In 1884, the German microbiologist and pediatrician Theodor Escherich began a study of infant gut microbes and their role in digestion and disease. During this study, he discovered a fast-growing bacterium that he called Bacterium coli commune, but which is now known as the biological rock star that is Escherichia coli (Escherich, 1988; Shulman et al., 2007; Zimmer, 2008). E. coli's meteoric rise and exalted status in biology stem from how easy it is to find and work with. Hardy, non-pathogenic, and versatile strains that grow quickly on many different nutrients can be isolated from virtually any human. These traits made E. coli a mainstay in microbiology teaching lab collections. Consequently, when early 20^th century microbiologists cast about for a model organism, E. coli was one of the most widely available choices.

Those who chose to work with E. coli included Bordet and Ciuca (1921), Werkman (1927), Wollman (1925), Wollman and Wollman (1937) and Bronfenbrenner and Korb (1925), Bronfenbrenner (1932), who between them performed groundbreaking studies on bacterial physiology, viruses, and genetics (Daegelen et al., 2009). By the 1940s, its use in many foundational studies firmly established E. coli as the bacterial model organism of choice, making it the obvious organism to work with at the onset of the molecular biology revolution in the 1950s. As a result, it became the organism in which the most basic aspects of life, including the genetic code, transcription, translation, and replication, were first worked out (Crick et al., 1961; Nirenberg et al., 1965; see Judson, 1996 for an excellent history of early molecular biology and E. coli's role in it). The resulting knowledge and molecular methods for investigating and manipulating its biology have since led to E. coli's prominence in academic and commercial genetic engineering, pharmaceutical production, and experimental microbial evolution (see Box 1 for a glossary of specialist terms used in this article ), not to mention the biotechnology industry, which contributed $500 billion to the global economy in 2011 (Cohen et al., 1973, Schaechter and Neidhardt, 1987; Lenski, 2004; Bruschi et al., 2011; Kamionka, 2011; Huang et al., 2012; Kawecki et al., 2013). It is not hyperbole to say that E. coli is now the most important model organism in biology (Zimmer, 2008; see Box 2).

For all of its importance, E. coli is quite nondescript. It is a fairly typical Gram-negative bacillus (see ‘Glossary’), measuring only about 1 μm long by 0.35 μm wide, although this can vary considerably depending on the strain and its conditions. Even at high magnification it looks like nothing more than a tiny sausage (Figure 1A). It may have whip-like flagella that it uses to move about its environment, or hair-like pili that allow it to attach to surfaces or to other cells (Figure 1B). Physiologically, it is a facultative aerobe, meaning that it can grow happily with or without oxygen, but it cannot grow at extremes of temperature or pH nor can it degrade dangerous pollutants, photosynthesize, or do a variety of other things that interest microbiologists. Phylogenetically, it is a member of the Enterobacteriaceae, and is closely related to such pathogens as Salmonella, Klebsiella, Serratia, and the infamous Yersinia pestis, which causes plague (Brenner and Farmer, 2007).

Figure 1

Download asset Open asset

In nature, E. coli is principally a constituent of the mammalian gut microbiome (see ‘Glossary’), but it is also found, albeit less commonly, in the gut microbiomes of birds, reptiles and fish, as well as in soil, water, plants, and food (Hartl and Dykhuizen, 1984; Leimbach et al., 2013). Its mammalian abode is why E. coli can metabolize lactose, the control of which was the subject of seminal studies of gene regulation (Jacob et al., 1960; Jacob and Monod, 1961). E. coli is typically the most common aerobe in the lower intestine of mammals. However, the gut is primarily an anoxic environment, and the extremely large, highly diverse (500+ taxa) gut microbial community is dominated by obligate anaerobes, such as members of Bacteroides and Firmicutes, which alone comprise ∼90% or more of the total gut microbial population (Bäckhed et al., 2005; Eckburg et al., 2005; Claesson et al., 2009; Tenaillon et al., 2010). By contrast, E. coli typically constitutes only 0.1–5% of the community, which partly reflects the fact that its niche is to be found in the relatively thin layer of mucus that lines the gut. In the mucus layer, E. coli grows in a complex, multi-species biofilm (see ‘Glossary’) in which it competes for an array of nutrients—one of the origins of its broad diet (Chang et al., 2004; Beloin et al., 2008). This rich food supply enables E. coli to maintain population densities of 10⁶–10⁹ cells per gram of fecal matter despite unavoidable and regular bulk losses (Savageau, 1983; Chang et al., 2004). In the human gut, the E. coli population typically includes a set of long-term residential strains, and also short-term transients that vary with diet, health, and with exposure to antibiotics (Sears et al., 1950; Savageau, 1983). The human gut E.coli population also varies due to its constant, largely unknown interactions with the broader microbiome, and with the host and the host's vast virome (see ‘Glossary’), against which it defends itself with restriction enzymes, which have become a key tool in molecular biology (see ‘Glossary’) (Kasarjian et al., 2003; Roberts, 2005; Minot et al., 2011; He et al., 2013; Shoaie et al., 2013; Virgin, 2014).

