Science of the Total Environment 643 (2018) 225–237

Contents lists available at ScienceDirect

Science of the Total Environment

journal homepage: www.elsevier.com/locate/scitotenv

Review

Overview of strategies for enhanced treatment of municipal/domestic

wastewater at low temperature
Hexi Zhou a, Xin Li a, Guoren Xu a,b,⁎, Huarong Yu a
a
State Key Laboratory of Urban Water Resource and Environment, Harbin Institute of Technology, Harbin 150090, China
b
National Engineering Laboratory for Sustainable Sludge Management & Resourcelization Technology, Harbin Institute of Technology, Harbin 150090, China

H I G H L I G H T S G R A P H I C A L A B S T R A C T

• Enhanced treatment of low temperature

wastewater is necessary to meet stricter
standards.
• Mechanisms of the effects of low tem-
perature on wastewater treatment are
discussed.
• Strategies for enhanced treatment of
municipal wastewater at low tempera-
ture are systematically summarized.
• Novel process/technology configura-
tions provide attractive alternatives for
performance intensifications at low
temperature

a r t i c l e i n f o a b s t r a c t

Article history: Biological wastewater treatment has been widely applied to municipal/domestic wastewater treatment systems.
Received 25 March 2018 However, low temperature significantly decreases process performance. Furthermore, increasingly stringent ef-
Received in revised form 5 June 2018 fluent discharge standards are causing wastewater treatment facilities to have to improve and maintain contam-
Accepted 8 June 2018
inants removal under low temperature. Hence, this review aims to summarize strategies for enhanced treatment
Available online 21 June 2018
of municipal/domestic wastewater at low temperature. First, mechanisms of the effects of low temperature on
Editor: Jay Gan wastewater treatment, including physiological characteristics, microbial growth rate, microbial activity, micro-
bial community structure and sludge settleability, are analyzed. Strategies for performance intensifications at
Keywords: low temperature, mainly operational parameters regulation, bioaugmentation, biofilm technology, chemical
Low temperature phosphorus precipitation and application of novel process technologies, are then reviewed. Finally, future direc-
Municipal/domestic wastewater tions to address low temperature wastewater are highlighted. A special emphasis is given to the application of
Enhanced treatment novel process/technology configurations to enhance process performance at low temperature in practical
Operational strategies engineering.
© 2018 Elsevier B.V. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 226
2. Mechanisms of the effects of low temperature on wastewater treatment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 226

⁎ Corresponding author at: State Key Laboratory of Urban Water Resource and Environment, Harbin Institute of Technology, Harbin 150090, China.
E-mail address: xgr@hit.edu.cn (G. Xu).

https://doi.org/10.1016/j.scitotenv.2018.06.100
0048-9697/© 2018 Elsevier B.V. All rights reserved.
226 H. Zhou et al. / Science of the Total Environment 643 (2018) 225–237

2.1. Physiological characteristics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 227

2.2. Microbial growth rate . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 227
2.3. Microbial activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 227
2.4. Microbial community structure . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 228
2.5. Sludge settleability . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 228
3. Strategies for enhanced treatment of low temperature wastewater. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 228
3.1. Operational parameters regulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 228
3.2. Bioaugmentation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 229
3.3. Biofilm technology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 230
3.3.1. Hybrid sludge/biofilm system . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 230
3.3.2. MBBR . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 230
3.3.3. BAF . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 230
3.4. Chemical phosphorus precipitation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 230
3.5. Novel process technology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 232
4. Future directions to address low temperature wastewater. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 234
5. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 235
Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 235
References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 235

