Available online at www.sciencedirect.
com
ScienceDirect
Understanding the impacts of intermittent supply on the
drinking water microbiome
Quyen M Bautista-de los Santos1, Karina A Chavarria2 and
Kara L Nelson2
Increasing access to piped water in low-income and middle-
income countries combined with the many factors that threaten
our drinking water supply infrastructure mean that intermittent
water supply (IWS) will remain a common practice around the
world. Common features of IWS include water stagnation, pipe
drainage, intrusion, backflow, first flush events, and household
storage. IWS has been shown to cause degradation as
measured by traditional microbial water quality indicators. In
this review, we build on new insights into the microbial ecology
of continuous water supply systems revealed by sequencing
methods to speculate about how intermittent supply conditions
may further influence the drinking water microbiome, and
identify priorities for future research.
Addresses
1
Department of Civil and Environmental Engineering, University of
Michigan, Ann Arbor, MI, United States
2
Civil and Environmental Engineering, University of California, Berkeley,
CA 94720, United States
Corresponding author: Nelson, Kara L (karanelson@berkeley.edu)
Current Opinion in Biotechnology 2019, 57:167–174
This review comes from a themed issue on Environmental
biotechnology
Edited by Lutgarde Raskin and Per Halkjær Nielsen
For a complete overview see the Issue and the Editorial
Available online 14th May 2019
https://doi.org/10.1016/j.copbio.2019.04.003
0958-1669/ã 2019 Elsevier Ltd. All rights reserved.
Introduction
Intermittent Water Supply (IWS) encompasses a variety of
supply practices that convey drinking water (DW) for a
limited duration, as opposed to Continuous Water Supply
(CWS), which conveys water 24-hours a day, every day, with
maintenance of a minimum pressure that guarantees ade-
quate flow and protects against intrusion. It is estimated that
one billion people rely on IWS, potentially leading to
4.52 million cases of diarrhea, 109 000 diarrheal disability
adjusted life years (DALYs), and 1560 deaths each year [1].
CWS systems (CWSs) become intermittent for a variety of
reasons and there is a growing body of literature document-
ing changes to water quality in IWS systems (IWSs) [2].
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Compared to CWSs, several characteristics of IWS have
the potential to increase deterioration of DW quality
during conveyance, as reviewed by Kumpel and Nelson
[3]. Low and negative pressures between supply cycles
can lead to intrusion or backflow. Growth of microorgan-
isms (including opportunistic pathogens) in biofilms,
loose deposits, and bulk water [4] may differ from
CWS due to the unique conditions that exist between
supply cycles and during first flush events (when supply is
restarted). Additionally, consumers are forced to store
water, and recontamination of stored water is well docu-
mented. Although the deterioration of water quality by
IWS is well described, no studies have shown how inter-
mittent supply affects microbial communities. Under-
standing how the unique features of IWS impact water
microbiomes compared to CWS (Figure 1) may help to
better characterize risks of IWS and provide insight into
strategies to protect water quality in IWS. Characterizing
the microbial ecology in IWSs could also help to under-
stand whether intermittent operation increases rates of
corrosion and decreases the stability of disinfectant
residual.
The aims of this review are to: (i) provide an overview of
what is known about the microbiology of IWS, with
emphasis on the links between microbial parameters
and system properties (e.g. engineering features, chemi-
cal parameters), (ii) draw from the available literature on
the microbiology of CWS to make inferences relevant to
IWS, and (iii) identify research priorities for understand-
ing the IWS microbiome and methods/approaches to
address current knowledge gaps. We also draw from
literature on DW systems that have features relevant to
IWSs (e.g. stagnation in premise plumbing, storage con-
tainers filled with community taps in CWS) and natural
environments (e.g. biofilms in intermittent streams).
The microbiology of IWS
The microbiology of IWSs has been characterized using
traditional culture-based techniques, with the aim of
defining whether water is potable or safe for human
consumption. Overall, indicator tests and water quality
parameters reveal that water quality in IWSs can deterio-
rate during distribution and after residential storage
[3,5–8] frequently exceeding the local regulations and
international recommended standards [9,10]. Addition-
ally, a deterioration in water quality is detected (high
turbidity, HPC counts, low chlorine concentration) in first
Current Opinion in Biotechnology 2019, 57:167–174
168 Environmental biotechnology

Figure 1

Fecal contamination (shallow sewer,

open drain, open defecation, animal
feces, latrine pit, septic tank, manure Environmental
or drainfield) contamination (soil)

