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

www.sciencedirect.com 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- et al. [16] analyzed bulk water and biofilm samples
tion [11,12]. However, fecal indicator organisms do not collected from an IWS system in Cali, Colombia, report-
represent the behavior of all pathogens and the entire ing that Proteobacteria, Cyanobacteria and Firmicutes were
DW microbial community. Pathogens and other non- the most abundant phyla in water samples and that
pathogenic microorganisms can exist in the absence of microbial communities in biofilms were more diverse
indicators [3]. Recent literature characterizing concen- than in bulk water samples. Nonetheless, these studies
trations of enteric pathogens in IWSs is lacking; however, have not elucidated how key features of IWS impact
cases of waterborne illnesses due to water supply in areas microbial communities and whether they might be dis-
where IWS is common continue to be documented tinct from CWS.
[1,6,13,14].
Impacts of disinfection
To our knowledge, microbial communities in IWS have Several variables shape microbial communities in
been explored to a limited extent using DNA sequencing the drinking water distribution system (DWDS) [17–32]
methods. Tokajian et al. [15] reported the presence of (Figure 2). Among these variables, the maintenance of a
viable Proteobacteria and several gram-negative bacteria in disinfectant residual (e.g. chlorine or chloramine) in IWS
an IWS system in Beirut, Lebanon. Montoya-Pachongo 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 disinfectant-free DW systems were shown. Regardless of
residual disinfectant is influenced by physical and chem- disinfectant residual (chlorination, chloramination or
ical parameters in the system. If the lifetime of chlorine is residual-free), Proteobacteria were the dominant bacterial
shorter than the water age, residual chlorine cannot reach phylum. However, there were significant differences in
the farthest locations of the DWDS (based on first-order other bacterial phyla depending on disinfectant practices
chlorine decay modeling for IWS) [33,34]. In IWS when (e.g. Operational Taxonomic Units (OTUs) classified as
supply is off, the chlorine residual in stagnant water will Legionella at the genus level had significant higher relative
decay over time due to demand from microorganisms, abundance and occurrence in disinfectant residual-free
organic matter and material introduced from intrusion. At systems compared to disinfected systems). This study
the start of a supply cycle, zero or low chlorine residual has also found that microbial communities in water samples
been documented due to the flushing of stagnant waters from residual-free systems were more diverse, compared
[12,35]. Once the first flush of water has exited the to samples with residual disinfectant. Furthermore, Fish
DWDS and supply stabilizes, it is possible to maintain a and Boxall [39] reported higher bacterial concentrations
consistent chlorine residual for the remainder of the in biofilms developed under a low chlorine regime, while
supply [12]. Bertelli et al. [40] reported the presence of more diverse
biofilms in sampling points with lower chlorine concen-
Studies of CWSs have revealed microbial shifts correlated trations, and the predominance of Pseudomonas spp. in
with disinfection and the selection of biofilms that are biofilms formed under higher chlorine concentrations in
resistant to disinfection [36,37,38]. Bautista-de los San- two CWSs supplied by treated ground water. These
tos et al. [36] conducted a meta-analysis of 16S rRNA results are particularly relevant with respect to IWS,
gene sequencing studies of bulk DW, in which differ- because it is more difficult to maintain a consistent
ences in microbial communities between disinfected and 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- on peat samples showed that majority of drought-sensi-
ent at the start of a water supply cycle, whereas once the tive OTUs were members of the phyla Bacteroidetes and
supply and residual disinfectant stabilizes the microbial Proteobacteria, which contain a high proportion of non-
community may be more similar to those found in chlori- dormant bacteria compared to other phyla [46]. Desicca-
nated CWSs. The effects of exposing biofilms (Figure 1) tion in temperate streambed sediments caused a shift in
to varying concentrations of chlorine warrant special bacterial community towards the composition typical of
attention, as these have been reported to contain more soils, and a decrease in extracellular enzyme activity;
microbial biomass than the bulk water in chlorinated interestingly, after 14 days of rewetting, the community
CWSs (pipe diameter of 100 mm) fed by river water recovered with respect to extracellular enzyme activity
treating utilities [41]. but did not return to the original taxonomic composition
of unaffected sediments, showing higher relative abun-
Impacts of stagnation dance of Alphaproteobacteria and lower relative abundance
In CWS that supply residential areas, stagnation usually of Bacteroidetes [47]. A similar behavior has been observed
occurs overnight, as a consequence of a diurnal water in saltmarsh sediments [48].