1. Introduction However, most WWTPs need to meet regional discharge standards

Biological wastewater treatment has been widely applied to munic-
ipal/domestic wastewater treatment processes because of its low oper-
ation costs, high removal efficiency and lower management
requirements (Zhou et al., 2016). During the process, organic matter
and nutrients (nitrogen and phosphorus) from various wastewater
sources are degraded and utilized through microbial metabolism. Tem-
perature is one of the most important environmental factors influencing
microbial functions in biological wastewater treatment processes. In-
deed, temperature can affect biochemical reactions in many ways,
such as reaction rates, reaction pathways, microorganism yields and
death rates (Huang et al., 2015). However, because of differences in geo-
graphic area (higher latitude or hilly regions) and seasonal changes (en-
tering into winter/spring), wastewater temperature can decrease to 8
°C–15 °C, even below 5 °C, which is common for wastewater treatment
systems located in a temperate climate. In Canada, wastewater temper-
atures in lagoon treatment systems decrease to as low as 4 °C during
winter operation (Delatolla et al., 2009), and the temperature at the
end of lagoon pond may drop to 1 °C (Hoang et al., 2014b). In view of
cold regions, low temperatures are defined as “1 °C–15 °C”, occurring
in areas including but not limited to most of Canada, North America,
northern Europe (Norway, Denmark and Sweden, etc.), Russia and
northern China (Wittgren and Mæhlum, 1997). Low temperature se-
verely inhibits microbial activity, substrate utilization rate and cell
growth (Pietikäinen et al., 2005), leading to deteriorated process perfor-
mance. As we all know, low temperature can significantly decrease
wastewater removal efficiency, despite differences in reactor configura-
tions. Therefore, it is still a challenge to maintain and improve process
performance of biological wastewater treatment under low tempera-
ture conditions.
In recent years, with the sustainable development of global economy
and increasing environmental protection consciousness of government
and citizens, the discharge standards of pollutants for wastewater treat-
ment have increasingly improved to alleviate water body pollution and
protect water environment (Jin et al., 2014). For instance, most munic-
ipal wastewater treatment plants (WWTPs) in China have been re-
quired to retrofit existing facilities or upgrade process configurations
to meet the Class 1A of GB 18918-2002 (national standard). Besides
the Class 1A requirement, Beijing, Tianjin and Anhui have issued their
own effluent discharge standards (DB 11890-2012, DB 12/599-2015
and DB 34/2710-2016, respectively), which are more stringent than
the national standard. In the United States (US), Environmental Protec-
tion Agency (EPA) has implemented national secondary treatment stan-
dards for discharges from municipal wastewater treatment facilities.
that are stricter than the secondary standards of US. Furthermore,
EPA's National Pollutant Discharge Elimination System permits estab-
lish different discharge limits and conditions for municipal wastewater
treatment facilities. Therefore, regional WWTPs must upgrade current
facilities to meet the requirements of new EPA permits. In the
European Union (EU), European Commission issued the Urban Waste-
water Treatment Directive (91/271/EEC) and the Water Framework Di-
rective to regulate discharge of urban wastewater. These requirements
have raised the need to retrofit existing WWTPs to meet stricter dis-
charge limits. Beside these directives, the EU members also established
new, strict effluent discharge standards based on the function and sen-
sitivity of receiving water bodies. In Canada, the government has re-
cently implemented the Wastewater Systems Effluent Regulations
that is the first national effluent quality standards. Wastewater systems
that do not meet these standards must upgrade. These high effluent
standards require effective removal of organic matter and nutrient
from wastewater treatment systems. Overall, the increasingly stringent
discharge guidelines have placed great pressure on municipal WWTPs
operators to remove excess contaminants from wastewater at low tem-
perature. Accordingly, how to sustain and enhance pollutants removal
of existing facilities at low temperature is an urgent issue for academic
and engineering fields.
Given the effects of low temperature on biological wastewater treat-
ment and more stringent effluent discharge standards of WWTPs, it is
necessary to improve wastewater treatment efficiency and maintain
operational stability under low temperature. Furthermore, innovative
approaches and technologies have been introduced to improve waste-
water treatment performance. Unfortunately, there has been few pa-
pers summarizing existing strategies to enhance wastewater
treatment performance at low temperature. Therefore, the main objec-
tive of this paper is to discuss mechanisms of the effects of low temper-
ature on wastewater treatment, summarize methods and strategies to
enhance the performance of municipal/domestic wastewater treatment
under low temperature and provide future directions to address low
temperature wastewater. This review will provide guidance to munici-
pal/domestic WWTPs operators and designers to select appropriate
strategies for performance intensification at low temperature.
2. Mechanisms of the effects of low temperature on wastewater
treatment
As mentioned above, temperature is very important to biological
wastewater treatment processes. Most microorganisms in this process
are temperature dependent, with optimum temperatures of 20 °C–35
 H. Zhou et al. / Science of the Total Environment 643 (2018) 225–237
°C (Table 1). Therefore, a decrease in wastewater temperature will inev-
itably affect microbial metabolism and contaminants removal. Specifi-
cally, decreases in temperature may lead to physiological
characteristics deterioration, microbial growth rate decrease, microbial
activity decline, microbial community structure change and sludge
settleability deterioration, which will have adverse effects on the perfor-
mance of wastewater treatment facilities.
2.1. Physiological characteristics
Changes in the environment, such as low temperature, can induce
physiological changes to cells. Low temperature negatively affects the
structural and functional properties of cellular components, both phys-
ically and chemically (Aguilera et al., 2007). Previous studies have
shown that low temperature could change cell membrane structure
and composition (Russell and Fukunaga, 1990; Russell, 1990). Mem-
branes are composed of phospholipids and proteins in a fluid colloidal
phase that exert biological function. As temperature decreases, cells
will regulate membrane lipid composition, resulting in increased unsat-
urated membrane lipids and decreased branched chain lipids (Bhakoo
and Herbert, 1979; Suutari and Laakso, 1993). However, these changes
decrease cell membrane fluidity and permeability and therefore, low
temperature leads to loss of biological function (Adams et al., 2010).
Changes in membrane structure also affect protein function via changes
in the liquid enzyme environment. For example, respiratory and trans-
port proteins function only in the fluid phase. Decreasing fluidity at
low temperature can reduce the activity of proteins, leading to loss of
substrate transport, which restricts microbial nutrient supply and in-
hibits microbial growth. It is widely accepted that, as temperature de-
creases below the optimum level, microbes begin to lose substrate
affinity, leading to lower substrate availability and microbial activity
(Nedwell, 1999). Furthermore, low temperature may damage the ex-
pression of microbial genes in transcription and translation processes
owing to enhanced interactions between the two strands of DNA and
the secondary structure of mRNA (Jones and Inouye, 1996). Cold can
also slow down protein synthesis, leading to decreased enzymatic activ-
ity (García-Ríos et al., 2016). These physiological characteristics nega-
tively shift to some extent as temperature declines, which has adverse
effects on microbial growth and function.
2.2. Microbial growth rate
In biological wastewater treatment systems, microbial communities
involved in removal of carbon, nitrogen and phosphorus mainly include
aerobic heterotrophs, aerobic nitrifiers (AOB and NOB), heterotrophic
denitrifiers and polyphosphate-accumulating microorganisms (PAOs),
which have optimum temperatures around 20 °C–35 °C (Table 1).
When environmental temperatures deviate from this range, the growth
rates of organisms may change. The effect of temperature on the maxi-
mum specific growth rate is commonly described using an Arrhenius
equation. As shown in Table 1, different functional microorganisms
have different maximum specific growth rates and therefore, tempera-
ture causes different impacts on microbial growth rates. Despite differ-
ent temperature effects, microbial growth rates generally decrease by
half for each 10 °C reduction in temperature (Rajeshwari et al., 2000).
Table 1
Kinetic parameters of functional organisms in wastewater treatment systems.
Indication Aerobic heterotrophs
Growth range of temperature 5 °C–40 °C [1]
Optimal temperature 15 °C–25 °C [1]
Temperature coefficients θ 1.0–1.04 [1]
Specific growth rate μ max 1.2–3.5 d−1 [1]
References: [1] (Zhang et al., 2000); [2] (Wiesmann et al., 2007); [3] (Brdjanovicab et al., 1998); [4] (Grady Jr et al., 2011); [5] (Mulkerrins et al., 2004); [6] (Wentzel et al., 1989)
227
As a result, microorganism yields decline at low temperature, which
can cause a decrease in biomass in wastewater treatment systems be-
cause of the washout and discharge of biomass when operated at con-
stant sludge retention times (SRTs). A stable biomass concentration is
crucial to achieving excellent contaminants removal in biological reac-
tors. Furthermore, the reaction rate and removal efficiency are closely
associated with biomass concentrations in wastewater treatment sys-
tems (Lübbecke et al., 1995). However, as temperature decreases, the
biomass concentration decreases, leading to deterioration of effluent
quality. Although psychrophilic bacteria can efficiently develop func-
tions during optimum low temperatures, the low percentages of
psychrotrophs cannot offset the loss of mesophilic bacteria growth
that still largely dominates wastewater treatment systems. Therefore,
as the microbial growth rate drops under low temperature, the biomass
concentration during the wastewater treatment process still decreases
quantitatively, which has adverse effects on biological contaminants
removal.
2.3. Microbial activity
Temperature not only affects the growth rates of microorganisms,
but also their activities. Specifically, the lower wastewater temperature,
the lower microbial activity, with a 50% reduction for every 10 °C de-
cline (Rajeshwari et al., 2000). Biological reaction kinetics in wastewater
treatment systems can generally be expressed by a simplified Arrhenius
equation. For example, nitrifying kinetics can be expressed with a tem-
perature correction coefficient (θ = 1.09) at temperatures between 5 °C
and 30 °C (Rusten et al., 1995; Young et al., 2017). Furthermore, bio-
chemical reaction processes involved in carbon, nitrogen and phospho-
rus removal have different temperature coefficients and therefore,
reaction rates are closely related to functional organism groups. Previ-
ous studies indicated that low wastewater temperature significantly re-
strained microbial activities (Salvetti et al., 2006; Zilouei et al., 2006),
resulting in the inhibition of microbial metabolism. To our knowledge,
nitrifying bacteria are very sensitive to temperature changes and low
temperature drastically decreases their activities and nitrification
rates. A sharp drop in nitrification rate was found at temperatures
lower than 15 °C, with 50% reduction at 12 °C and 100% at 5 °C, and
the optimized activity for nitrification process could be achieved at 15
°C–35 °C (Ducey et al., 2010). Head and Oleszkiewicz (2004) imple-
mented a sudden decrease in temperature from 20 °C to 10 °C in se-
quencing batch reactors (SBRs) and observed that the average
nitrification rate decreased 58% at 10 °C. The average ammonia removal
rate in laboratory moving bed biofilm reactors (MBBRs) after long-term
exposure to 1 °C was measured to be 18 ± 5.1% as compared to the av-
erage removal rate at 20 °C (Hoang et al., 2014a). Besides nitrification,
low temperature can inhibit the activity of denitrifying bacteria, leading
to a decrease in denitrification rate. Welander and Mattiasson (2003)
reported that the denitrification rate at 3 °C was approximately 55% of
that at 15 °C in a stirred lab-scale suspended carrier biofilm reactor.
Moreover, incubation temperatures from 22 °C to 4 °C resulted in an ap-
proximately 77% decrease in denitrification rates (Pfenning and
McMahon, 1997). These results demonstrate that low temperature can
cause a visible decrease in microbial activity.
Aerobic nitrifiers Heterotrophic denitrifiers PAOs
AOB NOB
5 °C–30 °C [2] 5 °C–40 °C [2] 5 °C–40 °C [1] 5 °C–30 °C [3]
28 °C–32 °C [2] 28 °C–32 °C [2] 34 °C–37 °C [1] 20 °C [5]
1.098–1.125 [4] 1.068–1.157 [4] 1.06–1.15 [1] 1.035–1.058 [4]
0.21–1.08 d−1 [1] 0.28–1.44 d−1 [1] 0.48–1.75 d−1 [1] 1.1–1.5 d−1 [6]
228 H. Zhou et al. / Science of the Total Environment 643 (2018) 225–237
2.4. Microbial community structure
Temperature variations also have a significant influence on micro-
bial community structure and species richness (Karkman et al., 2011;
Ma et al., 2013). Low temperature can shift the microbial community
structure of biological wastewater treatment systems because of differ-
ences in the sensitivity and resistance of microorganisms under temper-
ature stress. Generally, low temperature decreases microbial
community diversity and species richness, which may lead to deteriora-
tion of process performance (Chen et al., 2017). For instance, a study of
nitrite-oxidizing bacteria in activated sludge revealed that Nitrospira,
Nitrobacter and a novel cold-adapted nitrite oxidizer responded
strongly to temperature changes, and temperature significantly affected
the population structure of NOB despite their coexistence in the WWTP
(Alawi et al., 2009). Karkman et al. (2011) found that bacterial species
richness in a fixed bed bioreactor decreased when temperature declined
from 10 °C to 5 °C. Although Nitrosomonas and Nitrosospira have tradi-
tionally been considered as the main bacteria for ammonia oxidation
in biological nitrogen removal (BNR) systems, Nitrosospira are usually
present at temperatures lower than 15 °C because of higher resistance
to low temperature than Nitrosomonas (Siripong and Rittmann, 2007;
Zhang et al., 2011). In an enhanced biological phosphorous removal
(EBPR) system, low temperature was found to shift the microbial com-
munity from glycogen accumulating organisms (GAOs) to phosphorous
accumulating organisms (PAOs), which is beneficial to maintenance
and improvement of EBPR performance under low temperature
(Oehmen et al., 2007; Panswad et al., 2003). These results imply that
low wastewater temperature can significantly affect microbial commu-
nity structure.
2.5. Sludge settleability
The activated sludge process is the most commonly used technology
for biological wastewater treatment. A good settling sludge is necessary
for achieving good effluent quality. However, low temperature obvi-
ously affects sludge settleability, leading to poor solids-liquid separa-
tion. This is mainly attributed to excessive extracellular polymeric
substances (EPS) production. Because microbial metabolic activity is
low at low temperature, organic carbon from wastewater cannot
completely be utilized and therefore, some compounds are converted
to polysaccharides. Previous studies indicated that microorganisms pro-
duced large amounts of EPS to protect cells against adverse low temper-
ature stress (Ma et al., 2013; Wang et al., 2010; Wilén et al., 2008).
Excessive EPS are detrimental to the physicochemical properties of mi-
crobial aggregates, such as floc structure, surface charge and settling
characteristics. Furthermore, increasing EPS content may bring more
bound water into microbial aggregates, resulting in porous floc struc-
ture with low density, which significantly influences sludge settleability
(Yang and Li, 2009). Moreover, as temperature decreases, the viscosity
of activated sludge increases, leading to decreased settling velocity of
sludge flocs and hence poor settleability (Guo et al., 2013). As a result,
low temperature can cause poor sludge settleability, leading to deterio-
ration of process performance.
3. Strategies for enhanced treatment of low temperature
wastewater
As mentioned above, low temperature can change physiological
properties of cells, microbial growth rate, microbial activity, microbial
community structure and sludge settleability, leading to deteriorated
wastewater treatment performance. However, drops in temperature
are common because of seasonal climate changes. The effects of low
temperature on municipal/domestic wastewater treatment systems
have frequently been studied, but there is still a need to summarize ef-
fective strategies for enhanced treatment of wastewater under low
temperature.
3.1. Operational parameters regulation
Operational parameters regulation is the most common and pre-
ferred strategy for enhancing biological wastewater treatment under
low temperature. At present, when seasonal temperature drops or low
temperature shocks occur, WWTPs generally reduce the sludge loading
rate and increase their hydraulic retention times (HRTs), SRT and dis-
solved oxygen (DO) to improve resistance and maintain stable perfor-
mance (Wu et al., 2015; Yang et al., 2013). The regulation and control
of these process parameters can alleviate the adverse impacts of low
temperature.
The increase of HRT is an effective method to enhance wastewater
treatment of bioreactors, with a longer HRT decreasing the hydraulic
loading rate and increasing the biochemical reaction time, thereby im-
proving the removal efficiency of wastewater under low temperature.
In a membrane coupled expended granular sludge bed (EGSB) reactor
for domestic wastewater treatment, when the HRT increased from 3.5
to 5.7 h, the total COD removal increased from 76% to 81% at 11 °C
(Chu et al., 2005). Bodı́k et al. (2002) concluded that the COD removal
efficiency in an upflow anaerobic filter (UAF) depended on HRT values
at lower temperatures (5 °C–8 °C). For anaerobic treatment of domestic
sewage, HRTs approximately doubled with every 10 °C decrease
(Zeeman and Lettinga, 1999). Furthermore, a longer HRT in bioreactors
is better for achieving complete nitrification and denitrification at low
temperature. In a biological aerated filter (BAF) system treating low
temperature wastewater (6.5 °C), the nitrification rate increased from
30% to 54% and 95% for HRTs of 0.5 h, 1 h and 2 h, respectively (Ha
et al., 2010). These increases in HRT appear to partially counteract the
loss of nitrification rate with temperature drop.
SRT control is necessary to maintain process performance when sys-
tems suffer from low temperature conditions. A long SRT is conducted
by the increase of sludge return ratio or enlargement of returned sludge
volume to achieve high biomass concentration in bioreactors, decrease
the sludge loading rate and allow the enrichment of slow growing nitri-
fying bacteria. High biomass concentrations are effective to alleviate the
decreasing metabolic rate and microbial activity at low temperature. A
prolonged SRT lessened the influence of low temperature in a SBR for si-
multaneous nitrification and denitrification (SND) (Guo et al., 2013). A
membrane bioreactor (MBR) can retain a high biomass concentration
and be operated with a long SRT, which can achieve good treatment
properties even at low temperatures (Kishino et al., 1996). Adjusting
the SRT is an effective method for efficient nitrogen removal, with
around 45% longer SRT required at 10 °C compared to 20 °C (Kos, 1998).
DO is an important operational parameter in biological wastewater
treatment processes, because it has significant effects on the behavior
and activity of microorganisms living in bioreactors (Holenda et al.,
2008). Specifically, DO concentrations can be raised to optimize and im-
prove contaminants removal at low temperature. High DO levels not
only enhance oxygen mass transfer, but also improve the affinity of sub-
strates to microorganisms, partially offsetting the adverse effects of low
temperature. Previous studies indicated that higher DO concentrations
could enhance the rate of nitrification (Pochana and Keller, 1999;
Stenstrom and Poduska, 1980), which could decrease the effects of
low temperature. Increasing oxygen supply in a membrane separation
bioreactor for domestic wastewater could completely recover nitrifica-
tion at 10 °C and the average nitrogen removal returned to 90% and
85% under 10 °C and 5 °C, respectively (Chiemchaisri and Yamamoto,
1993). These results indicated that sufficient oxygen transfer could be
used to achieve good performance even if the temperature was as low
as 5 °C.
Operational parameters regulation (HRT, SRT and DO) has been uti-
lized as an effective method to improve effluent quality at low temper-
ature. However, modification of parameters may cause other
operational problems in bioreactors. For instance, a longer SRT often
leads to higher sludge loading of secondary clarifiers and no easier sep-
aration from liquid (Krhutková et al., 2006). Moreover, a higher DO may
 H. Zhou et al. / Science of the Total Environment 643 (2018) 225–237 229

