Science of the Total Environment 874 (2023) 162353

Contents lists available at ScienceDirect

Science of the Total Environment

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

Microbiological risks increased by ammonia-oxidizing bacteria under global

warming: The neglected issue in chloraminated drinking water
distribution system
Shikan Zheng, Jianguo Li, Chengsong Ye, Xuanxuan Xian, Mingbao Feng, Xin Yu
⁎
College of the Environment and Ecology, Xiamen University, Xiamen 361102, 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

• High temperatures continue to rise rapidly

under global warming.
• Outbreaks of waterborne diseases associ-
ated with high temperatures are summa-
rized.
• High temperatures promote AOB growth
in chloraminated pipe networks are dis-
cussed.
• Microbiological risks increased by AOB-
driven nitrification are reviewed.
• Further studies to understand and address
microbiological risks are warranted.

A R T I C L E I N F O A B S T R A C T

Editor: Damià Barceló A rising outbreak of waterborne diseases caused by global warming requires higher microbial stability in the drinking
water distribution system (DWDS). Chloramine disinfection is gaining popularity in this context due to its good persis-
Keywords: tent stability and fewer disinfection byproducts. However, the microbiological risks may be significantly magnified by
High temperatures ammonia-oxidizing bacteria (AOB) in distribution systems during global warming, which is rarely noticed. Hence, this
Ammonia-oxidizing bacteria
work mainly focuses on AOB to explore its impact on water quality biosafety in the context of global warming. Re-
Microbiological risks
Chloramine
search indicates that global warming-induced high temperatures can directly or indirectly promote the growth of
AOB, thus leading to nitrification. Further, its metabolites or cellular residues can be used as substrates for the growth
of heterotrophic bacteria (e.g., waterborne pathogens). Thus, biofilm may be more persistent in the pipelines due to
the presence of AOB. Breakpoint chlorination is usually applied to control such situations. However, switching be-
tween this strategy and chloramine disinfection would result in even more severe nitrification and other adverse ef-
fects. Based on the elevated microbiological risks in DWDS, the following aspects should be paid attention to in
future research: (1) to understand the response of nitrifying bacteria to high temperatures and the possible association
between AOB and pathogenic growth, (2) to reveal the mechanisms of AOB-mediated biofilm formation under high-
temperature stress, and (3) to develop new technologies to prevent and control the occurrence of nitrification in drink-
ing water distribution system.

⁎ Corresponding author.
E-mail address: xyu@xmu.edu.cn (X. Yu).

http://dx.doi.org/10.1016/j.scitotenv.2023.162353
Received 21 December 2022; Received in revised form 14 February 2023; Accepted 16 February 2023
Available online 22 February 2023
0048-9697/© 2023 Elsevier B.V. All rights reserved.
S. Zheng et al. Science of the Total Environment 874 (2023) 162353

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
2. Global warming: An essential factor affecting the safety of drinking water . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
2.1. Global warming . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
2.2. Global warming causes drinking water biosafety issues . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
3. Nitrification: More than significant in the water supply system . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
3.1. Nitrification . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
3.2. Nitrification occurs in DWDS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
4. Global warming accelerates the AOB growth . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
4.1. Direct promotion. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
4.1.1. AOB growth rate . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
4.1.2. Chemical chloramine decay . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
4.1.3. Microbiological chloramine decay . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
4.2. Indirect promotion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
4.2.1. Organic substance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
4.2.2. DO . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
4.2.3. pH. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
4.2.4. Corrosion products. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
5. Adverse effects of AOB-driven nitrification on biosafety . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
5.1. Promoted bacteria growth. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
5.2. Accelerate biofilm development . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
5.3. Shape microbial community . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
6. Conclusions and outlook . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
CRediT authorship contribution statement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
Data availability . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
Declaration of competing interest . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8

1. Introduction
Global warming is indisputable and poses one of the most significant
challenges for human beings since the industrial revolution. According to
the Intergovernmental Panel on Climate Change (IPCC), globally averaged
surface temperature increased by 0.85 °C from 1880 to 2012. It is projected
to rise by 1.4 to 5.8 °C from 1990 to 2100 (McCarthy et al., 2001; Stocker,
2014). With the increase in global mean temperatures, hot extremes be-
come more frequent, more intense, and longer lasting (Bragazza et al.,
2016; Meehl and Tebaldi, 2004). Recent evidence suggests that outbreaks
of waterborne diseases are positively associated with extreme heat events
(Fouladkhah et al., 2019; Guzman Herrador et al., 2015). For example, in
1997–1998, the average ambient temperature in Lima was 5 °C above nor-
mal, and the number of daily hospital admissions due to diarrhea increased
by 200 % over the same period (Checkley et al., 2000). Hence, it is logical to
mention that global warming may cause drinking water issues.
Nowadays, rapid urbanization is usually accompanied by the emer-
gence of large cities and megacities (Henderson and Wang, 2007). In
2018, 33 megacities with populations over 10 million worldwide were
projected to increase to 43 by 2030 (Economic, U.D.o., Division, S.A.P.,
2018). Meanwhile, growing demands have resulted in the expansion of
the water supply system (He et al., 2021). Data provided by Global
Economic Data, Indicators, Charts & Forecasts show that the total length
of a pipe network in Shanghai has reached 39,689.970 km in 2021
(https://www.ceicdata.com/pt). So long-term stability has become a
major requirement for disinfectants in distributed pipelines. Because
of an effective residual and fewer disinfection byproducts formation
due to its less reactivity, chloramine can remarkably maintain in long-
distance water distribution systems (Lee et al., 2011b; Zhang et al.,
2009). Hence, chloramination as secondary disinfection is becoming
more and more popular.
Unfortunately, chloramines trigger undesirable nitrification that
attracts world concerns (Hossain et al., 2022b; Zhang et al., 2009). Nitrifi-
cation is carried out mainly by nitrifying bacteria, including ammonia-
oxidizing bacteria (AOB) and nitrite-oxidizing bacteria (NOB). The former
can consume free ammonia obtained from the formation and decay of
chloramines as substrate (Pressman et al., 2012). In turn, the decay of
chloramine can also be accelerated by them. Besides, their metabolites or
cellular residues, both of which are biodegradable organic matter, can be
released as available substrates for heterotrophic bacteria growth. A com-
plicated microbial community can ultimately grow from scratch in the
drinking water distribution system (DWDS) (Keshvardoust et al., 2019;
Okabe et al., 2005; Sathasivan et al., 2008). The enhanced temperature
will accelerate the monochloramine decay under global climate change,
leading to the release of more free ammonia. Under such conditions, the
growth of AOB can be promoted in the two ways mentioned above. Mean-
while, the heterotrophic bacteria growth caused by AOB will also be signif-
icantly amplified. Hence, this work mainly focuses on non-pathogenic
microorganisms AOB to explore its impact on water quality biosafety in
the context of global warming.
2. Global warming: An essential factor affecting the safety of drinking
water
2.1. Global warming
A simple change in air temperature is shown in Fig. S1 to illustrate
global warming over the past years. Compared to 1980–1985, the global
surface temperature averaged over 2017–2022 is likely higher by about
0.74 °C. Further analysis found that the average maximum air temperature
in 2021 reached 18.0 °C, warming 2.0 °C up from 1980, and the average
temperature rose 0.5 °C over the same period (Fig. S1c and d). It means
the high temperature continues to warm more rapidly under global
warming. In fact, climate warming adversely impacts human society and
natural systems, primarily related to extreme events (Zhang and Zhou,
2020). World Weather Attribution (WWA) found that the global surface
temperature was 1.2 °C higher than in pre-industrial times, making extreme
heatwaves likely to increase at least 150-fold (Schiermeier, 2021). Global
warming-induced hot weather increase will be ordinary for future climate.