demand pattern where water consumption is higher in
the morning and early evening, and declines when people Dry/re-wetting periods could affect biofilm-associated
are at work or during the late night when people usually microorganisms in IWSs in different ways, depending on
sleep. Depending on the severity of IWS, stagnation during their susceptibility to desiccation. Among the microorgan-
a supply cycle may be less common than in CWS because isms likely present in IWS, both Firmicutes and Actinobac-
customers are busy using the water and filling containers, teria are gram-positive bacteria highly resistant to desicca-
and leakage rates are often high. Regardless, stagnation tion [49,50]. Furthermore, Firmicutes, Actinobacteria and
occurs between supply cycles in low-lying pipes and in several protozoa relevant for DW (e.g. Acanthamoeba, Cryp-
other sections until they drain. Erickson et al. [12] tosporidium, Giardia) can enter dormant states (e.g. endo-
reported microbial growth in the DWDS using HPC counts spores, endospore-like structures, cysts) which are highly
after a service interruption of 6–14 days in an IWS in resistant to desiccation and environmental stress [49,51,52].
Panama. Microbial growth due to overnight stagnation Therefore, a decrease in biofilm alpha-diversity during no
has been reported in CWS with [42] and without disinfec- flow periods, changes in community structure after pro-
tant residual [18,43]. Ling et al. [18] reported differences longed dry periods, and the survival of desiccation-resistant
in community structure between premise plumbing sam- microorganisms are likely in IWSs.
ples affected by stagnation and samples from mains; inter-
estingly, microbial communities in stagnant water samples Fish et al. [53] reported that biofilms in a model CWS
closer to the taps (i.e. sampling points) were more similar to were dominated by polysaccharides over proteins. More-
biofilm communities collected from water meters in the over, the production of extracellular polysaccharides is a
city, than to water from the mains. In IWS, a change in bacterial survival strategy under dry conditions [54] as
microbial community structure due to stagnation is likely to these molecules confer biofilms with fluidity and resis-
occur, and the magnitude and public health implications tance to desiccation [55]. Therefore, the survival of
will depend on the duration of the stagnation periods, the desiccation-resistant microorganisms in IWSs is likely
composition of the microbial community, both autochtho- aided by the polysaccharide-dominated extracellular
nous and introduced, and the persistence of disinfectant polymeric substances. Furthermore, the hydraulic regime
residual. is an important variable for DW biofilms, shaping their
structure (cell, carbohydrate and protein volume per area
Impacts of drained periods of biofilm) and bacterial community diversity [56,57].
Pipes in IWS experience drained periods, and their Differently to CWSs, biofilms in IWSs develop under
associated biofilms and loose deposits could experience hydraulic regimes that include low, transient and zero
dry periods from hours to days, followed by re-wetting pressures [12]. DW biofilms grown under high shear
periods. This section explores the potential impacts of stress are cohesively stronger than those grown under
dry/re-wetting periods and desiccation on biofilms; much lower shear stress [58], and cell clusters remaining on
less is known about the microbial communities in loose biofilms after exposure to high hydrodynamic shear stress
deposits, which are more likely to remain wetted at the are more difficult to detach (i.e. have higher detachment
bottom of the pipe. shear stress) [59]. Therefore, it is likely biofilms in IWSs
are cohesively weaker and more prone to cell detachment
In freshwater streams, flow intermittency causes a than those in CWSs.
decrease in biofilm alpha-diversity and changes in beta-
diversity [44]. Timoner et al. [45] reported an increase of Impacts of backflow and intrusion
Firmicutes (a phylum with several endospore-forming The likelihood of backflow and intrusion is higher in IWS
genera) and Actinobacteria during the non-flow period in (Figure 1), and can introduce microorganisms to the DW
a Mediterranean stream. A controlled drought experiment 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 can impact the microbiology of DW while stored, and
by backflow (e.g. in cross-connections between potable induce microbial growth [75,76]. Connected under-
water and a non-potable water source), its composition ground or rooftop tanks may be influenced by premise
will reflect the non-potable water source and its origin plumbing, whereas stand-alone storage containers could
(e.g. heating/cooling towers, chemical mixing tanks, or be influenced by hands and vessels that are used to
sinks/bath tubs) [63–65]. During intrusion, fecal contam- extract water [6].
ination from nearby sources of fecal contamination (e.g.