produce higher energy costs and lower settling efficiency. Therefore,
these negative factors should also be considered when optimizing and
regulating operational parameters to resist low temperature shock.
3.2. Bioaugmentation
Bioaugmentation is generally an effective way to improving biologi-
cal wastewater treatment performance at low temperature. By intro-
ducing selected pure strains/mixed cultures (such as psychrophilic
bacteria) into bioreactors, the amount and activity of functional bacteria
can be reinforced, and therefore pollutants removal can be significantly
enhanced despite adverse ambient temperatures. In recent years, bio-
augmentation technology has been comprehensively applied to munic-
ipal/domestic wastewater treatment to meet stricter requirements of
effluent discharge in cold regions (Table 2).
There have been serval bioaugmentation methods implemented to
wastewater treatment processes under low temperature. Directly intro-
ducing pure strains/mixed cultures into wastewater treatment systems
is the most common method. Guo et al. (2010) added specialized mixed
bacteria into biological municipal wastewater treatment processes at
low temperature and demonstrated that bioaugmentation was a suc-
cessful strategy to accelerate start-up and ensure daily stable perfor-
mance for practical application of facilities. Krhutková et al. (2006)
described a method of in situ bioaugmentation of nitrification in a full-
scale plant through returning the activated sludge located into a regen-
eration tank. Results indicated that poor performance of nitrification at
low temperature (b13 °C) could be fully compensated by enhancing the
nitrifying population in the activated sludge system. Because of the
characteristics of cold-adaptive bacteria, bioaugmentation by inoculat-
ing these cold-adaptive microorganisms into biological wastewater
treatment systems has been conducted in cold regions. In an intensified
synthetic wastewater treatment process in which screened deep-sea
psychrotolerant strains were inoculated into an aerobic dynamic mem-
brane bioreactor (ADMBR) (Huang et al., 2015), better performance was
achieved at low temperatures, revealing that bioaugmentation with
psychrotolerant strains was a feasible strategy to improve wastewater
treatment performance. By coupling enriched autotrophic-nitrification
and aerobic-denitrification consortiums in SBRs, the total nitrogen re-
moval was greatly enhanced at 10 °C, which demonstrated excellent po-
tential application in practical domestic wastewater treatment through
bioaugmentation (Zou et al., 2014).
Another bioaugmentation method is immobilization technique. This
tool can successfully protect microorganisms from grazing and reduce
biomass washout. Immobilization technology has been shown to be
an effective bioaugmentation way because of higher biomass concen-
tration, higher activity of cell, more stable performance of bioreactors
and easier separation from liquid (Xu et al., 2018). Attachment, contain-
ment and encapsulation are three methods of immobilization for bio-
logical wastewater treatment. A pilot-scale internal circulation aerobic
bioreactor (ICABR) with screened psychrotrophs immobilized on poly-
urethane foam treating domestic wastewater showed excellent organic
matter removal at 4 °C (Xu et al., 2018), which proved that microbial in-
tensification with immobilized psychrotrophs was a feasible strategy for
improving removal efficiency at low temperature. Vacková et al. (2011)
demonstrated that strains of Paracoccus denitrificans, Pseudomonas
fluorescenes or mixed cultures of psychrophilic denitrifiers encapsulated
in PVA pellets could be implemented into the full-scale denitrification
process to improve nitrogen removal at low temperature. By embed-
ding pellets with psychrophilic strains (heterotrophic nitrifying and
aerobic denitrifying bacteria) into subsurface wastewater infiltration
systems (SWISs), sewage treatment performance (such as NH+ 4 -N,
NO− 3 -N and TN removal) significantly improved at low temperature
(Liu et al., 2018). This embedding bioaugmentation strategy ap-
peared to be better than direct-dosing bioaugmentation because of
less inoculation loss. Immobilized bioaugmentation can also be suc-
cessfully applied by MBRs, in which the membrane module prevents
washout of inoculated specialized strains from the bioaugmented
system (Herrero and Stuckey, 2015). Although this method has not
been used for municipal/domestic wastewater treatment at low
temperature, a bioaugmented MBR for treatment of other types of
wastewater under adverse conditions was recently found to run
well, implying that coupling bioaugmentation with MBRs is an
effective alternative to municipal wastewater treatment at low
temperature.