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2.2. Global warming causes drinking water biosafety issues 3.1. Nitrification

Microbiological safety is essential for drinking water quality (van der
Kooij et al., 1999). However, 58 % of known human pathogenic diseases
can be exacerbated by climate change, in which rising temperatures greatly
threaten disease outbreaks (Mora et al., 2022). Studies have revealed a pos-
itive correlation between air temperature and water temperature (Mooij
et al., 2008; Zhao et al., 2019). For every 1.0 °C increase in air temperature,
the surface water temperature increased by about 0.6–0.8 °C (Morrill et al.,
2005). Although the increase rate of temperature is not large, the increment
in temperature cannot be ignored in the statistical sense. By 2050, the esti-
mated changes in annual average levels of water temperature are 2.0 °C
higher than the baseline value as a consequence of global warming
(Cromwell et al., 2007). Besides, human water consumption is predicted
to will further increase to 5235 km3 yr−1 by 2025 (Jenerette and Larsen,
2006). Considering the water supply's scale and amount, the temperature
change will significantly impact water quality in DWDS. In fact, various
water quality parameters were associated with the elevated temperature,
such as chlorine decay, total trihalomethane (TTHM), formation, bacterial
activity, and so on (Gunkel et al., 2022). In general, every 1 °C increase in
water temperature will accelerate the biochemical reaction by 10–20 %.
To understand this process more clearly, the models for estimating the
effects of water temperature changes on water quality parameters are
shown in Table 1. Besides, bacteria tend to be more optimal for growth at
warm temperatures, particularly opportunistic pathogens (Hossain et al.,
2022a; Vital et al., 2008). The outbreaks of waterborne diseases associated
with rising temperatures are summarized in Table 2. It can be seen that
elevated temperatures and outbreaks of waterborne diseases are not
accidental events that occur around the world. However, <40 % of
countries have established health surveillance systems for climate-
sensitive diseases, including weather and climate information (World
Health Organization, 2021).
Due to the acute and immediate nature of the waterborne microbial
disease, the biosafety of drinking water should be emphasized during
global warming. Unfortunately, the issue can also be caused by AOB,
which is otherwise rarely noticed. Therefore, this work will describe
this issue in detail below.
3. Nitrification: More than significant in the water supply system
According to the American Water Works Association (AWWA)
survey, approximately 27.6 % of water utilities in the United States
employed chloramine for secondary disinfection in 2017 (AWWA
Disinfection Committee, 2018). However, chloramines along with nitri-
fication might lead to adverse results, such as increased NO−
2 -N, hetero-
trophic bacteria growth, pipe network corrosion, and so on (Hossain
et al., 2022b). A survey conducted in 2017 showed that 34.5 % of utili-
ties did not consider converting chlorine to chloramine due to concerns
about nitrification (Bradley et al., 2020).
Based on the classical water treatment theory, nitrification is a two-step
microbial process carried out by chemoautotrophic bacteria. In the first
stage, ammonium, as an electron donor, which is oxidized to nitrite by
AOB (Yan et al., 2019). In the second stage, oxygen is the electron acceptor,
and nitrite is further oxidized to nitrate by NOB to complete the nitrification
(Wilczak et al., 1996). The approximate equations are given below (Zhang
et al., 2009):
NHþ −
4 þ 1:9O2 þ 0:069CO2 þ 0:0172HCO3 → 0:0172C5 H7 O2 N ð1Þ
þ 0:983NO− þ
2 þ 0:966H2 O þ 1:97H
NO− þ −
2 þ 0:00875NH4 þ 0:035CO2 þ 0:00875HCO3 þ 0:456O2 ð2Þ
þ 0:00875H2 O → 0:00875C5 H7 O2 N þ 1:0NO−
3
Nitrification, as a central part of the nitrogen cycle, is widespread in the
natural water environment, such as surface water, wastewater, marine, and
so on (Joye and Hollibaugh, 1995; Miner, 2006; Yan et al., 2019). As shown
above, the growth of nitrifying bacteria is mostly independent of ammo-
nium concentration in the environment (Miner, 2006). Therefore, nitrifica-
tion seems more difficult due to the distribution system's limitation of free
ammonia. Interestingly, frequent nitrification in chloraminated DWDS has
been reported on a global scale (Bradley et al., 2020).
3.2. Nitrification occurs in DWDS
In fact, the substrate limit concentration for nitrifying bacteria growth
under oligotrophic conditions is one order of magnitude lower than in
wastewater treatment. For instance, as the most abundant AOB in the distri-
bution system, the development of Nitrosomonas oligotropha was limited
only when free ammonia was lower than 0.1 mg N/L or even less (Miner,
2006; Sarker et al., 2013). Furthermore, chloramine decay provides a criti-
cal approach to increasing ammonia in DWDS (Table 3). According to the
breakpoint chlorination curve, utilities typically adopt Cl2/N mass ratios
ranging from 3:1 to 5:1 to ensure disinfection efficiency. It is noteworthy
that when Cl2/N reaches 3:1, 2 mg/L of chloramines can release
0.28 mg/L of free ammonia (Wahman and Pressman, 2014).
Nitrification occurs in DWDS, where the growth of nitrifying bacteria
exceeds their inactivation by disinfection (Wahman and Pressman, 2014).
Currently, approximately 30–63 % of utilities in the US that use chlora-
mines as secondary disinfection have experienced different degrees of
nitrification (Maestre et al., 2016; Seidel et al., 2005). Notably, once nitrifi-
cation starts, even chloramine at a dose of up to 8 mg/L was difficult to con-
trol it (Sarker et al., 2018; Skadsen, 1993). Hence, several water quality
parameters can be used as early warning indicators in utilities. Biological
and chemical indicators commonly used for monitoring are shown in
Table 4, and water utilities can choose freely according to the operating
conditions. Currently, the only existence of AOB without NO− 2 -N oxidizers

