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Journal of Applied Microbiology ISSN 1364-5072

REVIEW ARTICLE

Environmental Escherichia coli: ecology and public health

implications—a review
J. Jang1, H.-G. Hur2, M.J. Sadowsky1,3, M.N. Byappanahalli4, T. Yan5 and S. Ishii1,3
1 BioTechnology Institute, University of Minnesota, St. Paul, MN, USA
2 School of Environmental Science and Engineering, Gwangju Institute of Science and Technology, Gwangju, Korea
3 Department of Soil, Water, and Climate, University of Minnesota, St. Paul, MN, USA
4 Lake Michigan Ecological Research Station, Great Lakes Science Center, U.S. Geological Survey, Chesterton, IN, USA
5 Department of Civil and Environmental Engineering, University of Hawai’i at Manoa, Honolulu, HI, USA

Keywords
ecology, Escherichia coli, fecal indicator
bacteria, public health, water quality.
Correspondence
Satoshi Ishii, BioTechnology Institute, Univer-
sity of Minnesota, 1479 Gortner Ave., 140
Gortner Labs, St. Paul, MN, USA.
E-mail: ishi0040@umn.edu
2017/0075: received 13 January 2017, revised
29 March 2017 and accepted 31 March 2017
doi:10.1111/jam.13468
Summary
Escherichia coli is classified as a rod-shaped, Gram-negative bacterium in the
family Enterobacteriaceae. The bacterium mainly inhabits the lower intestinal
tract of warm-blooded animals, including humans, and is often discharged into
the environment through faeces or wastewater effluent. The presence of E. coli
in environmental waters has long been considered as an indicator of recent
faecal pollution. However, numerous recent studies have reported that some
specific strains of E. coli can survive for long periods of time, and potentially
reproduce, in extraintestinal environments. This indicates that E. coli can be
integrated into indigenous microbial communities in the environment. This
naturalization phenomenon calls into question the reliability of E. coli as a
faecal indicator bacterium (FIB). Recently, many studies reported that E. coli
populations in the environment are affected by ambient environmental
conditions affecting their long-term survival. Large-scale studies of population
genetics revealed the diversity and complexity of E. coli strains in various
environments, which are affected by multiple environmental factors. This
review examines the current knowledge on the ecology of E. coli strains in
various environments with regard to its role as a FIB and as a naturalized
member of indigenous microbial communities. Special emphasis is given on
the growth of pathogenic E. coli in the environment, and the population
genetics of environmental members of the genus Escherichia. The impact of
environmental E. coli on water quality and public health is also discussed.

the evolution of micro-organisms and a long-term

Introduction
Escherichia coli is a rod-shaped, Gram-negative bac-
terium, and classified as a member of the family Enter-
obacteriaceae within the Gammaproteobacteria class.
Escherichia coli is among one of the well-studied bacte-
ria. Escherichia coli can grow rapidly under optimal
growth conditions, replicating in ~20 min. Many gene
manipulation systems have been developed using E. coli
as the host bacterium, producing countless enzymes and
other industrial products. Genome sequence analysis of
E. coli was first reported in 1997. Since then, more than
4800 E. coli genomes have been sequenced. The fast-
growth characteristics of E. coli make it suitable to study
experimental evolution study of E. coli involving more
than 50 000 generations is ongoing (Tenaillon et al.
2016).
While we know many things about E. coli under labo-
ratory conditions, relatively little is known about the
ecology of this bacterium in the environment. Because
E. coli is frequently used as a faecal indicator bacterium
(FIB) for assessing water quality, the survival and
growth of E. coli in the environment raises concerns
regarding the use of this bacterium for indicating faecal
contamination. In addition, since some E. coli strains
and serotypes can cause human diseases, understanding
the ecology of this bacterium is important to prevent