sewers, pit latrines) can enter the DWDS along with the The dominance of Proteobacteria in independent domes-
microbial community of the environment outside of tic storage containers has been reported [7,77]; whereas,
pipes. This microbial community can include non-patho- Dada et al. [78] reported the dominance of
genic microorganisms commonly found in water, soil and Bacteroidetes. Farenhorst et al. [7] reported an enrichment
feces, and pathogens [34,66–70]. Moreover, the use of of Alphaproteobacteria in water samples from cisterns and
illegal connections and poor quality pipes prone to dam- Alphaproteobacteria and Bacteroidetes in water samples from
age can exacerbate intrusion in IWS. buckets. Low disinfectant residual combined with high
temperatures in rooftop tanks can lead to shifts in micro-
Impacts of air pockets bial communities and induce micro-environments that
The operation of IWS (e.g. valves opening and closing, select for distinct microbial communities, without neces-
pipe fill-up period when the water is initially on) gen- sarily demonstrating low water quality under traditional
erates air pockets. When flow is turned on to fill an empty culture-based methods [76]. Li et al. [75] reported
pipe, the entrapped air is displaced and finally expelled significant microbial growth in rooftop tanks, compared
from the system when the pressure is high enough. This to underground tanks, which may have been due to
displacement of air over the biofilm layer could cause cell higher temperatures. Microbial communities in water
detachment, depending on the properties of the biofilm mains were more similar to those in underground tanks
and the bacterial strains present in it. Using microfluidic than in rooftop tanks. Moreover, Legionella concentrations
experiments and P. aeruginosa PA01 biofilms, Jang et al. were significantly higher in underground tanks, while
[71] showed that air bubbles affected biofilm of different Mycobacterial concentrations were higher in rooftop
ages (4, 8 and 12 hours) in different ways: air removed, tanks. Further research is needed to elucidate how dif-
rearranged and did not affect the cells in 4 hour, 8 hour ferent storage practices and operational and environmen-
and 12 hour biofilms, respectively. Similarly, Sharma et al. tal factors influence microbial communities in DW during
[72] showed that the presence of microbubbles in the flow storage, and how to design and maintain stored water to
increased the detachment of Actinomyces naeslundii (hydro- reduce potential health risks.
phobic) biofilms from 40% to 98%, while detachment of
Streptococcus oralis (hydrophilic) and co-adhering aggre- Perspectives
gates of both bacteria was unaffected. The age biofilms on IWSs have unique features, and further investigation of
pipe walls and loose deposits in IWSs could be highly IWS microbiomes is warranted. Important gaps in the
variable. Biofilms in IWS could be very young because of literature that should be elucidated are: (a) the impacts of
the constant detachment that occurs during supply cycles; stagnation, drained periods, and air pockets/bubbles on
on the other hand, the biofilms could also be very old and the microbial community; (b) the temporal and spatial
resistant to detachment due to the diverse hydraulic dynamics of the IWS microbiome, to establish baseline
regime imposed by intermittency. It is likely that a conditions and detect deviations/events; (c) whether any
combination of both young and old biofilms is present unique features of IWS increase the growth of opportu-
in IWS. Moreover, these biofilms are formed by mixed nistic pathogens; (d) whether microbiome approaches can
microbial communities, and not single-species or double- lead to the development of affordable and field-deploy-
species biofilms (such as the ones tested by Jang et al. [68] able methods to detect contamination introduced by
and Sharma et al. [69]). Therefore, the effects of air intrusion/backflow and assess its respective health risk.
bubbles on biofilms and loose deposits representative To fill these knowledge gaps, a combination of controlled
of full-scale IWSs biofilms (e.g. old/young, mixed bacte- lab studies (to isolate variables) with field studies (to
rial species, relevant pipe material, wet/dry periods, rele- capture the complexity of full-scale systems) is recom-
vant flow rate and shear stress) warrant further mended. The application of molecular microbial meth-
investigation. ods, including high-throughput sequencing, is recom-
mended in combination with traditional culture-based
Impacts of storage methods. Rigorous experimental designs following best
Households relying on IWS must store water, and it is practices are needed [19,79,80,81]. Finally, meaningful
known that water quality during storage can be compro- collaborations between researchers in high-income coun-
mised [8,73,74]. Several factors including disinfectant tries and researchers in low-income and middle-income
residual, temperature, size and material of storage (con- countries could help to overcome the resource limitations
tainer/tank/vessel), cleaning cycles and retention times present in many regions with IWS.

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172 Environmental biotechnology

Conflict of interest statement 12. Erickson JJ, Smith CD, Goodridge A, Nelson KL: Water quality
 effects of intermittent water supply in Arraiján, Panama. Water
Nothing declared. Res 2017, 114:338-350.
Reports the varied effects of intermittent supply on water quality.
13. Moore S, Dongdem AZ, Opare D, Cottavoz P, Fookes M, Sadji AY,
Acknowledgement Dzotsi E, Dogbe M, Jeddi F, Bidjada B: Dynamics of cholera
epidemics from Benin to Mauritania. PLoS Negl Trop Dis 2018,
KAC acknowledges support from an NSF Graduate Research Fellowship 12:e0006379.
and a Ford Foundation Fellowship.
14. Trudeau J, Aksan A-M, Vásquez WF: Water system unreliability
and diarrhea incidence among children in Guatemala. Int J
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