Table 1
Models for evaluating the effect of water temperature on drinking water quality parameters.
Water quality Equation Note Reference(s)
parameters

Chlorine bulk decay rate kb ¼ F  TOC  e−RðTþ273Þ

E
kb is the bulk decay rate (h−1or day−1) F is a frequency factor, E is the (Lai and Dzombak, 2021)
activation energy (J/mol), and R is the ideal gas constant as 8.31 J/(mol·K)
TTHM formation TTHM = K ∙ C0a ∙ Tb ∙ TOCC ∙ pHd ∙ Bre C0 is the initial chlorine concentration and T is the temperature (°C) of (Lai and Dzombak, 2021)
treated water. TOC, pH, and Br (bromide concentration) are measurements
for the water source, and a to e and k are constants determined by model
fitting of measurements
1
Larson ratio ðCl− þSO2− þ 2
4 þNa Þ
LRM = modified Larson ratio, temperature T (°C), hydraulic retention time (Imran et al., 2005)
LRM ¼ Alk ð25
T
ÞHRT
[HRT (days)]. alkalinity [Alk (mg/L as CaCO3)]
Bacterial activity T −T 2 Act(T) is bacterial activity at temperature T (°C). Toptis the optimal (Lai and Dzombak, 2021)
ActðTÞ ¼ ActðT opt Þ expð−ðT opt
opt
−T i Þ Þ
temperature for the bacteria community, and Ti is a shape parameter.
Topt = 40 -(20 - T)/2 and
Ti = 18 - (20 - T)/2 when seasonal changes of temperature are considered

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Table 2
Selected outbreaks of waterborne infections associated with global warming in the world.
Continent Country/Region Study period Waterborne disease under study Waterborne disease Data source References

Global 1991–2008 Drinking water related waterborne Database developed by the Global (Guzman Herrador et al.,
disease outbreaks Infectious Disease Epidemiology Network 2015; Yang et al., 2012)
(GIDEON)
Global 1998–2009 Campylobacter cases Publish papers (Semenza et al., 2012)
Global 1966–2008 Cryptosporidiosis cases Publish papers (Jagai et al., 2009)
South America Lima, Peru 1997–1998 Diarrhea cases Hospital (Checkley et al., 2000)
Oceania New Zealand 1997–2008 Cryptosporidiosis cases National Notifiable Disease Surveillance (Lal et al., 2013)
system
Oceania New Zealand 1997–2006 Cryptosporidiosis and Giardiasis cases Surveillance data at the national level (Britton et al., 2010; Guzman
Herrador et al., 2015)
Europe England and Wales 1990–1999 Campylobacter cases Surveillance data at the national level (Guzman Herrador et al.,
2015; Louis et al., 2005)
Europe Republic of Ireland 2005–2012 Vero cytotoxin-producing Escherichia Surveillance data at national level (O'Dwyer et al., 2016)
coli(VTE)
Europe Denmark, Finland, 2000–2015 Campylobacter cases Surveillance data at national level (Kuhn et al., 2020)
Norway, and Sweden
North America Canada 1975–2001 Drinking water-related waterborne Published compilation at the national level (Thomas et al., 2006)
disease outbreaks
North America United States 2013 Naegleria fowleri The Louisiana Department of Health and (Cope et al., 2015)
Hospitals(DHH)
North America United States 1991–1992 Naegleria fowleri Public health agencies (Moore et al., 1993)
North America Philadelphia, 1994–2007 Campylobacteriosis cases Surveillance data at national level (Guzman Herrador et al.,
United States 2015; White et al., 2009)
North America Nunatsiavut, Canada 2005–2008 Gastrointestinal illness-related visits Administrative records (Guzman Herrador et al.,
2015; Harper et al., 2011)
South Africa KwaZulu-Natal 2000–2001 Cholera Global Task Force on Cholera Control, (Mendelsohn and
WHO Dawson, 2008)
Asia Dhaka, Bangladesh 1996–2002 Weekly number of patients visiting a Administrative records (Guzman Herrador et al.,
hospital due to non-cholera diarrhea 2015; Hashizume et al., 2007)
Asia Kon Tum, Vietnam 1999–2013 Shigellosis cases Administrative records (Lee et al., 2017)
Asia Guizhou, China 1984–2007 Typhoid and paratyphoid fever cases Surveillance data at national level (Guzman Herrador et al., 2015)
Asia Can Tho, Vietnam 2004–2011 Diarrhea cases The Preventive Medicine Centre (Phung et al., 2015)
(CTPMC)
Asia Azerbaijan 1970–1998 Cholera Surveillance data at national level (Gurbanov et al., 2011)
Asia and Latin -Northern India and 1875–1900 Cholera cases Reports from the Government and (Guzman Herrador et al.,
America Pakistan previously published data 2015; Jutla et al., 2013)
- Haiti
Oceania and Pacific Islands 1978–1998, with Diarrhea cases Surveillance data at national level (Guzman Herrador et al.,
Australia two missing years 2015; Singh et al., 2001)
Oceania and Brisbane, Australia 1996–2004 Cryptosporidiosis cases Surveillance data from the regional level (Guzman Herrador et al.,
Australia 2015; Hu et al., 2007)