570 Journal of Applied Microbiology 123, 570--581 © 2017 The Society for Applied Microbiology

J. Jang et al.
infection and spread of this pathogen to food, soil, and
water.
There are several review articles regarding the ecology
of E. coli in the environment (Ishii and Sadowsky 2008;
van Elsas et al. 2011). In this review, we update our cur-
rent knowledge regarding the survival and growth of
E. coli in the natural environment, with special emphasis
on the growth of pathogenic E. coli in the environment,
and the population genetics of environmental member of
the genus Escherichia. We also discuss the impact of envi-
ronmental E. coli on water quality and public health.
Escherichia coli as a faecal indicator bacterium to
evaluate water quality
Escherichia coli was initially believed to mainly inhabit the
lower intestinal tract of warm-blooded animals, including
humans, and be discharged to the environment through
faeces and wastewater treatment plants (Berthe et al.
2013). The concentration of E. coli per gram of faeces
varies among host species, typically reaching 107–109 in
human and 104–106 in domestic animals (Tenaillon et al.
2010). Escherichia coli is one of the predominant faculta-
tive aerobic bacterium in the intestinal tract, even though
the anaerobic bacteria outnumber E. coli by many orders
of magnitude (Berg 1996).
Based on the epidemiological studies done in the 1980s,
levels of E. coli in recreational water impacted by known
contaminant sources (e.g. sewage) was shown to correlate
with incidences of gastrointestinal illnesses (USEPA 1986;
Edberg et al. 2000). This led to the use of E. coli as an indi-
cator of faecal contamination in recreational water samples
(USEPA 1986). Based on the U. S. Environmental Protec-
tion Agency (USEPA)’s Ambient Water Quality Criteria
for Bacteria (USEPA 1986), water contact is not recom-
mended in freshwater beaches when E. coli levels are: (i)
over 235 colony-forming units (CFU) per 100 ml from a
single water sample, or when the geometric mean exceeds
126 CFU per 100 ml from at least five water samples col-
lected over a 30-day period.
Historically, culture-based methods (e.g. the membrane
filtration technique with selective growth media, defined
substrate technology and the most probable number
[MPN] technique) (Rice and Bridgewater 2012) have
been used to enumerate E. coli from recreational waters
and other water bodies. Defined substrate technology,
which uses an enzyme–substrate complex principle, has
been used to enumerate E. coli in environmental samples
(Edberg et al. 1990). The technique is based on the
E. coli-specific enzyme, b-glucuronidase. For example,
modified mTEC agar medium contains a substrate to
detect b-glucuronidase activity and allows for rapid and
specific E. coli detection (USEPA 2006). Furthermore,
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Environmental E. coli
commercially available kits (e.g. Colilert-18 and Quanti-
Tray/2000 system, IDEXX Laboratories, Westbrook, MA)
for the quantitative determination of E. coli from water
samples have been developed to reduce the time required
for analyses. While this technique has made the analytical
procedures of E. coli detection straightforward, and time-
and cost-effective, some E. coli strains (e.g. O157:H7 sero-
type strains) cannot be detected because they lack b-glu-
curonidase activity (Rump et al. 2012).
Escherichia coli as a human pathogen
Escherichia coli includes not only commensal strains but
also pathogenic ones that cause a variety of human dis-
eases—resulting in more than 2 million deaths each year
(Kaper et al. 2004). There are six well-studied intestinal
pathotypes of E. coli, including Shiga toxin-producing
E. coli (STEC), enteropathogenic E. coli (EPEC), entero-
toxigenic E. coli (ETEC), enteroaggregative E. coli
(EAEC), diffusely adherent E. coli and enteroinvasive
E. coli, including Shigella strains. These strains are classi-
fied by virulence properties and pathogenicity mecha-
nisms causing gastrointestinal diseases such as diarrhoea
(Nataro and Kaper 1998; Kaper et al. 2004). Entero-
haemorrhagic E. coli (EHEC) is one type of STEC that
can cause severe enteric diseases, such as haemolytic
uraemic syndrome and haemorrhagic colitis (Kaper et al.
2004) leading to acute renal failure and often death.
Escherichia coli O157:H7, the most well-known serotype
of EHEC, has caused many outbreaks of water- and
food-borne diseases in many countries. The incidence of
non-O157 STEC has been increasing in recent years,
including those caused by serotypes O26, O45, O103,
O111, O121 and O145 (Farrokh et al. 2013). Some
E. coli strains can also cause extraintestinal diseases, and
are called extraintestinal pathogenic E. coli (ExPEC). The
ExPEC, which were defined by disease association,
include uropathogenic E. coli, neonatal meningitis-asso-
ciated E. coli and sepsis-causing E. coli (Dale and Wood-
ford 2015).
Pathogenic E. coli strains are implicated in many water-
borne outbreaks, and STEC and EPEC have been fre-
quently reported to be responsible for waterborne
outbreaks worldwide (Chandran and Mazumder 2015).
Pathogenic E. coli contamination of the environment may
occur through manure and other animal wastes, wastewa-
ters from slaughterhouses and effluent from wastewater
treatment plants (Baliere et al. 2015). Although extensive
studies have been done on the clinical aspects of the patho-
genic E. coli strains, including mode of pathogenesis, diag-
nosis and sources (Kaper et al. 2004; Croxen et al. 2013),
their prevalence in the environment has not been exten-
sively examined in greater detail. This emphasizes the need
571