Table 2
Application of bioaugmentation technology for municipal/domestic wastewater treatment at low temperature.

Bioaugmentation source Bioreactor Temperature Performance variation Reference

(°C)

Nitrifiers A2 O 14 The ammonia removal efficiency increased (Pei et al., 2015)

by 25%, and specific ammonia utilizing rate and
specific nitrite utilizing rate increased by 1.86 and
1.90 times.
Specialized mixed bacteria A/O, SBR, Oxidation 13 ± 2, 13 ± 2, 12 ± 2 The effluent quality met the Class 1B of GB (Guo et al., 2010)
ditch 18918‐2002.
Nitrifying bacteria from regenerated Activated sludge winter: 10–13 The ammonia nitrogen elimination was higher than (Krhutková et al., 2006)
return sludge process 90%.
Two deep-sea psychrotolerant strains ADMBR 25, 20, 15, 10, 5 Higher removal efficiency for COD, NH+ 4 -N, TN, TP (Huang et al., 2015)
15, 12, 10, 7, 5 at 15 °C or lower.
Enriched autotrophic-nitrification and SBR 10 The maximum specific nitrifying/denitrifying rate (Zou et al., 2014)
aerobic-denitrification consortiums reached 8.85 and 32.93 mg N/g SS/h. SBR achieved
a higher TN removal rate of 3.3 mg N/L/h.
Nitrifying biomass treating warm centrate SBR 10 Effluent NH+ 4 -N concentrations were b5 mg/L. (Head and Oleszkiewicz,
2004)
Paenibacillus sp.XP1 Constructed 15–21 The removal efficiencies were 73% for COD, 94% for (Shao et al., 2013)
wetland NH+4 -N and 78% for TN.
Screened psychrotrophs strains ICABR 4, winter: 4–10, summer: The effluent COD maintained among 31–58 mg/L, (Xu et al., 2018)
immobilized on PUF 20–28 resulting in 83%–90% COD removal at 4 °C.
Paracoccus denitrificans, Pseudomonas SBR 15, 10, 8, 5 The specific denitrification rate varied from 26.2 to (Vacková et al., 2011)
fluorescens 297 mg NO− 3 -N/kg pellets/h or 2.4 to 36.6 mg
and mixed culture of psychrophilic NO−3 -N/g proteins/h.
denitrifiers
encapsulated into PVA
Seven psychrophilic strains SWIS 22 ± 2, 15 ± 2, 12 ± 2 The average effluent concentrations of NH+ 4 -N, (Liu et al., 2018)
(heterotrophic nitrifying NO−3 -N,
and aerobic denitrifying bacteria) TN and COD embedding bioaugmentation
were 4.48, 9.67, 14.56 and 27.57 mg/L at 12 °C.
230 H. Zhou et al. / Science of the Total Environment 643 (2018) 225–237
However, bioaugmentation is still at the risk of bioaugmentation
failures. For example, it is often reported that a significant increase in
bioreactor performance after bioaugmentation is only maintained for
a short time. Owing to competition or inhibition, selected strains often
lose their abilities shown in the laboratory pure cultures conditions
(Herrero and Stuckey, 2015). These practical operational problems
should be considered when applying bioaugmentation methods.
3.3. Biofilm technology
To our knowledge, biofilm has the potential to decrease temperature
sensitivity of embedded bacteria. Therefore, filling suspended or fixed
carriers/media to form biofilms is a common method for elevating the
performance of biological wastewater treatment systems under low
temperature. Suspended or fixed carriers/media can provide sufficient
attachment surfaces for microbial growth and proliferation, and there-
fore highly increase the total amount of biomass. Furthermore, these
carriers allow for the enrichment of slow growing nitrifying bacteria,
which is essential to ammonia oxidation during the wastewater treat-
ment process. The activities of AOB and NOB on attached carriers have
been reported to be higher than in suspended biomass (Regmi et al.,
2011). Among these biofilm technologies, hybrid sludge/biofilm system,
MBBR and BAF are commonly applied to low temperature wastewater
treatment.
3.3.1. Hybrid sludge/biofilm system
A hybrid sludge/biofilm system is often designated as integrated
fixed-film/activated sludge (IFAS), which is a modification of conven-
tional activated sludge process (Zhou et al., 2016). This technology com-
bines the advantages of suspended activated sludge and attached
biofilm, and therefore provides stable and reliable pollutants removal
under low temperature. In particular, IFAS can provide year round nitri-
fication, which will allow retrofitting existing facilities in cold climates.
As shown in Table 3, several studies have demonstrated that hybrid
sludge/biofilm was a reliable and successful alternative to biological
wastewater treatment under cold conditions (Randall and Sen, 1996;
Andreottola et al., 2000; Di Trapani et al., 2013; Zhou et al., 2016).
Hubbell et al. (2006) implemented a full-scale demonstration of IFAS
using a new fabric media and eight years of operation indicated that
this retrofitting technology was successful for cold weather nitrification.
Similar findings also demonstrated a hybrid activated sludge/biofilm
process could be efficiently applied to upgrade a conventional activated
sludge plant to achieve year round nitrification in a cold climate region
(Di Trapani et al., 2011). Besides enhancement of nitrification and deni-
trification, the experimental results also confirmed that EBPR could be
incorporated successfully into the IFAS system at low temperature (10
± 1 °C) (Sriwiriyarat and Randall, 2005b), but this decoupling process
did not appear to efficiently remove phosphorus.
3.3.2. MBBR
MBBR was initially designed as a nitrogen remove system in the
1980s (Hem et al., 1994). Because of its advantages of small footprints,
simple operation and efficient removal, MBBR has been applied for car-
bon removal, as well as for nitrification and denitrification. Recently,
MBBR has been demonstrated to have the potential for achieving and
maintaining nitrification at low temperature (Hoang et al., 2014a,
2014b; Bjornberg et al., 2009; Ødegaard, 2006; Delatolla et al., 2010).
Andreottola et al. (2000) evaluated the performance of a full-scale up-
grade of an existing wastewater treatment plant using a MBBR system
at low temperature (5 °C–15 °C). Results indicated the MBBR system
was capable of stable and efficient removal, despite seasonal tempera-
ture fluctuations. Ødegaard (2006) also found that complete nitrifica-
tion could be achieved at 11 °C for full-scale MBBR applications in
Europe, with nitrification and denitrification rates as high as 1.2 g
−
NH+ 2 2
4 -N/m /d and 3.5 g NO3 -N/m /d, respectively. Welander and
Mattiasson (2003) studied the denitrification process in a MBBR at
low temperature and proved that MBBR was a useful alternative for en-
hancing denitrification performance in a cold climate. Besides second-
ary treatment, MBBR has been identified as a potential tertiary unit for
ammonia removal in cold climates. Young et al. (2016) demonstrated
that ammonia effluent concentrations below 5 mg/L in a MBBR system
could be achieved at 1 °C, a critical temperature for tertiary treatment
for lagoons in northern climates. Similar studies also indicated MBBR
technology had significant ammonia removal capacity at 1 °C (Hoang
et al., 2014a; Almomani et al., 2014). Hence, this system appears to
have the potential as an upgrade or replacement technology for the en-
hanced removal of carbon and nitrogen at low temperature.
3.3.3. BAF
BAF, an attached growth treatment system, is widely adopted for en-
hanced wastewater treatment with high removal efficiency and capac-
ity for organic matter and ammonia. Paffoni et al. (1990) confirmed that
BAF technology was feasible as a compact tertiary treatment for effluent
polishing and allowed to upgrade effluent quality and expand the ca-
pacity of existing facilities. Payraudeau et al. (2001) studied BAF tech-
nology as a tertiary treatment in the Davyhulme Wastewater
Treatment Works and proved that this technology was an effective
BNR retrofit capable of highly effective ammonia removal at tempera-
tures as low as 7 °C. Hansen et al. (2007) evaluated the process perfor-
mance of activated sludge and BAF over ten years of full-scale operation
and concluded that BAF could maintain better and more stable nitrifica-
tion compared to the activated sludge, particularly at low temperature.
Because of the advantages for improving and maintaining ammonia re-
moval in cold climates, BAF has been identified as a potential solution to
achieve year round nitrification in Canada, where it may be incorpo-
rated with current lagoon wastewater treatment systems (Delatolla
et al., 2010). Ha et al. (2010) investigated temperature effects on nitrifi-
cation in BAF and found that BAF had adequate nitrification (95%) at a
HRT of 2 h at 6.5 °C. When the HRT was reduced to 1 h, BAF remained
high nitrification rate (92%) by recirculating 200% effluent. The high ef-
fluent quality implied that BAF technology could be used as an add-on
process after the aerated lagoons for nitrification under cold weather
conditions. However, BAF must be periodically backwashed to remove
excess solids, which may increase operational costs and management
requirements.
Taken together, these investigations indicate that biofilm technology
is an effective upgrade for improving organic matter and nitrogen re-
moval from municipal/domestic wastewater under low temperature.
However, these biofilm technologies have relatively poor biological
phosphorus removal because of less waste sludge. Therefore, coupling
chemical coagulation with biofilm technologies seems to be a valid al-
ternative for enhancing removal of carbon, nitrogen and phosphorus
in cold climates.
3.4. Chemical phosphorus precipitation
Chemical phosphorus precipitation has been widely applied as a re-
liable approach for improving phosphorus removal from municipal/do-
mestic wastewater. Today, WWTPs that utilize secondary biological
wastewater treatment at low temperature often do not remove suffi-
cient amounts of phosphorus to meet stringent effluent standards.
Chemical precipitation with metal salts (iron, aluminum and calcium)
is a common commercial practice to enhance phosphorus removal.
This approach involves the addition of soluble metals salts to wastewa-
ter and the dissolved cations efficiently bond with soluble phosphorus,
subsequently eliminated by forming precipitated sludge. A study of
chemical phosphorus removal showed that coagulant species, coagu-
lant dosages and pH were the main factors influencing the process
(Clark and Stephenson, 1999), and therefore low temperature could
have less impact on chemical phosphorus precipitation. Nutt (1985)
found that chemical precipitation was technically and economically fea-
sible for retrofitting WWTPs to achieve b1.0 mg/L TP. In many practice
 H. Zhou et al. / Science of the Total Environment 643 (2018) 225–237 231