Literature review (n = 23).

is the most common problem faced by utilities (Skadsen, 2002). Hence, this
work mainly focuses on the AOB in drinking water distribution systems.
4. Global warming accelerates the AOB growth
According to the surveys, nitrification occurred in 30 % of utilities that
used chloramines as a secondary disinfectant in 2005 and by 2017 this
number had reached 67 % (AWWA Disinfection Committee, 2018; Seidel
Table 3
Chemical reactions involving the release of ammonia in chloramine decay. (Based
on (Hossain et al., 2022a; Hossain et al., 2022b)).
Reactions Reaction description
et al., 2005). Elevated temperature can accelerate monochloramine decay
in theory, facilitating the release of free ammonia and then accelerating
the growth of AOB. On the other hand, together with these surveys, control-
ling nitrification is the primary reason for converting chloramine to free
chlorine in water utilities. In 2005, about 21 % of respondents switched
to free chlorine in the summer, and the proportion rose to 38 % in 2017.
The increasing trend shows that summer high temperature induced by cli-
mate change is conducive to nitrification and needs to be prevented. The in-
creased severity of hot weather conditions under global warming will not
only impact water temperature but will also be accompanied by changes
in water quality parameters such as organic matter, dissolved oxygen
(DO), pH, etc. Such conditions can directly or indirectly promote AOB
growth in DWDS, thus leading to nitrification.

3 NH2Cl → N2 + NH3 + 3 Cl− + 3H+ Chloramine 4.1. Direct promotion

C5H7O2N + 10 NH2Cl + 9 H2O→4
CO2 + HCO3− + 11 NH4++10 Cl−
NH2Cl + NO− −
2 + H2O → NH3 + NO3 + HCl
−
NH2Cl + 2H++2 Fe2+ → 2 Fe3++NH+
4 +Cl
NH2Cl + Cu(s) + OH− ⇄CuO(s) + Cl− + NH3
3NH2Cl + Br− → N2 + NH3 + 3Cl− + 3H++Br−
auto-decomposition
Natural organic matter
(NOM) oxidation
by chloramine
Nitrite oxidation
by chloramine
The reaction of chloramine
with pipe corrosion products
The reaction of chloramine
with pipe corrosion products
The reaction of chloramine
with bromide
4.1.1. AOB growth rate
Temperature is one of the most influential environmental factors for mi-
crobial growth (Lee et al., 2011a). AOB has adapted to survival in a wide
temperature range of 4–45 °C, while the optimum growth temperature is
25–30 °C (Zhang et al., 2009). Data from USEPA indicated that
Nitrosomonas's maximum specific growth rate was doubled for every
10 °C increase in temperature at 10–30 °C (USEPA, 1993). Besides, ammo-
nia utilization and biomass yield also increase coupled with temperature
(Groeneweg et al., 1994; Zhang et al., 2009). Furthermore, the efficacy of

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Table 4
Change of water quality characteristics of distribution system during the early warning.
Monitoring parameters Usefulness Typical range Symptoms Alert leave Reference

Water temperature Very useful 5–35 °C Increase 15 °C (Vikesland et al., 2001; Wilczak et al., 1996)
Total chlorine Very useful 1.0–3.0 mg/L Decrease 1.8 mg/L (Miner, 2006)
Chloramine residual Very useful 1.0–2.0 mg/L Decrease 0.6 mg/L (Miner, 2006; Wolfe et al., 1990)
Free ammonia Very useful 0.01–0.05 mg/L Initially increase then decrease 0.1 mg/L (Miner, 2006)
Nitrite-N Very useful 0.010 mg/L Increase 0.010 mg/L (Miner, 2006; Wahman and Pressman, 2014)
pH Useful Normal Decrease Less than target (Yang et al., 2007; Miner, 2006)
Heterotrophic bacterial growth Useful 100 CFU/mL Increase 350 CFU/mL (Vikesland et al., 2001; Wolfe et al., 1990)
Microbiological decay factor Very useful < 0.2 Increase 0.3 (Hossain et al., 2022b)

Table 5
Temperature dependency of important reaction rates and equilibrium constants. (Based on (Wahman and Pressman, 2014)).
Reaction Rate/equilibrium constant (T in Kelvin) Reference(s)