Environmental E. coli
for additional studies to understand the ecology of these
bacteria in extraintestinal environments.
Escherichia coli as an antibiotic resistant
bacterium
Since E. coli commonly resides in the intestines of warm-
blooded animals, it is subjected to frequent encounters
with antibiotics, providing it with high selection pressure
leading to resistance against antibiotics consumed by its
host (Looft et al. 2012). This led to the hypothesis that
the antibiotic resistance patterns of E. coli strains from
different hosts could be used to track host origin (Har-
wood et al. 2014). While this method was subsequently
shown not to be useful for its intended purpose, specific
E. coli phylogenetic groups were shown to exhibit differ-
ent resistance levels to antibiotics, regardless of the acqui-
sition of resistance, indicating that the genetic
background of E. coli also affects its antibiotic resistance
pattern (Tenaillon et al. 2010; Brisse et al. 2012).
Natural environments, such as water, soils and wastew-
ater treatment plants, have been considered to be bacte-
rial genetic reactors, in which active genetic exchanges
routinely occur among different bacteria, similar to that
which occur in the host intestine (Baquero et al. 2008).
Genes encoding antibiotic resistance are frequently associ-
ated with mobile genetic elements, such as plasmids and
transposons, which can be exchanged between bacteria
belonging to different phylogenetic lineages (Wellington
et al. 2013). Many previous studies have reported mul-
tidrug-resistant E. coli strains found in the environment,
indicating possible public health risks derived from
human activities (Dhanji et al. 2011; Walsh et al. 2011;
Jang et al. 2013).
Diversity of Escherichia coli
Commensal and pathogenic E. coli strains display diverse
phenotypic and genotypic variants. E. coli has been tradi-
tionally serotyped based on three types of somatic (O),
capsular (K) and flagellar (H) antigens, and more than
700 E. coli serotypes have been identified based on the
combination of O and H antigens (Nataro and Kaper
1998). Escherichia coli strains can be also classified into
several phylogenetic groups: A, B1, B2 and D (Clermont
et al. 2000). Recently, the E. coli phylogenetic grouping
has been revised based on multilocus sequence typing
(MLST) and genome sequence data to include the new
groups C, E, F and Escherichia clade I, which are compar-
atively rare to the major phylogenetic groups (i.e. A, B1,
B2 and D) (Clermont et al. 2013). Clermont et al. (2013)
developed a multiplex PCR system to rapidly classify
E. coli strains into one of the seven phylogenetic groups
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J. Jang et al.
(A, B1, B2, C, D, E, F and Escherichia clade I) without
performing MLST, sequencing and other time-consuming
approaches. In general, strains belonging to different phy-
logenetic group show different phenotypic and genotypic
traits (Gordon 2004; Meric et al. 2013); thus, phyloge-
netic group identification of unknown E. coli strains may
provide important information regarding their physiolog-
ical and ecological properties.
Escherichia coli strains vary in other phenotypic charac-
teristics, such as ability to form biofilms and utilization
of carbon sources (Cooper and Lenski 2000). This diver-
sity of E. coli has been explained by the impact of the
genomic makeup of the organism adapting to the host
intestinal or the extraintestinal natural environments (van
Elsas et al. 2011). Horizontal gene transfer plays an
important role in the acquisition of new genes in E. coli
(Doi et al. 2012), while genetic mutations can also con-
tribute to the E. coli phenotypic diversity such as carbon
metabolism (Cooper and Lenski 2000). While about 2000
genes commonly appear in multiple E. coli genomes (i.e.
core genes), there are many strain- or group-specific
genes, increasing the size of the E. coli pan-genome to
>18 000 genes. This suggests the great impact of horizon-
tal gene transfer for genomic plasticity of the E. coli
(Touchon et al. 2009). It has been suggested that E. coli
strains adapted to specific hosts would lose fitness in
other environments (Franz and van Bruggen 2008), sug-
gesting that phenotypic variation in E. coli may be due to
ecological adaptation.
Escherichia coli is highly diverse at the genotypic level
as well. High genotypic diversity has been identified in
E. coli based on the repetitive extragenic palindromic
PCR (rep-PCR) DNA fingerprinting (Jang et al. 2011,
2013, 2015; Byappanahalli et al. 2012) and pulsed field
gel electrophoresis (Johnson et al. 2013). Such genotypic
diversity appears to be common among environmental
strains (Byappanahalli et al. 2007; Ishii and Sadowsky
2008). Whole-genome typing methods such as the rep-
PCR DNA fingerprinting technique can reveal the alter-
ation of microbial genome structures, which allows these
techniques to be used in studying plasticity, molecular
phylogeny, and evolution of microbial genomes (Ishii
and Sadowsky 2009).
Escherichia coli in intestinal tracts of warm-
blooded animals
Escherichia coli may have evolved to grow in the intestinal
tract of warm-blooded animals where carbon/energy
sources are abundantly present with high moisture and
moderate pH and temperature. Many E. coli strains are
acid-resistant because they need to pass through the low-
pH environment in the animal/human stomach to arrive
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J. Jang et al. Environmental E. coli

