to take up nutrients from
media containing low levels of nutrient nitrogen, phos-
phorous and other trace elements.
2.6. Temperature
Temperature affects all biological reactions. The
temperature coefficient for floc-forming bacteria is
1.015 for municipal wastewater (
),
while the estimated temperature coefficient values for
M. parvicella strains 4B and RN1 are 1.140 and
1.105, respectively (
). These
imply that the growth of filamentous bacteria is fa-
vored at high temperature. In fact, the temperature-
dependent filamentous growth can be interpreted well
4. Outgrowth of filamentous bacteria in aerobic
granular sludge SBR
Aerobic granulation is a gradual process involving
progression from suspended sludge to aggregates and
further to aerobic granules with a regular outer shape
and compact structure
). Sludge
volume index (SVI) has been commonly used as an
a
b
2
µ
m
5
µ
m
Fig. 1. Microstructures of aerobic granules grown on glucose (a) and acetate (b)
).
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Y. Liu, Q.-S. Liu / Biotechnology Advances 24 (2006) 115–127
Fig. 2. Coexistence of non-filamentous and filamentous bacteria in acetate-fed aerobic granule (
.
indicator of sludge settleability as well as filamentous
growth in activated sludge processes.
shows
changes in SVI and biomass concentration observed
in a large scale aerobic granular sludge SBR fed with
acetate as the sole carbon source. SVI is seen to drop
with the formation of aerobic granules and this is
accompanied by an increase in biomass concentration.
Aerobic granules remain very stable from day 40 to day
100, then a significant increase in SVI is observed
3
), indicating occurrence of filamentous growth in aer-
obic granules. The latter was further confirmed by
microscopic observations (
.
Generally, a sludge has very good settling character-
istics if the SVI value is below 80 ml g
1
. The out-
growth of filamentous bacteria in or on aerobic granule
causes poor settleability and subsequently the washout
of biomass, as indicated by a drop in biomass concen-
tration (
Occurrence of filamentous growth has
been widely reported in aerobic granular sludge SBR
treating different kinds of wastewaters
,
2002; Pan, 2003; McSwain et al., 2004; Tay et al.,
2004; Wang et al., 2004; Hu et al., 2005; Jiang, 2005;
Schwarzenbeck et al., 2005
).
shows the out-
growth of filamentous bacteria on aerobic granules
grown on dairy effluent. Similar fluffy granules were
observed by
Although filamen-
tous growth is a common phenomenon in aerobic gran-
ular sludge SBR, low-levels and moderate-levels of
filamentous growth do not cause operational problems
and may even stabilize the granule structure (
.
However, overgrowth of filamentous bacteria is un-
wanted as it leads to: 1. poor settleability of aerobic
granules; 2. washout of filamentous granules from
SBR; 3. filamentous granules outcompeting the non-
10
250
MLSS
SVI
8
200
6
150
4
100
2
50
0
0
0
30
60
90
120
150
Time (days)
Fig. 3. Changes in sludge volume index (SVI) and biomass concentration in aerobic granular sludge SBR (
).
 Y. Liu, Q.-S. Liu / Biotechnology Advances 24 (2006) 115–127
119
a
b
Fig. 4. Morphology of non-filamentous (a: on day 58 corresponding to
) and filamentous aerobic granules (b: on day 129 corresponding to
). Bar: 2 mm.
filamentous granules; 4. increased concentration of
suspended solids; and 5. eventual disintegration of
aerobic granules (
). The ultimate consequence
of filamentous growth is a failure of the aerobic gran-
ular sludge SBR.
is discharged out of the SBR in accordance with the
preset selection pressures in terms of settling time,
volume exchange ratio and effluent discharge time
). Such an operation strategy makes
use of a low SRT during the period of granulation (
6
). However, as aerobic granulation proceeds, the set-
tleability of biomass progressively improves, i.e. the
SRT tends to gradually stabilize at about 25 days. It
should be pointed out that in most aerobic granular
sludge SBRs, the SRT is not strictly controlled, but
varies naturally with changes in sludge settleability
under given selection pressures.
hypothesized that filamentous bac-
teria have much lower maximum specific growth rate
than floc-forming bacteria as illustrated in
Thus,
a long SRT favors filamentous growth because of a low
specific growth rate of filamentous bacteria. A survey
of domestic wastewater treatment plants revealed that a
SRT of longer than 10 days generally caused serious
filamentous growth problems because of M. parvicella
5. Possible causes of overgrowth of filamentous
bacteria in aerobic granular sludge SBR
As discussed earlier, many factors can trigger fila-
mentous growth in a biological process. Following
main causes can be identified for the overgrowth of
filamentous bacteria in aerobic granular sludge SBR.
5.1. Long SRT in aerobic granular sludge SBR
SRT is recognized to be inversely correlated with the
specific microbial growth rate, i.e. a long SRT implies a
low specific growth rate. During the formation of aero-
bic granules, a substantial amount of suspended sludge
Fig. 5. Outgrowth of filamentous bacteria in aerobic granules grown on dairy effluent
).
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