Table 3
Application of biofilm technology for enhanced treatment of municipal/domestic wastewater at low temperature.

Carriers type Bioreactor Temperature Performance variation Reference

(°C)

Polypropylene Hybrid A2O 26, 22, 18, 14, The average effluent of COD, NH+4 -N, TN and TP were 29.8, 3.9, 10.9 (He et al., 2016a)
sphere filler 10 and 0.45 mg/L with the average removal rate of 84.5%, 91.3%, 78.1%
and 91.8% at 10 °C.
Suspended carriers Hybrid A/O 25, 15, 10 The average removal rates of NH+4 -N and TN were 95.7% and 72% with (Zhou et al., 2016)
the average effluent concentration of 2.4 mg/L and 14.3 mg/L at 10 °C.
+
AnoxKaldnes K1 IFAS 13–22 The average effluent NH4 -N was 0.37 mg/L at 11 °C–15 °C. The average (Onnis-Hayden et al.,
effluent TP was 1.2 mg/L with influent varying 6–21.7 mg/L. 2011)
BioWeb IFAS The IFAS train removed approximately 20% more ammonia than the other (Hubbell et al., 2006)
activated sludge trains.
AccuWeb fabric IFAS 5–17 The average effluent ammonia was below 0.5 mg/L. (Hubbell and McDowell,
2003)
Accuweb media IFAS 10 ± 1 The complete nitrification could be achieved. (Sriwiriyarat and
Randall, 2005a)
Ringlace media IFAS 13 The nitrification rate increased by 125%, attaining 1.75 kg NH4+-N/d/m at (Randall and Sen, 1996)
15 °C. 30%–88% of NO− 3 -N formed in the aerobic zone was denitrified.
Kaldnes™ K1 Hybrid MBBR 9.72, 11.54, The COD loading rates were up to 3.0 kg TCOD/m3/d and 1.8 kg FCOD/m3/d. (Di Trapani et al., 2013)
13.83
Kaldnes™ K1 Hybrid MBBR 11.5 The removal efficiency of NH+ 4 -N was 99% with ammonium volumetric (Di Trapani et al., 2011)
loading rates up to 0.15 kg NH+ 3
4 -N/m /d.
Suspended carriers Hybrid 11–20 The nitrification rate was 0.9–1.2 g NH+ 2
4 -N/m /d corresponding to a (Christensson and
sludge/biofilm volumetric rate of 19–23 g NH4+-N/m3/d. Welander, 2004)
process
FLOCOR-RMP® MBBR 5–15 The organic and ammonia loads were the average 7.9 g COD/m2/d (Andreottola et al., 2000)
and 0.9 g NH+ 2
4 -N/m /d. Typical carbon and nitrogen were 73% and 72% at
temperature lower than 8 °C.
K1 MBBR 3–14 Nitrification rates and denitrification rates were as high as 1.2 g NH+ 2
4 -N/m /d (Ødegaard, 2006)
and 3.5 g NO− 2
3 -N/m /d at 11 °C.
Kaldnes K1 MBBR 3–20 The max denitrification rate varied between 1.54 and 4.6 g NOx−-N/m2/d (Welander and
with NO− −
3 -N of 2.3–4.9 mg/L and NO2 -N of 0.1–0.2 mg/L in the outlet. Mattiasson, 2003)
AnoxKaldnes K5 MBBR 1 The ammonia effluent concentrations were below 5 mg/L, with a maximum (Young et al., 2016)
removal rate of 230 g N/m3/d.
AnoxKaldnes K3 MBBR 1–20 The average ammonia removal were 0.26 and 0.11 kg N/m3/d at 20 °C (Almomani et al., 2014)
and 1 °C, respectively.
K1 MBBR 4.2 The average removal of ammonia was over 40%. (Wessman and Johnson,
2006)
Plastic module MBBR 7.7–21 The average NH+ 4 -N removal efficiencies were 92.4% below 15 °C and (Bjornberg et al., 2009)
85.6% above 15 °C.
AnoxKaldnes K3 MBBR 20, 5, 1 The nitrification rate at 5 °C was 66 ± 3.9% and 64 ± 3.7% compared (Hoang et al., 2014b)
to the rate at 20 °C. The nitrification rates at 1 °C were 18.7 ± 5.5% and
15.7 ± 4.7% compared to the rate at 20 °C.
AnoxKaldnes K3 MBBR 20, 1 The average ammonia removal rate at 1 °C was 18 ± 5.1% of removal at 20 °C. (Hoang et al., 2014a)
AnoxKaldnes K5 MBBR 20, 1 The average removal rate at 1 °C were 22.8% of the maximum ammonia (Young et al., 2017)
removal rate at 20 °C.
Kaldnes MBBR 3–4 The rates of ammonia removal were approximately 0.21 kg N/m3/d and (Delatolla et al., 2010)
0.14 kg N/m3/d at 8 °C and 4 °C, respectively.
Floating media BAF 7–10 The outlet ammonia concentration always remained below 1 mg/L. (Payraudeau et al., 2001)
Natural zeolite, BAF 20–25, 7–10 Zeolite BAF and expanded clay BAF have COD and NH+ 4 -N removals in the (He et al., 2007)
expanded clay range of 74.5%–88.47% (average of 81.57%), 71.73%–88.49% (average of 81.06%),
71.91%–87.76% (average of 80.49%) and 38.41%–77.17% (average of 65.42%),
respectively, under water temperature of 7 °C–10 °C.
Gravel BAF 6.5 Approximately 95% of NH+ 4 -N was nitrified at a HRT of 2 h. By recirculating (Ha et al., 2010)
200% of the effluent, NH+ 4 -N removal improved from 54% to 92% at a HRT of 1 h.
Floating media BAF 7 The maximal nitrification capacity was about 0.59 kg of formed (Canler et al., 2003)
NO− 3
3 -N/(m of material)/d.
Kaldness BAF 3–4 The rates of ammonia removal were approximately 0.26 kg N/m3/d and (Delatolla et al., 2010)
0.18 kg N/m3/d at 8 °C and 4 °C, respectively.
Expanded schist BAF 12–14 An ammonia load of 0.5 kg N/m3/d was completely oxidized at 13 °C. (Paffoni et al., 1990)
Vitrified clay medium BAF 10.9–23.1 The ammonia removal rate ranged from 72% to 88% at 10.9 °C–15.3 °C. (Stensel et al., 1988)
The effluent TBOD concentrations were b15 mg/L during the operation.
Floating polystyrene BAF 10–17 The monthly average of ammonia was 0.5–1.2 mg/L. The yearly average of (Thøgersen and Hansen,
carrier total nitrogen was 5.4 mg/L. 2000)
Non-woven polyester BAF The average removal of COD, BOD, SS and TKN were 88%, 90%, 91% and 46% in winter. (Abou-Elela et al., 2015)
fabric
Floating media BAF 8–18 The ammonia effluent was below 5 mg/L. The yearly average of COD and TN were 58 (Hansen et al., 2007)
mg/L and 8.7 mg/L, respectively.