in the intestinal tract. Host intestinal conditions can

affect the E. coli population structure. Relative abundance
of E. coli phylogenetic groups depends on the host-animal
and diet (Gordon 2013). In addition, DNA fingerprinting
patterns of E. coli strains can be differentiated by their
host animals (Ishii and Sadowsky 2009; Gomi et al.
2014). Antibiotic resistance and nutrient utilization pat-
terns of E. coli may also contain host-specific phenotypic
traits, subjected to antimicrobial agents and diets con-
sumed by different hosts (Hagedorn et al. 2003; Sayah
et al. 2005). However, these characteristics are not as
stable as genotypic ones.
Since E. coli has been used as a faecal indicator in
waterways, host-specific traits of E. coli strains have been
used with some success to identify potential sources of
the faecal pollution (i.e. microbial source tracking; MST)
(Ishii et al. 2007; Wang et al. 2013). Potential sources of
E. coli can be identified either by (i) comparing host-spe-
cific characteristics (e.g. DNA fingerprinting patterns) of
E. coli strains isolated from environment with those iso-
lated from known sources (i.e. library-dependent MST)
or by (ii) using host-specific marker genes of E. coli
which can be detected by PCR or via DNA probes (i.e.
library-independent MST) (Harwood et al. 2014). How-
ever, because of the large diversity within E. coli strains,
sources of the majority (>60%) of E. coli strains isolated
from beach environment may not be identified by
library-dependent method (Ishii et al. 2007). Increasing
the number of strains in a known source library may
improve MST results, but E. coli from nonanimal sources
also need to be included. In addition, it has been specu-
lated that E. coli does not have enough host specificity to
discriminate among its sources (Gordon 2001). This
could influence false-positive and -negative results of
host-specific markers when taking a library-independent
approach (Hamilton et al. 2010).
Survival and growth of Escherichia coli in natural
environment
Until relatively recently, E. coli was thought not to sur-
vive well outside of the host, as it was unable to replicate
in the environments (Winfield and Groisman 2003).
However, recent studies have shown that this bacterium
can survive for long periods of time outside of the
intestinal tract and reproduce in soil, sand and sediment
in tropical, subtropical and temperate climates (Ishii and
Sadowsky 2008). Some E. coli can become naturalized
(i.e. become part of indigenous microflora) in these envi-
ronments (Ishii et al. 2006). Naturalized E. coli genotypes
were distinct from animal-host origin E. coli genotypes
when repeatedly observed from the environment over
months or years (Ishii et al. 2006; Tymensen et al. 2015).
These populations have been reported in sand, soil and
sediments as well as in association with macrophytic
algae and periphyton (Ishii and Sadowsky 2008; Sad-
owsky and Whitman 2011).
Potentially pathogenic E. coli strains can also survive
and grow in natural environments. Byappanahalli et al.
(2015) detected high levels of eaeA, which encodes inti-
min of EPEC, in Cladophora mats. eaeA is one of the
most frequently detected pathogen genes in the environ-
ment (Hamilton et al. 2010; Ishii et al. 2014; Zhang et al.
2016). The concentrations of eaeA, as well as ftsZ and
uidA (genes used for E. coli-specific qPCR), increased in
the beach environments when conditions became favour-
able (Fig. 1), suggesting that eaeA-positive E. coli (i.e.
potential EPEC) can grow in these environments and
potentially influence water quality. Escherichia coli O157:
H7 and other pathogenic E. coli are also known to persist
in manure and on the surface of leafy green vegetables
(e.g. lettuce and spinach) and can cause food poisoning
outbreaks (Delaquis et al. 2007). Well-known examples