NH3+ HOCl→NH2Cl + H2O k1=2.37 × 1012e-1510/TM−1 h−1 (Morris and Isaac, 1983)
HOCl+NH2Cl → H2O + NHCl2 k3=1.08 × 109e-2010/TM−1 h−1 (Morris and Isaac, 1983)
NH2Cl + H2O → NH3 + HOCl k2=6.7 × 1011e-8800/Th−1 (Morris and Isaac, 1983)
NH2Cl + NH2Cl → NH3+ NHCl2 k5=kH[H+]+kHCO3[HCO− 3 ]+kH2CO3[H2CO3]
kH=3.78 × 1010e-2169/T M−2 h−1 (Vikesland et al., 2001)
kHCO3=1.5 × 1035e-22,144/TM−2 h−1 (Vikesland et al., 2001)
kH2CO3=2.95 × 1010e-4026/TM−2 h−1 (Vikesland et al., 2001)
H2O⇌OH− + H+ kW=10-(1.5×10−4T2-1.23×10−1T+37.3) (Snoeyink and Jenkins, 1980
H2CO3⇌HCO−3 + H
+
kH2CO3=10-(1.48×10−4T2-9.39×10−2T+21.2) (Snoeyink and Jenkins, 1980)
HCO-3⇌CO2−
3 + H+ kHCO3=10-(1.19×10−4T2-7.99×10−2T+23.6) (Snoeyink and Jenkins, 1980)
HOCl⇌H++OCl− kHOCl=10-(1.18×10−4T2-7.86×10−2T+20.5) (Morris, 1966)
4 ⇌H + NH3
NH+ +
kNH4=10-(1.03×10−4T2-9.21×10−2T+27.6) (Bates and Pinching, 1950)

chloramine for controlling nitrification was also correlated with tempera-
ture. Chick–Watson model has been applied to describe chloramine
inactivation under different temperatures. It suggested the inactivation
rate coefficient k were 0.0006 L/(mg·min), 0.009 L/(mg·min), 0.014 L/
(mg·min) at 8 °C, 26 °C, 35 °C, respectively (Zhang et al., 2021). Although
the inactivation of AOB can be accelerated with increasing temperature,
it is much slower than the growth rates (Wahman and Pressman, 2014).
Sarker et al. (2013) developed a model to describe the AOB biostability in
chloraminated water supply systems. The results showed that the μm/ kd
(the maximum specific growth rate of AOB over the rate constant of disin-
fectant inactivation) can be used to predict the onset of nitrification. The
values of Nitrosomonas europaea increased with temperature and reached
a maximum near 35 °C. Overall, even in the presence of chloramines, rising
water temperatures in actual drinking water distribution systems under
global warming may favor the growth of AOB.
4.1.2. Chemical chloramine decay
Maintaining adequate disinfection residue is a vital strategy to
control nitrification. However, the chloramine decay rate doubles with
every increase of 16 °C (Nguyen et al., 2012; Sathasivan et al., 2009).
Chloramine decay mainly includes chemical and biological processes. The
reactions between chloramine and NOM, halides, and other reduced
compounds like Fe2+ and Cu2+ and auto-decomposition leads to chemical
decay (Roy et al., 2020; Sathasivan et al., 2005). Studies showed that the
half-life of monochloramine at 35 °C and pH 7.5 is about 75 h, which is
four times that at 4 °C (Vikesland et al., 2001). In fact, the temperature
affected many reaction rates and equilibrium constants of the chemical
decay process (Table 5). For simplification, the formation rate of
dichloramine is the primarily limited reactions step to be considered in
the decay rate of chloramine (Vikesland et al., 2001). As can be seen,
elevated temperature can accelerate the dichloramine formation, thus
promoting monochloramine decay and providing more free ammonia for
AOB growth.
dependency on chloramine decay coefficients. Data showed that E/R values
of the chemical and biological decay coefficients were 3551 ± 705 K−1
and 6924 ± 700 K−1, respectively.
AOB is the primary driver of microbial chloramine decay (Hossain et al.,
2022a, 2022b; Sathasivan et al., 2005). N. europaea as a well-studied AOB
was adopted to describe the possible monochloramine loss pathways by
AOB (Fig. 1) (Krishna et al., 2012; Maestre et al., 2013; Maestre et al.,
2016; Vikesland et al., 2001; Wahman and Speitel, 2015; Wahman et al.,
2009): (i) consumed by the bacteria through inactivation reaction with
cellular components, (ii) N. europaea can promote chloramine hydrolysis
by utilizing the free NH3 released from monochloramine (NH2Cl); (iii)
NH3 was oxidized to hydroxylamine (NH2OH) by N. europaea using ammo-
nia monooxygenase (AMO), which further reacted abiotically with chlora-
mine; (iv) N. europaea using hydroxylamine oxidase (HAO) oxidized
NH2OH to NO− −
2 , and then NO2 reacted with NH2Cl; (v) soluble microbial
products can be released by N. europaea through growth and metabolism,
and then promoted the attenuation of monochloramine under catalysis.
(vi) NH2Cl was converted to NH2OH by N. europaea through cometabolism,
which accounted for 30 %–60 % of the total attenuation of
monochloramine. As previously shown, the temperature can facilitate the

4.1.3. Microbiological chloramine decay

Microbiological decay is dominant in chloramine loss in bulk water
(Sathasivan et al., 2005). The biological decay process is more vulnerable
to temperature than chemical decay. First-order decay coefficients E/R
were evaluated by Sathasivan et al. (2009), to explore the temperature Fig. 1. Chloramine decay process mediated by N. europaea.

5
S. Zheng et al. Science of the Total Environment 874 (2023) 162353

AOB growth, which may make the loss of chloramine more challenging to nitrite as an alternative electron acceptor in low oxygen or anoxic environ-
control in the face of global warming. ments (Kowalchuk and Stephen, 2001; Zhang et al., 2009).