cases, chemical phosphorus removal is a common supplementation
for biological phosphorus removal. In a pilot-scale MBR treating mu-
nicipal wastewater, a final effluent phosphorus concentration b 0.3
(95%) mg/L was achieved with the addition of ferrous salts, which
demonstrated that the addition of ferrous salts was a good alterna-
tive to improving phosphorus removal in the MBR system (Wang
et al., 2014). Despite the widespread use of chemical phosphorus re-
moval, it seems to attract little research interest in wastewater treat-
ment fields, especially for low temperature wastewater. Chemical
phosphorus precipitation with high quality effluent also has disad-
vantages, such as, high chemical costs and considerable creation of
chemical sludge.
232 H. Zhou et al. / Science of the Total Environment 643 (2018) 225–237

3.5. Novel process technology
Several novel wastewater treatment processes have been developed
to enhance contaminants removal and strengthen the capacity of
wastewater treatment systems. These novel technologies have been re-
ported to be feasible or favorable for municipal/domestic wastewater
treatment at low temperature (Table 4).
In recent years, the development and application of MBRs have
attracted more attention to upgrade and retrofit existing municipal
WWTPs to meet stricter discharge demands. This technology involves
suspended growth activated sludge systems that utilize microporous
membranes for solid/liquid separation instead of secondary clarifiers.
Compared to conventional activated sludge, MBR technology has
many advantages, including higher biomass concentrations, highly im-
proved effluent quality and significant operational reliability. Therefore,
MBR technology appears to have the potential to improve the perfor-
mance of municipal/domestic wastewater treatment during winter.
Gurung et al. (2017) assessed the performance of a pilot-scale MBR to
treat real municipal wastewater at low temperature (7 °C–20 °C) in
Nordic regions. Despite low temperature operation, high effluent qual-
ity was still achieved. The average effluent concentrations of COD,
NH+ 4 -N and TP were 18.7 mg/L, 0.02 mg/L and 0.43 mg/L, with the aver-
age removal rate 92.8%, 100% and 90.6%, respectively. Moreover, no
significant differences in terms of COD and NH+ 4 -N removal were ob-
served in a full-scale pre-denitrification MBR system treating urban
wastewater, when the mixed liquor temperature decreased from N25
°C to b15 °C (Arévalo et al., 2014). Furthermore, a long-term full-scale
MBR operation in California showed excellent process performance
year round, with the COD, TN and TP removal efficiencies of 95%, 94%
and 66%, respectively (Tu et al., 2017). Of course, MBR stability depends
on the magnitude of fluctuations by temperature variations. Zhang et al.
(2014) found that low wastewater temperature deteriorated effluent
quality, but MBR was still a good practice for wastewater treatment in
low temperature zones. However, membrane fouling and energy con-
sumption remain operational obstacles and challenges to the wide-
spread application of MBR. Specially, low temperature results in
intensified membrane fouling, such as increasing permeate fluid viscos-
ity, which should be given further thought when applying MBR for en-
hancement of municipal/domestic wastewater treatment at low
temperature.
Aerobic granular sludge (AGS) technology is regarded as a promising
biotechnology for the treatment of municipal/domestic wastewater.
Compared to conventional activated sludge, aerobic granules exhibit
compacted structure, diverse microbial species and excellent settling
capability. Therefore, it has been widely applied for the treatment of
various wastewaters, including municipal wastewater. Lab-scale and

Table 4
Novel process technology for municipal/domestic wastewater treatment at low temperature.

Novel technology Bioreactor Temperature Performance variation Reference

(°C)