7 6
(a) (b)
(log copies per g algae)

6 5
Bacteria density

4
5
3
4
2
3 1

2 0
0 2 4 6 8 10 0 5 10 15 20 25 30 35
Time (day) Time (h)

Figure 1 Growth of indigenous Escherichia coli populations in (a) Cladophora mat under laboratory incubation conditions at 27°C and (b) Clado-
phora mat left at a field conditions. Density of both total E. coli (as measured by qPCR targeting ftsZ and uidA) and potential EPEC (as measured
by qPCR targeting eaeA) increased in the algae mat. Incubation and qPCR conditions are described in Whitman et al. (2014) and Byappanahalli
et al. (2015) respectively.

Journal of Applied Microbiology 123, 570--581 © 2017 The Society for Applied Microbiology 573

Environmental E. coli
include a spinach-associated outbreak of E. coli O157:H7
in 2006 (Jay et al. 2007) and a sprout-associated outbreak
of STEC O104 in 2011 (Frank et al. 2011). The persis-
tence of pathogenic E. coli is affected by several factors,
such as plant genotype, bacterial ability for plant colo-
nization and interactions with indigenous phytobacteria
(Martınez-Vaz et al. 2014). Interestingly, cellular
responses of enteric pathogens exposed to the vegetable
environment have been observed to include similar gene
expressions required to colonize the host intestine, indi-
cating that enteric bacteria may have the ability to colo-
nize vegetables by using similar mechanisms as are
required for animal cells (Goudeau et al. 2013). Various
antibiotic resistance genes have been also detected in
E. coli strains from the environment. Several E. coli
strains containing both extended-spectrum beta-lactamase
genes and virulence factors for intestinal and extraintesti-
nal pathotypes have been isolated from river water envi-
ronments (Jang et al. 2013). This is in contrast to studies
suggesting a trade-off between resistance and virulence of
E. coli (Johnson et al. 1991; Vila et al. 2002). The role of
environmental E. coli strains with respect to the dissemi-
nation of antibiotic resistance and virulence in natural
environments is currently not well understood and there-
fore needs to be clarified in the future.
Environmental factors influencing the growth
and survival of Escherichia coli
The growth and survival of E. coli in natural environ-
ments can be influenced by both biotic and abiotic fac-
tors (Rochelle-Newall et al. 2015). Abiotic factors include
temperature, water and nutrient availability, pH, and
solar radiation. Biotic factors include the presence of
other micro-organisms, and the ability of E. coli to
acquire nutrients, compete with other micro-organisms
and form biofilms in natural environments. These factors
are discussed in detail below:
Temperature
Temperature is probably the most important factor influ-
encing E. coli survival and growth in the environment.
While temperature is stable and optimal for E. coli growth
(36–40°C) in the intestinal tract of warm-blooded animals,
temperature in natural environment is generally low
(<30°C). Escherichia coli can grow in soil at temperatures
>30°C, although their death rate is faster in warm (>30°C)
than cold (<15°C) temperatures (Ishii et al. 2006, 2010).
For example, E. coli survived for over 6 months in sun-
dried algal mats stored in airtight plastic bags at 4°C
(Whitman et al. 2003), indicating that E. coli have the abil-
ity to survive long term under temperature conditions
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J. Jang et al.
lower than that in host bodies. Fluctuating temperature
conditions can also influence E. coli survival and growth.
Soil-borne E. coli grow and maintain their populations bet-
ter in temperature-fluctuating conditions than under con-
stant warm temperature conditions (Ishii et al. 2010).
However, survival and growth ability of E. coli in tempera-
ture-fluctuating conditions may vary by genotype. Lower
survival rates of E. coli O157:H7 in manure were observed
under fluctuating temperature conditions as compared to
constant temperatures, and a larger amplitude of tempera-
ture fluctuation reduced E. coli growth more than smaller
amplitudes (Semenov et al. 2007).
Water availability
Natural or substrate-induced (salt or sugar) low water
activity (or potential) controls what microbes have the
potential to grow given that all other factors are in
acceptable tolerance ranges. Desiccation is one of the
common stresses to bacteria in natural environments
(Evans and Wallenstein 2012). Rehydration can cause an
anoxic environment around the cells (van Elsas et al.
2011); therefore, E. coli and other bacteria need to adjust
their membranes and gene regulation to adapt to the des-
iccation and rehydration cycles (Evans and Wallenstein
2012). Growth of E. coli in the soil environment was neg-
atively influenced by soil desiccation; while E. coli survival
rates were not different between dried and wet soils (Ishii
et al. 2010). Upon rehydration, E. coli that survived in
desiccated soil showed growth, indicating that water
availability is critical for E. coli to grow.
Nutrient availability
The availability of nutrients such as carbon, nitrogen and
phosphorus is also an important factor influencing E. coli
survival and growth in the environment. Natural environ-
ments are generally low in readily available nutrients
compared with the intestinal tract of warm-blooded ani-
mals. Escherichia coli is versatile in energy acquisition and
can degrade various kinds of carbon substrates, including
aromatic compounds (Dı́ az et al. 2001). In addition,
E. coli showed a catabolic flexibility under glucose-limited
conditions, resulting in the efficient uptake of diverse car-
bon sources (Franchini and Egli 2006). Such versatility
and flexibility in energy and carbon acquisition should
help E. coli survive and grow in the environment (Ishii
and Sadowsky 2008; Brennan et al. 2013).
pH
Environmental pH can also influence the survival and
growth of E. coli in soil, and the level of pH resistance