Air pocket

Bulk+
Particle
associated
bacteria

Biofilm

Loose
deposits Leakage Seasonally fluctuating
groundwater table with potential
(a) (b) (c) to periodically submerge pipes

Fecal contamination source Environmental

(latrine pits, septic tanks, contamination
sewers) (groundwater)

Current Opinion in Biotechnology

Microbial components in IWS. The cross section of a CWS pipe (a) is compared with IWS pipes. Considering the intermittency of the water
supply, the pipes in IWS can experience several conditions that range from completely full with positive pressure similar to CWS (a) and low or
negative pressures (b), to partially drained (c) and completely drained. Microbial communities in DW systems assemble in four distinct
components: (i) biofilms; (ii) bulk water or planktonic; (iii) suspended particles; and (iv) loose deposits. Among these four components, biofilms
and loose deposits have been reported to contain most of the microbial biomass in chlorinated CWSs [4,82–84]. In IWS systems, there is a
higher risk of external microorganisms being introduced during low or negative pressure events via intrusion (from environment) or backflow
(from cross-connections; not shown). The autochthonous DW microbiota in CWSs biofilms has been reported to be dominated by
Proteobacteria [57]; other relevant taxa detected in lower abundance include Actinobacteria, protozoa (Acanthamoeba) and fungi [57,74]. The
autochthonous viral diversity in CWSs has not been explored with high-throughput sequencing methods. Microorganisms introduced during
contamination events potentially include environmental (e.g. soil, water) and enteric microorganisms from fecal contamination. The soil
microbiome is dominated by Proteobacteria, Actinobacteria and Acidobacteria [68]. Firmicutes dominate the healthy human and livestock gut
microbiome [69,70]. Besides intrusion and backflow, other factors characteristic of IWS that may alter the microbial community include
stagnation, wet/dry cycles, and loss of disinfectant residual.

flush samples, when supply is restored after an interrup-
tion [11,12]. However, fecal indicator organisms do not
represent the behavior of all pathogens and the entire
DW microbial community. Pathogens and other non-
pathogenic microorganisms can exist in the absence of
indicators [3]. Recent literature characterizing concen-
trations of enteric pathogens in IWSs is lacking; however,
cases of waterborne illnesses due to water supply in areas
where IWS is common continue to be documented
[1,6,13,14].
To our knowledge, microbial communities in IWS have
been explored to a limited extent using DNA sequencing
methods. Tokajian et al. [15] reported the presence of
viable Proteobacteria and several gram-negative bacteria in
an IWS system in Beirut, Lebanon. Montoya-Pachongo
et al. [16] analyzed bulk water and biofilm samples
collected from an IWS system in Cali, Colombia, report-
ing that Proteobacteria, Cyanobacteria and Firmicutes were
the most abundant phyla in water samples and that
microbial communities in biofilms were more diverse
than in bulk water samples. Nonetheless, these studies
have not elucidated how key features of IWS impact
microbial communities and whether they might be dis-
tinct from CWS.
Impacts of disinfection
Several variables shape microbial communities in
the drinking water distribution system (DWDS) [17–32]
(Figure 2). Among these variables, the maintenance of a
disinfectant residual (e.g. chlorine or chloramine) in IWS
is essential to protect against intrusion and microbial

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Understanding the impacts of intermittent supply on the drinking water microbiome Bautista-de los Santos, Chavarria and Nelson 169

Figure 2

Raw water Treated water Distributed water Premise plumbing Residential storage

Temporal variation Treatment train Temperature Temperature

Filtration Water chemistry Water chemistry
Disinfection Pipe material Type of materials
Pipe age Age of materials
Temporal variation Stagnation
DWTP Surface area to volume ratio

POU

Disinfectant residual

Cell concentration
Community dissimilarity
Current Opinion in Biotechnology

Variables affecting the DW microbiome in CWS. Several variables shape the microbial communities in the DWDS. Roeselers et al. [17] and Ji et al.
[25] reported that the drinking water treatment train was the dominant factor distinguishing bacterial communities in drinking water samples.
Looking at individual treatment steps, both filtration [26–29] and disinfection [30] have been reported to significantly shape bacterial communities,
while disinfection significantly shapes the fungal community [28]. Temperature [32], pipe materials and water chemistry [25] shape the drinking
water microbiome. Moreover, the DWDS microbiome experiences temporal and spatial variation. Seasonal [31], monthly [32], weekly [20] and daily
[19] changes in community structure/membership have been reported in DWDS with disinfectant residual. Monthly and daily variations in total and
intact cell concentrations and Adenosine Triphosphate (ATP) concentration have also been reported in systems with disinfectant residual [21,22]
and systems without disinfectant residual [23]. Spatial variations are observed during distribution of the treated water [24], with bacterial
community dissimilarity [31,32] and variation in cell concentrations [21,22] increasing with distance from the treatment plant. Such temporal and
spatial variations in the DW microbiome are likely observed in IWSs.