MBR MBR 7–20 The average effluent concentrations of COD, NH+ 4 -N and TP were 18.7 mg/L, 0.02 mg/L and (Gurung et al.,
0.43 mg/L with the average removal rate 92.8%, 100% and 90.6%, respectively. 2017)
MBR MBR 9–31 The COD and BOD5 removal rates for all temperatures were over 98% and 99.5%, (Arévalo et al.,
respectively. The NH+4 -N removal rate reached 99% with effluent concentrations lower than 2014)
1 mg/L during the different temperature periods.
MBR MBR 13–22 The effluent COD concentrations were 10 ± 5 mg/L and 25 ± 4 mg/L at temperature of 22 (Zhang et al., 2014)
°C and 13 °C, respectively. The average effluent NH+4 -N concentration was b0.1 mg/L
throughout the experimental period.
MBR MBR 8–30 The COD and BOD5 removal were 94%, 98% and 90%, 90% in summer and winter, (Shin et al., 2014)
respectively. The average effluent COD and BOD5 were below 23 mg/L and 9 mg/L,
respectively.
MBR MBR 13–20 The COD, TN and TP removal efficiencies were 95%, 94% and 66%, respectively. (Tu et al., 2017)
AGS SBR 7 The removal performance was 75%–80% in COD, 70%–76% in TN and 50%–60% in TP. (Gonzalez-Martinez
et al., 2017)
AGS SBR 3, 5, 7 The performance achieved 75%–80% for COD, 90%–95% for BOD5, around 50% for NH+ 4 -N at (Gonzalez-Martinez
5 °C. et al., 2018)
AGS SBR The average effluent TN and TP were 6.9 mg/L and 0.9 mg/L, respectively. The maximum (Pronk et al., 2015)
volumetric conversion rate for nitrogen and phosphorus were respectively 0.17 and 0.24
kg/m3/d.
AGS SBAR 12, 15, 18 The average removal efficiencies of COD, NH+ 4 -N, TN and TP were over 90.9%, 94.7%, 75.4% (Jiang et al., 2016)
and 80.2%, respectively, at 12 °C.
AGS SBAR 10 The average removal efficiencies of COD, NH+ 3−
4 -N and PO4 -P were 90.6%–95.4%, (Bao et al., 2009)
72.8%–82.1% and 95.8%–97.9%.
PN SBR 11.9–26.5 High nitrogen removal efficiency with effluent total nitrogen below 3 mg/L could be (Yang et al., 2007)
achieved.
PN SBR 11–26 The effluent TN and TN removal efficiency were maintained at 2 mg/L and 98%, (Gu et al., 2012)
respectively.
PN/A MBBR 15–29 The removal efficiencies of ammonium and total nitrogen were over 90% and 70%, with (Laureni et al.,
average effluent ammonia and total nitrogen of 2 mg/L and 6 mg/L, respectively. 2016)
PN/A MBBR 10–20 The effluent ammonia concentration was kept b8 mg/L during the whole operation. The (Gilbert et al., 2014)
ammonia conversion was 15 g N/m3/d at 10 °C.
PN/A SBR 12 The nitrogen removal was above 90%. (Hu et al., 2013)
Aerobic SBR 10 The maximum specific nitrifying and denitrifying rates were 8.85 and 32.93 mg N/g SS/h, (Zou et al., 2014)
denitrification respectively.
Aerobic SBR 25, 15, 10, 5 This process effectively removed COD and nitrate (above 90%) even at 5 °C. (Wang et al., 2015)
denitrification
Electrochemical MBR 20, 10 The system removed N99% of ammonia, N95% of dissolved COD and N90% of ortho-P. (Wei et al., 2012)
MFC A2O 12–14.7 The average removal efficiencies of COD, TN and TP increased by 15.9%, 9.3% and 1.4%, (Xie et al., 2014)
respectively.
Electrocoagulation Rotating hanging 13.2–25.6 The effluent quality was achieved with 0.26 mg/L BOD5, 11.46 mg/L COD, 0 mg/L NH+ 4 -N, (Nguyen et al.,
media bioreactor and 3.81 mg/L TN and 0.03 mg/L TP. 2014b)
MBR
Electrochemical MBR 15.4 ± 2.5 The removal rates of COD, NH+ 3−
4 -N and PO4 -P were 92%, 99% and 99%, respectively. (Hasan et al., 2014)
Microalgae Batch 25, 15, 5 The average total nitrogen and phosphorus removal were 72% and 100%, respectively. (Delgadillo-Mirquez
et al., 2016)
 H. Zhou et al. / Science of the Total Environment 643 (2018) 225–237
pilot-scale studies of the feasibility of using AGS for simultaneous re-
moval of COD, nitrogen and phosphorous under low temperature have
recently been published. For example, a lab-scale AGS system was suc-
cessfully started-up and operated at 7 °C using cold-adapted activated
sludge from Finland as inoculum, with removal performance of 75%–
80% for COD, 70%–76% for TN and 50%–60% for TP. (Gonzalez-Martinez
et al., 2017). The high removal capacity indicated this system was a re-
liable alternative to enhancing pollutants removal under low tempera-
ture. In another study, an AGS bioreactor using cold-adapted sludge
from Lapland also achieved high carbon, nitrogen and phosphate re-
moval efficiency at 5 °C (Gonzalez-Martinez et al., 2018). Recently, a
full-scale AGS system for domestic wastewater treatment in
Netherlands was evaluated (Pronk et al., 2015). The operational data
showed that the effluent requirements (7 mg/L N and 1 mg/L P) were
easily reached in Dutch climate conditions. This appears to imply that
AGS technology can be effectively implemented for the treatment do-
mestic wastewater. However, low temperature can lead to operational
failures, such as destruction of granules and washout of biomass and
therefore, it is difficult to startup such systems under cold temperature.
Moreover, this technology showed unstable operation at temperatures
as low as 8 °C because of excessive growth of filamentous bacteria
(Gonzalez-Martinez et al., 2017). Efforts have been taken to achieve
the stable operation and full-scale application of this technology. As a
promising technology, AGS still needs further study to improve the sta-
bility and performance for the application of full-scale system at low
temperature.
Nitrogen removal via nitrite based on traditional nitrification-
denitrification process has been rapidly developed. Because of shorten-
ing reaction process, this approach produces savings in the oxygen
needs during nitrification, a reduction in the denitrification organic
matter requirements, and a decrease in excess sludge production. In a
pilot-plant SBR, nitrogen removal via nitrite from municipal wastewater
treatment at low temperature using a real-time control strategy was in-
vestigated. Results showed that high nitrogen removal (TN below
3 mg/L) could be achieved for a long period, implying that partial nitri-
fication (PN) denitrification could be feasible for treating real municipal
wastewater at low temperature (Yang et al., 2007). Ma et al. (2009)
demonstrated that the nitrite pathway improved TN removal by about
20% compared to the nitrate pathway in a pilot-scale continuous pre-
denitrification plant treating domestic wastewater. Anaerobic ammonia
oxidation (anammox) also provides a novel and promising biological ni-
trogen removal alternative for wastewater treatment. The implementa-
tion of anammox via combined partial nitritation/anammox (PN/A) for
autotrophic nitrogen removal in municipal wastewater treatment may
significantly increase in the future because of reduced aeration costs, di-
minished sludge production and no external carbon source. To date, the
PN/A process has been applied for municipal wastewater treatment at
low temperature. Laureni et al. (2016) assessed the long-term stability
of mainstream PN/A process in lab-scale MBBRs operating at low tem-
perature for pre-treated municipal wastewater and demonstrated that
this technology was reliable when operated at temperatures above 13
°C. Similarly, stable PN/A could be achieved in a MBBR treating synthetic
wastewater in winter when the wastewater temperature did not drop
below 13 °C (Gilbert et al., 2014). Hu et al. (2013) investigated nitrogen
removal from pre-treated municipal wastewater by a lab-scale
nitritation-anammox bioreactor at low temperature and proved that
this application could be successfully achieved for over 300 days with
nitrogen removal of above 90% at temperatures as low as 12 °C. How-
ever, these applications were conducted in lab-scale or pilot-scale and
therefore, challenges to achieving full-scale implementation and main-
taining long-term stable and reliable operation under cold conditions
still exist.
SND means that nitrification and denitrification can occur concur-
rently in a single reactor under identical operating conditions. SND has
become an attractive technology for nitrogen removal because of its po-
tential to eliminate the need for a separate nitrification stage, resulting
233
in a simplified and smaller plant design. Compared to conventional ni-
trification and denitrification process, this process also reduces the
need for carbon source and oxygen consumption. Many studies have fo-
cused on operational conditions for achieving SND. Wang et al. (2006)
successfully established SND in a MBBR by controlling DO at about
2 mg/L and achieved approximately 89.9% TN removal. In an intermit-
tently aerated reactor, the average COD and nitrogen removal efficien-
cies reached above 95% and 90%, respectively, under optimal
conditions. The high nitrogen removal was mainly attributed to effec-
tive SND via nitrite (Yooa et al., 1999). Another similar study indicated
TN removal efficiency could reach 87.8% via short-cut SND in an inter-
mittently aerated moving bed MBR (Yang and Yang, 2011). These stud-
ies described highly effective nitrogen removal, implying that it has the
potential for application to enhance wastewater treatment at low tem-
perature. However, Guo et al. (2013) investigated the influences of tem-
perature on SND in a SBR and found that operational parameters
regulations and control could alleviate the effects of low temperature,
but the performance of SBR through SND was still extremely low at 10
°C and 5 °C. These findings implied that this SND system could not effec-
tively resist the effects of low temperature. Therefore, how to effectively
apply SND technology for municipal wastewater treatment at low tem-
perature deserves further exploration.
Recently, bacteria capable of both heterotrophic nitrification and
aerobic denitrification have drawn increasing attention for their poten-
tial application in BNR. Compared to traditional nitrogen removal pro-
cess, aerobic denitrification is widely focused on higher growth rate
and more efficient substrate removal of simultaneous organic carbon
and nitrogen. Significantly, SND can be achieved under single aerobic
conditions and hence highly enhance the removal of nitrogen. Further-
more, some strains can exhibit effective nitrogen removal, even at low
temperature. For example, Aeromonas sp. HN-02 obtained 0.90 mg/L/h
of ammonia removal rate, even at 5 °C and showed higher tolerance
to low temperature than common mesophilic bacteria (Chen et al.,
2014). Moreover, the average removal rates at 10 °C reached as high
as 3.03, 2.51 and 1.88 mg N/L/h for ammonia, nitrite and nitrate, respec-
tively (Yao et al., 2013). Pseudomonas tolaasii Y-11 was also shown to
have the potential to remove ammonia, nitrite and nitrate at low tem-
perature (He et al., 2016b). By coupling psychrotrophic autotrophic ni-
trifying and aerobic denitrifying consortiums, the maximum specific
nitrifying/denitrification rate reached 8.85 and 32.93 mg N/g SS/h, re-
spectively, at 10 °C, implying huge potential for efficient nitrogen re-
moval in practical applications at low temperature (Zou et al., 2014).
Wang et al. (2015) successfully established a stable lab-scale aerobic
denitrifying process and demonstrated that effective COD and nitrate
(N90%) removal could be achieved, even at 5 °C. These isolated cold-
adapted aerobic denitrifying bacteria provide a new aspect for highly ef-
fective nitrogen removal at low temperature. However, further study
should be conducted to evaluate the long-term stability of aerobic deni-
trification and how to enlarge its application to full-scale wastewater
treatment systems.
Recently, a novel process incorporating both phosphorus and nitro-
gen removal has been developed, in which denitrifying polyphosphate
accumulating organisms (DNPAOs) use nitrite or nitrate instead of oxy-
gen as electron acceptors to simultaneously remove phosphorus and ni-
trogen from wastewater. In comparison with conventional biological