4.2.3. pH
4.2. Indirect promotion
It is virtually certain that anthropogenic carbon dioxide (CO2) emission
is the primary driver of current global warming (Arias et al., 2021). Data
4.2.1. Organic substance
presented by Riedel (2019) showed that with every 1 °C increase in temper-
Source water quality is susceptible to climate change, which may lead to
ature, the pH of groundwater dropped by 0.02 due to CO2 accumulation.
changes in water quality of the pipe network and eventually promotes AOB
The response of pH to global warming can affect AOB growth in various
growth in DWDS (Fig. 2). With the increase in microbial activity and the de-
ways. First, free ammonia is the actual enzyme substrate for AOB growth,
crease in water level under global warming, organic matter accumulation in
which decreases with decreasing pH, indicating that higher pH is the poten-
freshwater was observed (Evans et al., 2006). Related studies predicted that
tial for nitrification (Eq. 3) (Yang et al., 2007). Besides, the inactivation of
for every 1 °C increase in temperature, dissolved organic matter of surface
AOB is also sensitive to pH. Oldenburg et al. (2002) explored the inactiva-
water increased by about 15.2–30.3 % (Valdivia-Garcia et al., 2019). More-
tion rates of Nitrosomonas europaea by chloramine at different pH. The
over, the low molecular weight (MW) organic is dominant because of the
results showed that the inactivation rate coefficient k decreased from
rapid microbial biodegradation at high temperatures. Research shows its
2.5 × 10−3 L/(mg Cl2·min) to 2.4 × 10−4 L/(mg Cl2·min) with the pH in-
removal efficiencies in the coagulation/sedimentation/rapid sand filtration
creased from 7 to 9. This result was consistent with Zhang et al. (2021),
process are less than half that of high MW organic matter (So et al., 2017).
which ascribed to the higher HOCl proportion of total chloramine in
Furthermore, more severe algal blooms have been observed as eutrophica-
lower pH. Moreover, pH impacts the form and the decay of chloramines
tion intensified due to the decomposition rate increases in phosphorus re-
(Wolfe et al., 1984; Vikesland et al., 2001). Strictly speaking, chloramine
lease in extreme heat events (Zhan et al., 2022). The release of algal
mainly includes monochloramine, dichloramine, and trichloramine. Yet,
organic matter (AOM) and taste and odor compounds increased due to
monochloramine was the dominant chloramine species in drinking water
cell lysis during water treatment (Xian et al., 2022). AOM is rich in protein-
treatment due to its stability and fewer DBPs production, and it prefers to
aceous material, making it more difficult to remove (Ritson et al., 2014). Al-
form at the pH range of 7–9 (Wilczak et al., 1996; Vikesland et al., 2001).
though the reactivity of chloramines is lower than chlorine, it can still react
Meanwhile, the decay rate of chloramine under low pH conditions is accel-
with NOM (Hossain et al., 2022a). The process is mainly divided into two
erated. It suggested that lower pH was more likely to cause nitrification due
pathways: (i) NOM direct reaction with chloramine; (ii) NOM especially
to less chloramine residue and more ammonia concentration (Valentine,
organic nitrogen compounds reaction with free chlorine from chloramine
1998). Given these different effects of pH, the nitrification response to pH
hydrolysis (Duirk et al., 2005; Hossain et al., 2022a). Therefore, the in-
is complex. It is well accepted that maintaining higher pH is generally
creased organic matter in water resources would result in higher consump-
regarded as a strategy to prevent nitrification in DWDS, which seems
tion of chloramine in subsequent treatment. Under such conditions, both
more difficult to achieve under global warming.
nitrifiers and heterotrophic bacteria can survive under lower disinfectant
residue (Bradley et al., 2020; Hossain et al., 2022a). NHþ þ
4 þ H2 O ! NH3 þ H3 O (3)

4.2.2. DO
Higher temperatures can also accelerate the reduction of DO concentra-
tion in water. On the one hand, DO saturation constants decreased by 4 %
for every 1 °C increased in temperature. On the other hand, increased
biological oxygen demand further reduces DO in water (Ozaki et al.,
2003; Riedel, 2019). As aerobic bacteria, the oxygen half-saturation
constant of AOB in pure and activated sludge culture was about
0.3–1.3 mg/L (Zhang et al., 2009). Generally, DO in water varies with tem-
perature commonly between 7 and 9 mg/L, which is sufficient for AOB
growth (Hu et al., 2021). Even if biofilm or corrosion products may provide
an anaerobic micro-environment, AOB can still survive by using nitrate or
4.2.4. Corrosion products
Previous studies have demonstrated that temperature increases are ac-
companied by changes in several key corrosion parameters, like biological
activity, DO, solution properties, diffusion rates, and so on (McNeill and
Edwards, 2001). Generally, the elevated temperature of the aquatic envi-
ronment will favor pipeline corrosion.
Copper and iron as pipe materials are widely used in drinking water
pipe systems worldwide (Zhang et al., 2002; Sarin et al., 2004). For copper
pipes, once corrosion occurs, Cu2+ is more easily released into the water
(Fig. 2) (Sarker et al., 2018). Additionally, as a common algicide, CuSO4

Fig. 2. Effects of global warming on nitrification in DWDS.