growth. Similar to CWS, in IWS the persistence of a
residual disinfectant is influenced by physical and chem-
ical parameters in the system. If the lifetime of chlorine is
shorter than the water age, residual chlorine cannot reach
the farthest locations of the DWDS (based on first-order
chlorine decay modeling for IWS) [33,34]. In IWS when
supply is off, the chlorine residual in stagnant water will
decay over time due to demand from microorganisms,
organic matter and material introduced from intrusion. At
the start of a supply cycle, zero or low chlorine residual has
been documented due to the flushing of stagnant waters
[12,35]. Once the first flush of water has exited the
DWDS and supply stabilizes, it is possible to maintain a
consistent chlorine residual for the remainder of the
supply [12].
Studies of CWSs have revealed microbial shifts correlated
with disinfection and the selection of biofilms that are
resistant to disinfection [36,37,38]. Bautista-de los San-
tos et al. [36] conducted a meta-analysis of 16S rRNA
gene sequencing studies of bulk DW, in which differ-
ences in microbial communities between disinfected and
disinfectant-free DW systems were shown. Regardless of
disinfectant residual (chlorination, chloramination or
residual-free), Proteobacteria were the dominant bacterial
phylum. However, there were significant differences in
other bacterial phyla depending on disinfectant practices
(e.g. Operational Taxonomic Units (OTUs) classified as
Legionella at the genus level had significant higher relative
abundance and occurrence in disinfectant residual-free
systems compared to disinfected systems). This study
also found that microbial communities in water samples
from residual-free systems were more diverse, compared
to samples with residual disinfectant. Furthermore, Fish
and Boxall [39] reported higher bacterial concentrations
in biofilms developed under a low chlorine regime, while
Bertelli et al. [40] reported the presence of more diverse
biofilms in sampling points with lower chlorine concen-
trations, and the predominance of Pseudomonas spp. in
biofilms formed under higher chlorine concentrations in
two CWSs supplied by treated ground water. These
results are particularly relevant with respect to IWS,
because it is more difficult to maintain a consistent
chlorine residual. Thus, in IWSs, it is likely that a