phosphorus removal, denitrifying phosphorus removal does not require
the addition of an external carbon substrate for denitrification, while
also providing considerable savings in aeration energy. Therefore,
denitrifying phosphorus removal has been applied to achieve higher ni-
trogen and phosphorus removal. Ng et al. (2001) evaluated the feasibil-
ity of denitrifying phosphorus removal in an anaerobic/anoxic SBR.
Results indicated that anoxic phosphorus uptake with simultaneous de-
nitrification could occur in the anoxic zone, with phosphorus removal
rate of 40%–100%. Simultaneous biological phosphorus and nitrogen re-
moval with enhanced anoxic phosphate uptake was also investigated in
another SBR. The system showed stable phosphorus and nitrogen
234 H. Zhou et al. / Science of the Total Environment 643 (2018) 225–237
removal performance with the average removal of TOC 92%, TN 88% and
phosphorus 100%, respectively, implying a promising potential for en-
hanced biological phosphorus and nitrogen removal (Lee et al., 2011).
Zeng et al. (2011) studied denitrifying phosphorus removal in a contin-
uous anaerobic-anoxic-oxic (A2O) process treating domestic wastewa-
ter. Results showed that the average TN and phosphorus removal
were 75% and 98%, respectively, as well as denitrifying phosphorus re-
moval of 66%–91% occurred in the anoxic zone. Another similar study
also showed that phosphorus removal was mainly completed by
denitrifying phosphorus removal of about 90% occurred in the anoxic
zone (Zeng et al., 2013). These results indicated that denitrifying phos-
phorus removal could be effectively achieved to enhance the removal of
nitrogen and phosphorus. However, there is few studies on denitrifying
phosphorus removal at low temperature. Accordingly, future studies
should focus on whether denitrifying phosphorus removal process can
be successfully applied to low temperature wastewater.
There has recently been growing interest in the development of
electrochemical methods to improve biological wastewater treatment.
Appropriate electrical stimulation may improve bioactivity and micro-
bial metabolism. High removal efficiency in a bio-electrochemical sys-
tem was attributed to coupling the electrochemical process and
biodegradation (Liu et al., 2017), which appears to be conducive to alle-
viating the impact of low temperature on biological reaction process. Al-
though this method has been not applied to wastewater treatment at
low temperature, utilizing bio-electrochemical technology will always
be an attractive alternative because of less influence by low tempera-
ture. In a modified A2O system embedding electrolysis treating munici-
pal wastewater, the removal efficiencies of TN and TP increased by
14.35% and 21.69%, respectively (Gong et al., 2018). These results indi-
cated that A2O coupling electrolysis was an effective way to strengthen
the performance for treatment of municipal wastewater. In another A2O
embedding microbial fuel cell (MFC) treating real sewage, the average
removal efficiencies of COD, TN and TP increased by 15.9%, 9.3% and
1.4%, respectively, implying that embedding MFC in the A2O wastewater
treatment process could enhance pollutants removal (Xie et al., 2014).
Wei et al. (2012) studied an electrically enhanced membrane bioreactor
(EMBR) at room temperature (20 ± 2 °C) with a synthetic feed and at
10 °C with real sewage and found that EMBR removed N99% of NH+ 4 -
N, N95% of dissolved COD and 90% of PO3− 4 -P, implying the potential
for application of this system treating domestic wastewater under
cold climatic conditions. An experiment to investigate the retrofit ability
of removing soluble TP and soluble COD from municipal wastewater
through electrocoagulation technology also demonstrated that superior
performance could be achieved, with phosphorus and soluble COD re-
moval of N99% (b0.2 mg/L) and 75% (b10 mg/L), respectively (Nguyen
et al., 2014a). These findings indicated that this method could be used
in existing municipal WWTPs to enhance pollutants removal under
low temperature. However, these applications mainly focused on lab-
scale or pilot-scale, and therefore full-scale application for improving
municipal wastewater treatment at low temperature would have po-
tential advantages because of the stable electrochemical process.
Microalgae have attracted considerable attention in recent years be-
cause of their photosynthetic functions and efficient nutrient removal.
With the growing concerns on microalgae, extensive studies are being
conducted to apply microalgae to wastewater treatment. Microalgae-
bacterial process has been regarded as an environmental friendly alter-
native for the treatment of domestic wastewater. The first application of
this technology was implemented in the 1950s in California for the
treatment of domestic wastewater. Moreover, microalgae have been
shown to effectively take up nitrogen and phosphorus from wastewater
with high removal efficiency (80%–100%) (Gonçalves et al., 2017).
Therefore, microalgae can be easily incorporated into advanced waste-
water treatment processes to improve nitrogen and phosphorus re-
moval. Furthermore, symbiotic interactions can be established
between microalgae and bacteria, which is central to enhancement of
biological nutrient removal during wastewater treatment processes. In
an algal-bacterial biofilm bioreactor treating domestic wastewater, the
average removal efficiencies of carbon, nitrogen and phosphorus were
91%, 70% and 85%, respectively (Posadas et al., 2013). Su et al. (2011)
studied an algal-bacterial culture treating municipal wastewater in a
stirred tank photobioreactor and found the average removal efficiencies
of COD, TKN and phosphate of 98.2, 88.3% and 64.8%, respectively. An
evaluation and simulation for microalgae introduction in WWTPs
showed that the microalgae-activated sludge process could reduce en-
ergy consumption and CO2 emissions, but would require large land
areas (Nordlander et al., 2017). Moreover, low temperature affects the
growth rate of microalgae and biomass production (Delgadillo-
Mirquez et al., 2016). Microalgae-bacterial process has rarely been re-
ported to improve contaminants removal from low temperature waste-
water. Therefore, there remains a long way to go for its application.
4. Future directions to address low temperature wastewater
Herein, existing strategies for improving pollutants removal from
municipal/domestic wastewater under low temperature are summa-
rized. However, further studies are still required to obtain satisfactory
wastewater treatment performance at low temperature. Specific steps
that need to be taken are outlined below.
1) Develop efficient bioaugmentation technology
Bioaugmentation has been considered as a useful strategy for im-
proving and maintaining the performance of municipal/domestic
wastewater treatment at low temperature. Therefore, an important di-
rection concerning bioaugmentation technology is screening, enriching
and utilizing cold-adapted bacteria with high removal efficiencies.
However, the loss of cold-adapted communities from wastewater treat-
ment systems still exist during long-term operation. More information
should also focus on how to effectively implement bioaugmentation
methods.
2) Exploit new process/technology configurations
New process/technology configurations appear to be attractive al-
ternatives to existing facilities to intensify the performance of wastewa-
ter treatment at low temperature. Each process/technology has specific
characteristics and advantages. Process configurations can take full ad-
vantage of two or more existing methods/techniques, which will be
very effective for improving the performance of low temperature
wastewater. For example, coupling A2O with BAF has been proved to
be an effective method for enhanced nitrogen and phosphorus removal
at low temperature (Wang et al., 2011). A novel hybrid treatment sys-
tem combining a rotating hanging media bioreactor and submerged
MBR with electrocoagulation to treat municipal wastewater also
showed higher removal efficiency (Nguyen et al., 2014b). Therefore,
new process configurations may be widely applied for enhanced treat-
ment of low temperature wastewater in the future.
3) Explore novel process pathways
Novel process pathways referring to wastewater treatment are ex-
plored more in depth. Many studies have focused on PN, anaerobic am-
monium oxidation, SND, heterotrophic nitrification and aerobic
denitrification, and denitrifying phosphorus removal. However, most
of these technologies remain in a lab-scale or pilot-scale, and there is
still a long way to go for full-scale municipal/domestic wastewater
treatment applications at low temperature. Therefore, future studies
should be directed on exploiting these novel technologies, which are
very important to improving process performance at low temperature.
4) Deeply study microbial community structure
 H. Zhou et al. / Science of the Total Environment 643 (2018) 225–237
Considering that biological wastewater treatment is a microbial-
ecological driven process, exploration of microbial community dynam-
ics under low temperature is necessary to understand process perfor-
mance. However, there are few studies focusing on the mechanisms of
microbial community variations in response to low temperature. Be-
sides the bacterial community, archaeal and fungal communities have
been reported to play a major role in biological wastewater treatment
systems. Indeed, significant numbers of ammonia oxidation archaea
(AOA) have been found in municipal WWTPs, implying that AOA
might play a role in autotrophic ammonia oxidation involved in nitro-
gen removal from wastewater treatment systems (Limpiyakorn et al.,
2011). Therefore, future studies should focus on deeply revealing the in-
ternal mechanisms between changes in microbial community structure
and process performance under low temperature conditions.
5) Explore enzyme functions of key groups of organisms
Enzymes are catalysts of biochemical reaction processes, and micro-
bial metabolism highly depends on enzyme functions in biological
wastewater treatment systems. Low temperature can decrease enzyme
activity, leading to poor contaminants removal. Therefore, future stud-
ies should focus on mechanisms of enzyme expression, variations in en-
zyme activities and regulation of enzyme functions, referring to key
groups of wastewater treatment at low temperature.
5. Conclusion
Low wastewater temperature affects the physiological characteris-
tics, growth rate and activity of microorganisms, microbial community
structure and sludge settleability, which can lead to deterioration of
process performance. Here, strategies for enhanced treatment of munic-
ipal/domestic wastewater at low temperature are summarized. It can be
concluded that operational parameters regulation (HRT, SRT and DO),
bioaugmentation (directly adding pure strains/mixed cultures and im-
mobilization technique), biofilm technology (hybrid sludge/biofilm sys-
tem, MBBR and BAF), chemical phosphorus precipitation and
application of novel process technologies (MBR, AGS, PN, PN/A, SND,
heterotrophic nitrification and aerobic denitrification, denitrifying
phosphorus removal, bio-electrochemical and microalgae-bacteria)
are effective methods to improve and maintain the performance of
existing municipal wastewater treatment systems under low tempera-
ture. In the future, novel process configurations and process pathways
will provide attractive alternatives for performance intensifications of
low temperature wastewater even if further studies remain required.
Acknowledgments
This work was funded by the National Natural Science Foundation of
China (No. 51478138).
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