J. Jang et al.
varies by strains (van Elsas et al. 2011). Escherichia coli
serotype O157:H7 strains showed superior survival at low
pH, as compared to non-O157 E. coli strains (Lin et al.
1996). Similar to acidophiles, some E. coli O157:H7
strains can survive better at low pH than at relatively
high pH (van Elsas et al. 2011). Therefore, specific E. coli
strains could survive selectively, influenced by local pH of
the environment. Escherichia coli uses several well-studied
mechanisms, such as the decarboxylase/antiporter-depen-
dent acid resistance systems, to resist low pH (Foster
2004).
Solar radiation
Solar radiation is the most effective abiotic factor causing
death of FIB in environmental waters. The inactivation
process of FIB by sunlight involves three major mecha-
nisms utilizing photobiological, photooxidative and pho-
tochemical pathways. Solar radiation, especially those in
the lower wavelengths (i.e. ultraviolet (UV) light) can
directly cause DNA damage (photobiological mechanism)
and oxidation of cellular contents (photooxidative mech-
anism), but these mechanisms are effective only at depths
to which sunlight reaches (e.g. upper surface water)
(Whitman et al. 2004). Since water is an effective filter of
light, this mostly occurs in the upper water column
(<22 cm depth) or on the soil surface. In the photochem-
ical inactivation process, oxygen-free radicals (O) and
hydrogen peroxides (H2O2) are produced when oxygen
(O2) and organic matter are exposed to sunlight. These
destructive chemicals can be delivered to the deeper areas
(90 cm depth) of the water environment (Whitman et al.
2004). The effect of sunlight on the E. coli survival may
vary by insolation time or turbidity of the water environ-
ment. In soil and sediment, E. coli may receive less
impact from sunlight than in the water environment.
Presence of other micro-organisms
Escherichia coli interacts with other micro-organisms in
all natural habitats. Escherichia coli can be predated by
protozoa and lysed by phages. These two biological
mechanisms have been reported to be responsible for up
to 70% of the FIB removal over 120 h in river water
(Korajkic et al. 2014). Escherichia coli also needs to com-
pete with indigenous micro-organisms for limited nutri-
ent sources, and defend themselves from antagonism in
the environment. Escherichia coli populations grew much
better in sterile vs nonsterile soils, indicating that micro-
biota has a crucial effect on E. coli survival (Unc et al.
2006; Ishii et al. 2010). The survival of E. coli populations
recently introduced into the environment is also affected
by the diversity of the indigenous microbial community.
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Environmental E. coli
For example, the survival of an introduced E. coli O157:
H7 strain and the diversity of the indigenous microbial
community were observed to be in inverse proportion
(van Elsas et al. 2011), suggesting that the ecological
niches fully filled with highly complex microbiota may be
difficult to invade.
Ability to form biofilms
Biofilms formed by E. coli on surfaces in aquatic environ-
ments, such as sediments, is a well-known factor contribut-
ing to the persistence of E. coli in natural environments
(Lee et al. 2006). Biofilms protect the bacteria from hostile
environmental conditions such as UV radiation, desicca-
tion, protozoan predators, and chemicals including antibi-
otics and disinfectants (McDougald et al. 2012). They also
may provide bacteria with a source of nutrients. Bacterial
cells detached from mature biofilms can be transported to
other locations by increased flow rates in aquatic environ-
ments and result in the building of new biofilms (McDou-
gald et al. 2012), indicating that biofilm-borne E. coli can
be transported to alternate sites and observed without evi-
dence of faecal contamination in the environment.
Differential survival/growth ability among Escherichia
coli strains
The ability of E. coli strain to acquire nutrients, compete
with other micro-organisms, survive and grow in the
environment is likely to vary by strains and genotype.
Thus, differential survival/growth ability among E. coli
strains could cause a shift in E. coli populations in
wastewater or faecal-impacted sediments (Anderson et al.
2005) and in manure-amended soil (Topp et al. 2003).
Population genetics of environmental E. coli strains is dis-
cussed in further detail below.
Population genetics of environmental Escherichia
coli strains
The environmental conditions within which E. coli resides
has been suggested to influence the genomic traits of the
bacterium (Tenaillon et al. 2010). In the host-animal
intestine, E. coli population structure is determined by
the conditions of the gastrointestinal tract, which in turn,
is influenced by host physiology and diet. Similarly, the
genetic structures of E. coli populations in the natural
environment are shaped by abiotic and biotic environ-
mental factors (van Elsas et al. 2011). Multiple studies
have reported unique E. coli genotypes representative of
environmentally adapted strains (Anderson et al. 2005;
Ishii et al. 2006; Ishii and Sadowsky 2008; Byappanahalli
et al. 2012).
575
 13652672, 2017, 3, Downloaded from https://ami-journals.onlinelibrary.wiley.com/doi/10.1111/jam.13468 by Nat Prov Indonesia, Wiley Online Library on [22/02/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Environmental E. coli J. Jang et al.