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170 Environmental biotechnology
distinctive, rich and diverse microbial community is pres-
ent at the start of a water supply cycle, whereas once the
supply and residual disinfectant stabilizes the microbial
community may be more similar to those found in chlori-
nated CWSs. The effects of exposing biofilms (Figure 1)
to varying concentrations of chlorine warrant special
attention, as these have been reported to contain more
microbial biomass than the bulk water in chlorinated
CWSs (pipe diameter of 100 mm) fed by river water
treating utilities [41].
Impacts of stagnation
In CWS that supply residential areas, stagnation usually
occurs overnight, as a consequence of a diurnal water
demand pattern where water consumption is higher in
the morning and early evening, and declines when people
are at work or during the late night when people usually
sleep. Depending on the severity of IWS, stagnation during
a supply cycle may be less common than in CWS because
customers are busy using the water and filling containers,
and leakage rates are often high. Regardless, stagnation
occurs between supply cycles in low-lying pipes and in
other sections until they drain. Erickson et al. [12]
reported microbial growth in the DWDS using HPC counts
after a service interruption of 6–14 days in an IWS in
Panama. Microbial growth due to overnight stagnation
has been reported in CWS with [42] and without disinfec-
tant residual [18,43]. Ling et al. [18] reported differences
in community structure between premise plumbing sam-
ples affected by stagnation and samples from mains; inter-
estingly, microbial communities in stagnant water samples
closer to the taps (i.e. sampling points) were more similar to
biofilm communities collected from water meters in the
city, than to water from the mains. In IWS, a change in
microbial community structure due to stagnation is likely to
occur, and the magnitude and public health implications
will depend on the duration of the stagnation periods, the
composition of the microbial community, both autochtho-
nous and introduced, and the persistence of disinfectant
residual.
Impacts of drained periods
Pipes in IWS experience drained periods, and their
associated biofilms and loose deposits could experience
dry periods from hours to days, followed by re-wetting
periods. This section explores the potential impacts of
dry/re-wetting periods and desiccation on biofilms; much
less is known about the microbial communities in loose
deposits, which are more likely to remain wetted at the
bottom of the pipe.
In freshwater streams, flow intermittency causes a
decrease in biofilm alpha-diversity and changes in beta-
diversity [44]. Timoner et al. [45] reported an increase of
Firmicutes (a phylum with several endospore-forming
genera) and Actinobacteria during the non-flow period in
a Mediterranean stream. A controlled drought experiment
Current Opinion in Biotechnology 2019, 57:167–174
on peat samples showed that majority of drought-sensi-
tive OTUs were members of the phyla Bacteroidetes and
Proteobacteria, which contain a high proportion of non-
dormant bacteria compared to other phyla [46]. Desicca-
tion in temperate streambed sediments caused a shift in
bacterial community towards the composition typical of
soils, and a decrease in extracellular enzyme activity;
interestingly, after 14 days of rewetting, the community
recovered with respect to extracellular enzyme activity
but did not return to the original taxonomic composition
of unaffected sediments, showing higher relative abun-
dance of Alphaproteobacteria and lower relative abundance
of Bacteroidetes [47]. A similar behavior has been observed
in saltmarsh sediments [48].
Dry/re-wetting periods could affect biofilm-associated
microorganisms in IWSs in different ways, depending on
their susceptibility to desiccation. Among the microorgan-
isms likely present in IWS, both Firmicutes and Actinobac-
teria are gram-positive bacteria highly resistant to desicca-
tion [49,50]. Furthermore, Firmicutes, Actinobacteria and
several protozoa relevant for DW (e.g. Acanthamoeba, Cryp-
tosporidium, Giardia) can enter dormant states (e.g. endo-
spores, endospore-like structures, cysts) which are highly
resistant to desiccation and environmental stress [49,51,52].
Therefore, a decrease in biofilm alpha-diversity during no
flow periods, changes in community structure after pro-
longed dry periods, and the survival of desiccation-resistant
microorganisms are likely in IWSs.
Fish et al. [53] reported that biofilms in a model CWS
were dominated by polysaccharides over proteins. More-
over, the production of extracellular polysaccharides is a
bacterial survival strategy under dry conditions [54] as
these molecules confer biofilms with fluidity and resis-
tance to desiccation [55]. Therefore, the survival of
desiccation-resistant microorganisms in IWSs is likely
aided by the polysaccharide-dominated extracellular
polymeric substances. Furthermore, the hydraulic regime
is an important variable for DW biofilms, shaping their
structure (cell, carbohydrate and protein volume per area
of biofilm) and bacterial community diversity [56,57].
Differently to CWSs, biofilms in IWSs develop under
hydraulic regimes that include low, transient and zero
pressures [12]. DW biofilms grown under high shear
stress are cohesively stronger than those grown under
lower shear stress [58], and cell clusters remaining on
biofilms after exposure to high hydrodynamic shear stress
are more difficult to detach (i.e. have higher detachment
shear stress) [59]. Therefore, it is likely biofilms in IWSs
are cohesively weaker and more prone to cell detachment
than those in CWSs.
Impacts of backflow and intrusion
The likelihood of backflow and intrusion is higher in IWS
(Figure 1), and can introduce microorganisms to the DW
distribution system (DWDS) [60–62]. Although it is
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Understanding the impacts of intermittent supply on the drinking water microbiome Bautista-de los Santos, Chavarria and Nelson 171
difficult to identify the particular microbiota introduced