6
S. Zheng et al.
can be used to mitigate the algal bloom induced by high temperatures, but
inappropriate use may also lead to the accumulation of Cu2+ in bulk water
(Xian et al., 2022). Although the elevated level of Cu2+ can inhibit nitrifi-
cation to some extent, it was also the limiting element in drinking water
safety standards (Sarker et al., 2018). In this case, orthophosphate is
adopted to alleviate pipeline corrosion. In turn, the reduction in copper
leaching also reduces the toxicity of excess copper to nitrifying bacteria,
which increases nitrifying bacteria in the system (Zhang et al., 2009). For
iron pipes, DO was the key electron acceptor for the corrosion of iron
metal, an iron release increased with the DO concentration decreased
(Sarin et al., 2004). It has been confirmed that Fe2+ is the primary form re-
leased from corroded pipes (Sarin et al., 2004; McNeill and Edwards, 2001).
Based on Table 3, Fe2+ was projected to involve chemical chloramine
decay, thus promoting nitrification.
5. Adverse effects of AOB-driven nitrification on biosafety
AOB is the main driver of nitrification, which accelerated growth
facilitates nitrification. Nitrification is commonly accompanied by a series
of adverse effects, such as promoting bacteria growth, accelerating biofilm
development, and shaping the microbial community, which ultimately re-
sults in increased microbial risks in DWDS.
5.1. Promoted bacteria growth
Typically, the ability of microbial regrowth mainly depends on the con-
tent of the disinfection residues and the concentrations of substrate
required for growth (Liu et al., 2002; Srinivasan and Harrington, 2007).
Nitrification plays a vital role in bacteria regrowth by satisfying both condi-
tions. Rapid decay of chloramines is usually observed after the onset of ni-
trification (Zhang and DiGiano, 2002). A study reported that chloramines
in finished-water reservoirs were lost from 1.4 mg/L to 0.8 mg/L in one
day during nitrification (Wolfe et al., 1988). In a 2007 survey, more than
half of the utilities stated that their system reported chlorine depletion asso-
ciated with nitrification (AWWA Disinfection Committee, 2018). Besides,
metabolites or cellular residues of AOB can be used as substrates for the
growth of heterotrophic bacteria (Zhang et al., 2009). Okabe et al. (2005)
confirmed this process using microautoradiography combined with fluores-
cence in situ hybridization. Specifically, the 14C transfer from the nitrifying
bacteria to heterotrophic bacteria was observed to demonstrate that
heterotrophic bacteria preferentially utilize substrates related to nitrifying
bacterial products. Indeed, researchers have discovered the growth of
heterotrophic bacteria caused by nitrification as early as 1985 (Wolfe
et al., 1988).
Hence, we analyzed the heterotrophic bacteria growth during nitrifica-
tion in DWDS (Fig. 3a). According to standards for drinking water quality in
China (GB5749–2006), the limit of heterotrophic plate count (HPC) in
drinking water is 100 CFU/mL. As can be seen, most of the HPC detected
Fig. 3. (a)The HPC level and (b) the relationship between AOB and HPC (the data were obtained and replotted from (Park et al., 2013; Regan et al., 2002; Wolfe et al., 1990;
Yang et al., 2008)) during nitrification in DWDS.
7
Science of the Total Environment 874 (2023) 162353
were well above drinking water standards; some even exceeded 30 times.
The relationship between AOB and HPC in previous studies is further ana-
lyzed in Fig. 3bIt indicates that there is a strong correlation between HPC
and AOB.
In recent years, it has been realized that chloramine loss and nitrifying
conditions may affect the diversity of putative pathogenic bacteria in
DWDS. Pathogenic microorganisms such as Legionella, Mycobacteria, Pseu-
domonas, and amoebas were all detected in chloramine disinfection systems
(Krishna et al., 2021; Waak et al., 2019). Krishna et al. (2021) compared the
sequencing results of water samples to the full-length 16S rRNA gene
sequences of fifty-four pathogenic bacterial species obtained from the
National Centre for Biotechnology Information database. The results
showed that 31 putative pathogens were detected in the laboratory, and
full-scale DWDS when disinfectant residues ranged from 0.03 to
2.2 mg/L. Mycolicibacterium fortuitum and Pseudomonas were detected in
both systems, and Mycolicibacterium was the dominant bacteria with high
disinfectant residue, which relative abundances up to 50 % in biofilm.
Exposure to Mycolicibacterium spp. by drinking water may cause a series
of diseases, including respiratory, genito-urinary tracts, and gastrointestinal
(Loret and Dumoutier, 2019). Unfortunately, the relationship between ni-
trification and pathogenic bacteria is not fully understood.
5.2. Accelerate biofilm development
Biofilm is ubiquitous in DWDS. Once nitrification occurs, biofilm
formation can be promoted by multiple pathways. Firstly, biofilms are the
primary form of bacterial growth (Trunk et al., 2018); about 95 % of bacte-
ria in drinking water supply systems are present in biofilms (Zhu et al.,
2021). Hence, it is reasonable that the increases in HPC accompanied by
nitrification are beneficial to biofilm formation (Keshvardoust et al.,
2019). Secondly, releasing H+ during the ammonia-oxidizing process can
drop the system's pH. Generally, a pH value of 6 or less can be detected if
nitrification occurs (Liu et al., 2016). The electrostatic repulsion between
bacteria and solid surface decreases with the decrease in pH value, which
increases the adhesion potential of bacteria on the pipeline's surface (Liu
et al., 2016). Lastly, changes in water quality, such as DO consumption,
pH, and alkalinity reduction caused by nitrification will accelerate the
corrosion of the pipe network system (Sarker et al., 2018). At the same
time, corroded pipes are more conducive to microbial attachment and
colonization owing to the rough surface (Pedersen, 1990). On the other
hand, trace metals released during corrosion, such as iron and copper, are
the elements needed for microbial growth (Liu et al., 2016).
With a dense cell population, biofilm not only accelerates the transfer of
antibiotic-resistance genes but serves as a reservoir for opportunistic path-
ogens, which pose adverse effects on global public health (Li et al., 2018;
Pullerits et al., 2020). AOB is mainly distributed inside the biofilm to pro-
tect it from disinfectant attacks (Rantanen et al., 2020). Nitrifying biofilm
formation was accompanied by the accumulation of nitrifying bacteria,
S. Zheng et al. Science of the Total Environment 874 (2023) 162353