Number of genes
100
Environmental
C-IV Salmonella typhi
50 C-V

1 C-III

E. albertii C-I

E. fergusonii
E
E. fergusonii
B1
ATCC 35469
A B2

Enteric

C-I TW08933
TW15818 E. albertii
TW15838 TW10509 B156

(A)
Commensal MG1655
(B1)
shigella
TW09308
EHEC C-V
(E) E1118
UTI89
APEC UPEC
TW09276
(B2) TW09231
E. coli TW14182 TW11588 C-III
H605 0·01
C-IV

Figure 2 Phylogenic relationships of commensal and environmental Escherichia strains. The phylogenetic network was constructed based on the
1910 core gene sequences. Phylogenetic grouping of Escherichia strains (A, B1, B2, C (subgroups I, III, IV and V) and E) is shown in parenthesis.
The circular tree shows the amount of recent horizontal transfer of core genes between the genomes of the clades. The thickness of the line is
proportional to the number of genes transferred (scale at upper left in figure). Adapted from Luo et al. (2011) with permission from the
publisher. [Colour figure can be viewed at wileyonlinelibrary.com]

Comparative genomic analysis between environmen-
tally adapted E. coli strains and other enteric E. coli
strains have expanded the understanding of the evolu-
tionary lineage of this bacterium. Whole-genome phylo-
genetic analysis was performed using nine environmental
E. coli strains, which survived better in the external envi-
ronment than in the human intestine (Walk et al. 2009;
Ingle et al. 2011). These studies showed that these envi-
ronmental strains belonged to clades distantly divergent
from enteric E. coli and other Escherichia strains (Luo
et al. 2011) (Fig. 2). Therefore, strains in the environ-
mental Escherichia clade may represent novel species even
though they are indistinguishable from E. coli based on
traditional phenotypic tests (Luo et al. 2011), as well as
the 16S rRNA gene-based phylogenetic analysis. While
members of the environmental Escherichia clade generally
did not contain nine genes (malX, eaaG, sfa-focDE, sat,
stx1, hlyD, papA, pic and espC) among 27 genes of the
E. coli pan-genome, three genes (uidA, gadAB and fimH)
were frequently present (Walk et al. 2009), which support
the usefulness of uidA as a marker gene for E. coli and
environmental Escherichia clades. Genetic exchange of
core genes was detected, but only within the environmen-
tal clade or within enteric E. coli strains and not between
environmental clades and enteric E coli strains (Luo et al.
2011) (Fig. 2). This indicates that there could be possible
ecological barriers to gene flow between environmental
and enteric Escherichia strains. Genome sequencing of
additional environmental Escherichia strains is needed to
confirm this initial observation.
Environmental and commensal Escherichia strains may
differ in terms of growth and survival mechanisms.