by backflow (e.g. in cross-connections between potable
water and a non-potable water source), its composition
will reflect the non-potable water source and its origin
(e.g. heating/cooling towers, chemical mixing tanks, or
sinks/bath tubs) [63–65]. During intrusion, fecal contam-
ination from nearby sources of fecal contamination (e.g.
sewers, pit latrines) can enter the DWDS along with the
microbial community of the environment outside of
pipes. This microbial community can include non-patho-
genic microorganisms commonly found in water, soil and
feces, and pathogens [34,66–70]. Moreover, the use of
illegal connections and poor quality pipes prone to dam-
age can exacerbate intrusion in IWS.
Impacts of air pockets
The operation of IWS (e.g. valves opening and closing,
pipe fill-up period when the water is initially on) gen-
erates air pockets. When flow is turned on to fill an empty
pipe, the entrapped air is displaced and finally expelled
from the system when the pressure is high enough. This
displacement of air over the biofilm layer could cause cell
detachment, depending on the properties of the biofilm
and the bacterial strains present in it. Using microfluidic
experiments and P. aeruginosa PA01 biofilms, Jang et al.
[71] showed that air bubbles affected biofilm of different
ages (4, 8 and 12 hours) in different ways: air removed,
rearranged and did not affect the cells in 4 hour, 8 hour
and 12 hour biofilms, respectively. Similarly, Sharma et al.
[72] showed that the presence of microbubbles in the flow
increased the detachment of Actinomyces naeslundii (hydro-
phobic) biofilms from 40% to 98%, while detachment of
Streptococcus oralis (hydrophilic) and co-adhering aggre-
gates of both bacteria was unaffected. The age biofilms on
pipe walls and loose deposits in IWSs could be highly
variable. Biofilms in IWS could be very young because of
the constant detachment that occurs during supply cycles;
on the other hand, the biofilms could also be very old and
resistant to detachment due to the diverse hydraulic
regime imposed by intermittency. It is likely that a
combination of both young and old biofilms is present
in IWS. Moreover, these biofilms are formed by mixed
microbial communities, and not single-species or double-
species biofilms (such as the ones tested by Jang et al. [68]
and Sharma et al. [69]). Therefore, the effects of air
bubbles on biofilms and loose deposits representative
of full-scale IWSs biofilms (e.g. old/young, mixed bacte-
rial species, relevant pipe material, wet/dry periods, rele-
vant flow rate and shear stress) warrant further
investigation.
Impacts of storage
Households relying on IWS must store water, and it is
known that water quality during storage can be compro-
mised [8,73,74]. Several factors including disinfectant
residual, temperature, size and material of storage (con-
tainer/tank/vessel), cleaning cycles and retention times
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can impact the microbiology of DW while stored, and
induce microbial growth [75,76]. Connected under-
ground or rooftop tanks may be influenced by premise
plumbing, whereas stand-alone storage containers could
be influenced by hands and vessels that are used to
extract water [6].
The dominance of Proteobacteria in independent domes-
tic storage containers has been reported [7,77]; whereas,
Dada et al. [78] reported the dominance of
Bacteroidetes. Farenhorst et al. [7] reported an enrichment
of Alphaproteobacteria in water samples from cisterns and
Alphaproteobacteria and Bacteroidetes in water samples from
buckets. Low disinfectant residual combined with high
temperatures in rooftop tanks can lead to shifts in micro-
bial communities and induce micro-environments that
select for distinct microbial communities, without neces-
sarily demonstrating low water quality under traditional
culture-based methods [76]. Li et al. [75] reported
significant microbial growth in rooftop tanks, compared
to underground tanks, which may have been due to
higher temperatures. Microbial communities in water
mains were more similar to those in underground tanks
than in rooftop tanks. Moreover, Legionella concentrations
were significantly higher in underground tanks, while
Mycobacterial concentrations were higher in rooftop
tanks. Further research is needed to elucidate how dif-
ferent storage practices and operational and environmen-
tal factors influence microbial communities in DW during
storage, and how to design and maintain stored water to
reduce potential health risks.
Perspectives
IWSs have unique features, and further investigation of
IWS microbiomes is warranted. Important gaps in the
literature that should be elucidated are: (a) the impacts of
stagnation, drained periods, and air pockets/bubbles on
the microbial community; (b) the temporal and spatial
dynamics of the IWS microbiome, to establish baseline
conditions and detect deviations/events; (c) whether any
unique features of IWS increase the growth of opportu-
nistic pathogens; (d) whether microbiome approaches can
lead to the development of affordable and field-deploy-
able methods to detect contamination introduced by
intrusion/backflow and assess its respective health risk.
To fill these knowledge gaps, a combination of controlled
lab studies (to isolate variables) with field studies (to
capture the complexity of full-scale systems) is recom-
mended. The application of molecular microbial meth-
ods, including high-throughput sequencing, is recom-
mended in combination with traditional culture-based
methods. Rigorous experimental designs following best
practices are needed [19,79,80,81]. Finally, meaningful
collaborations between researchers in high-income coun-
tries and researchers in low-income and middle-income
countries could help to overcome the resource limitations
present in many regions with IWS.
Current Opinion in Biotechnology 2019, 57:167–174
172 Environmental biotechnology
Conflict of interest statement
Nothing declared.
Acknowledgement
KAC acknowledges support from an NSF Graduate Research Fellowship
and a Ford Foundation Fellowship.
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