which is more stable to chloramine interference (Keshvardoust et al., conducive to the growth of nitrifying bacteria in chloraminated drinking
2020). First, the biofilm matrix polymers like polysaccharides can react water distribution systems. Biosafety problems caused by nitrification,
with chloramine. In this case, reducing chloramine concentration and re- such as heterotrophic bacteria growth, biofilm development, and microbial
leasing free ammonia benefit AOB growth. In turn, the chloramine decay community change, pose a significant threat to drinking water safety
induced by AOB decreases the interference of chloramines on biofilm. Be- management. Therefore, understanding the potential mechanism of the
sides, Pressman et al. (2012) explored the effect of monochloramine on biosafety risk caused by nitrifying bacteria under continuous high-
the activity, vitality, and recovery of nitrifying biofilms. The results showed temperature stress is crucial for ensuring the safety of drinking water
that even if monochloramine completely penetrated the biofilm, complete under global warming; still, it has scarcely been studied until now. Hence,
vitality loss did not occur. Oxygen utilization was quickly recovered in the following points can be pursued in future research:
the biofilm when chloramine was removed. Hence, AOB within biofilm
(1) AOB can promote the growth of heterotrophic bacteria. In turn, hetero-
makes developing biofilm in DWDS more difficult to control.
trophic bacteria compete with AOB for resources such as DO and living
space. The response of nitrifying bacteria to high temperatures
5.3. Shape microbial community
(e.g., growth, enzyme, metabolism) and the effect of this change on
the occurrence, fate, and distribution of nitrifying bacteria and other
The microbial community in DWDS can be shaped by nitrification, pri-
bacteria, especially pathogenic microorganisms, are issues of concern
marily related to chloramine decay. Previous studies have demonstrated
to ensure water quality safety.
that Actinobacteria and Gammaproteobacteria were the dominant classes
(2) In addition to accelerating the decay of chloramine, biofilm provides
at chloramine concentrations of 1.65 mg/L-2.18 mg/L. Comparatively,
shelter for opportunistic pathogens. AOB is the main driving force of
Solibacteres, Nitrospira, Sphingobacteria, and Betaproteobacteria were
biofilm formation in DWDS. Understanding the mechanism of biofilm
the dominant classes when chloramine was lower than 0.65 mg/L. It
formation mediated by AOB under extreme weather conditions can
showed higher richness than in high chloramine conditions (Krishna
provide a scientific theoretical basis for future control of biofilm forma-
et al., 2013). Further analysis found that Pseudomonas, Methylobacterium,
tion in the pipe network system.
and Sphingomonas were the dominant genera before nitrification. However,
(3) Frequent high temperature provides favorable conditions for nitrifica-
with the onset of nitrification, Sphingomonas gradually dominated, and its
tion. However, traditional nitrification-control strategies do not always
relative abundance increased by 3 times to 40 % (Krishna et al., 2013). A
provide long-term nitrification prevention. Therefore, new technolo-
similar result was observed by Hwang et al. (2012), Methylobacteriaceae
gies should be developed to control nitrification. Microbiome-based
and Sphingomonadaceae were also more abundant in chlorinated water
bioindicators have been shown to predict the potential onset of a nitri-
in DWDS with alternating use of chlorination and chloramination.
fication episode, which can help control nitrification earlier before it
Methylobacterium species isolated from the hospital tap water with resis-
becomes severe. In addition, based on the chemical signals between
tance to 8 antibiotics, especially imipenem and tetracycline (Furuhata
bacteria, application of quorum-sensing inhibitors to suppress AOB
et al., 2006). Sphingomonas, as monochloramine-resistant organisms, not
growth is also one potential strategy to control nitrification.
only secret exopolysaccharides that react with chloramines but enhance
cellular adhesion that accelerate biofilm formation (Cruz et al., 2020).
Breakpoint chlorination is a common strategy for water utilities to
Supplementary data to this article can be found online at https://doi.
control nitrification. It refers temporarily converts chloramines into free
org/10.1016/j.scitotenv.2023.162353.
chlorine, thereby inhibiting AOB growth and altering bacterial communi-
ties (Odell et al., 1996; Zeng and Mitch, 2016). However, the microbial
CRediT authorship contribution statement
community is resilient, which refers to the recovery rate after disturbances
to alternative stable states (Gomez-Alvarez et al., 2016). Recent studies
Shikan Zheng: Conceptualization, Investigation, Writing – original
have proposed that although the gene copy numbers of AOB and Nitrospira
draft. Jianguo Li: Investigation, Formal analysis. Chengsong Ye: Method-
decreased significantly during chlorination, which average log reduction
ology, Data curation. Xuanxuan Xian: Software. Mingbao Feng: Visuali-
was 2.4 and 2.1, respectively. However, a rapid rebound immediately
zation, Supervision. Xin Yu: Supervision, Writing – review & editing,
occurred after a month of burning, which can increase by up to one order
Funding acquisition.
of magnitude. Moreover, nitrification seemed more serious 6–12 months
later, and microbial community structure gradually returned to the state be-
fore chlorine burns (Wang et al., 2014). Besides, because of the precursors Data availability
released from nitrifying biofilm, the increased formation of halogenated
disinfection byproducts in bulk water was found during chlorine treatment Data will be made available on request.
(Zeng and Mitch, 2016). In addition, the chlorine resistance of bacteria is
also enhanced during the process (Bal Krishna et al., 2013; Batté et al., Declaration of competing interest
2003). The existence of chlorine-resistance bacteria is more difficult to in-
active by chloramine. Worse still, accumulating studies have reported that The authors declare that they have no known competing financial inter-
chlorine-resistance bacteria are more likely to be antibiotic-resistant ests or personal relationships that could have appeared to influence the
(Khan et al., 2016; Tong et al., 2021). Khan et al. (2016) isolated 22 genera work reported in this paper.
from water supply systems to explore the relationship between disinfectant-
and antibiotic-resistant in bacteria, they found the chlorine-resistant bacte- Acknowledgments
ria showed a significant correlation with tetracycline, sulfamethoxazole
and amoxicillin, which p < 0.05. Considering the more severe nitrification This research was supported by the National Natural Science Founda-
and other adverse effects after breakpoint chlorination, the long-term con- tion of China (U2005206) and Xiamen Municipal Bureau of Science and
trol of nitrification in waterworks faces challenges. Technology (YDZX20203502000003).

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