576 Journal of Applied Microbiology 123, 570--581 © 2017 The Society for Applied Microbiology

J. Jang et al.
Comparative transcriptome analysis suggests that envi-
ronmental Escherichia strains are likely better adapted to
low-nutrient conditions (Vital et al. 2015). Compared
with commensal strains, environmental Escherichia strains
showed higher levels of transcription for stress defence
genes under carbon-limited growth conditions. They also
showed survival-like phenotype, that is, not investing
energy to stay alert for nutrient scavenging/assimilation
under low-nutrient conditions.
Implication for water quality and public health
We now know that some Escherichia populations can sur-
vive and grow in environmental conditions for prolonged
periods (Ishii and Sadowsky 2008; van Elsas et al. 2011).
Environmentally adapted Escherichia strains are indistin-
guishable from faecally derived strains based on current
water quality testing methods and may not indicate the
occurrences of recent faecal contamination. Therefore,
the presence of environmental Escherichia populations
severely confounds the use of this bacterium as a FIB. In
a study by Byappanahalli et al. (2015), high levels of
E. coli in water most likely originated from algae or beach
sand, not from faecal droppings. In addition, poor corre-
lations between concentrations of E. coli and those of
enteric pathogens (e.g. Wu et al. 2011; Ishii et al. 2014)
may be due, in part, to the occurrences of environmental
Escherichia populations. FIB-based methods need to be
improved to specifically quantify only E. coli of faecal ori-
gin (e.g. source-specific qPCR). Alternatively, FIB-inde-
pendent water quality monitoring, such as direct
multipathogen quantification (Ishii et al. 2014; Byappana-
halli et al. 2015) may be a better predictor of human
health risks.
The long-term survival and growth of E. coli in the
environment is also of concern if they carry virulence fac-
tor or antibiotic resistance genes. Because intimin,
encoded by eaeA, is the most important virulence factor
for EPEC (Kaper et al. 2004), eaeA-positive E. coli may
cause human diseases. Therefore, environmental survival
and growth of eaeA-positive E. coli should be considered
as a potential human health hazard. The gene eaeA is
located on a pathogenicity island, known as locus of
enterocyte effacement (LEE), which can be horizontally
transferred (Kaper et al. 2004; Hazen et al. 2013). The
LEE pathogenicity island was distributed to phylogeneti-
cally diverse groups of EPEC (Hazen et al. 2013),
although environmental eaeA-positive E. coli strains were
not included in their study. In addition to the virulence
factor genes, antibiotic resistance genes can be also trans-
ferred among E. coli, including environmental strains,
which is also of great concern for public health (Touchon
et al. 2009; Wellington et al. 2013).
Journal of Applied Microbiology 123, 570--581 © 2017 The Society for Applied Microbiology
13652672, 2017, 3, Downloaded from https://ami-journals.onlinelibrary.wiley.com/doi/10.1111/jam.13468 by Nat Prov Indonesia, Wiley Online Library on [22/02/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Environmental E. coli
Conclusions and future perspectives
Based on studies done in the past few decades, the pres-
ence of environmental Escherichia is now well recognized.
These environmental E. coli may be of animal-origin and
have become adapted to their surrounding environments;
or may retain the characteristics of their ancestral linage,
which was environmental bacteria using soil and sedi-
ment as their primary habitat. More data are needed,
especially genomic information of environmental Escheri-
chia strains, to clarify the evolutionary history of environ-
mental E. coli. There are many questions still remaining,
including: (i) can environmental Escherichia still colonize
the intestinal tract of warm-blooded animals? (ii) how do
these bacteria influence current water quality monitor-
ing?; and (iii) are these bacteria potentially pathogenic to
humans? Further research is needed to answer these
questions.
Acknowledgements
This work was supported, in part, by the University of
Minnesota’s Discovery, Research and InnoVation Econ-
omy (MnDRIVE) initiative. Any use of trade, firm, and
product names is for descriptive purposes only and does
not imply endorsement by the US Government.
Conflict of Interest
The authors have no conflict of interest to declare.
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