A host organism carefully regulates its microbiome in poorly understood ways that have an impact on its health (Schluter and Foster, 2012). For instance, the human gut secretes immunoglobulin A, which appears to facilitate the formation of E. coli biofilms on the intestinal mucosa, suggesting that their presence is welcome (Bollinger et al., 2003). While long considered to have a commensal relationship with its host, in which E. coli secures food and a nice warm home while contributing little in return, it is increasingly clear that the host-E. coli relationship is really a mutualism. Indeed, E. coli benefits its host in a number of ways. It produces vitamin K and vitamin B12, both of which are required by mammalian hosts (Bentley and Meganathan, 1982; Lawrence and Roth, 1996). E. coli also maintains a friendly environment for its anaerobic neighbors by consuming oxygen that enters the gut. Perhaps most importantly, E. coli competitively excludes pathogens from its niche in the gut, rather like how friendly barbarian tribes, settled by the Roman Empire on its frontiers, helped to keep out the more dangerous tribes (Chang et al., 2004).

E. coli's relationship with a host literally begins at birth. Newborns are typically inoculated with maternal E. coli through exposure to her fecal matter during birth and from subsequent handling (Nowrouzian et al., 2003; Leimbach et al., 2013). Although perhaps disconcerting to ponder, this inoculation seems to be quite important. Indeed, E. coli becomes more abundant in the mother's microbiome during pregnancy, increasing the chances of her newborn's inoculation (Koren et al., 2012). The colonizing strains typically have secretion systems and pili that allow them to attach to and interact with the infant's gut epithelium (Feeney et al., 1980; de Muinck et al., 2013). This newly established and rapidly growing E. coli population then changes the structure and function of the epithelial cells in ways that appear crucial for healthy microbiome development (Tomas et al., 2015). It is therefore concerning that early human infant colonization by E. coli has been declining in the US and in other Western nations as rates of caesarean delivery have increased and hospital hygiene has continued to improve (Grönlund et al., 1999; Nowrouzian et al., 2003; Adlerberth, 2006). Indeed, this decrease has been accompanied by broader microbiome changes, including increased infant gut colonization by Staphylococcus aureus, which is linked to an increased risk of developing a variety of disorders, including asthma, obesity, and diabetes (Lindberg et al., 2000, 2004; Neu and Rushing, 2011; Sannasiddappa et al., 2011; Rudi et al., 2012; Azad et al., 2013; Moeller et al., 2014). The long-term consequences of disrupting humanity's long association with E. coli are under intensive investigation.

An inevitable consequence of being a gut microbe is to be regularly excreted into the external world. The mucus lining of the gut is constantly sloughed off and excreted in fecal matter, so cells of a resident E. coli population are shed almost as soon as that population is established. E. coli's long-term life cycle is hence biphasic, and despite being exquisitely adapted to the good life inside of a host, E.coli must also be adapted to successfully acclimate to a harsher life outside the host (Savageau, 1983). This is a remarkable feat. Whereas life on the inside is easy and stable, every aspect of the external environment, be it nutrition, temperature, oxygen, moisture, pH, and/or the surrounding microbial community, can fluctuate wildly (Savageau, 1983; Winfield and Groisman, 2003; van Elsas et al., 2011). It is likely that the hardiness, metabolic flexibility, and substrate breadth that have made E. coli such a valuable model organism evolved in part to permit it to survive this hostility and variability long enough to make it back to a host (van Elsas et al., 2011).

Another interesting trait that is almost certainly relevant to E. coli's survival of its environmental phase is the production of persister variants. First observed in Staphylococcus during experiments with penicillin, persisters are rare, highly antibiotic-tolerant phenotypic variants that arise at random in bacterial populations (Hobby et al., 1942; Bigger, 1944; Balaban et al., 2004; Lewis, 2010; Zhang, 2014). Persisters are not an adaptation specifically to antibiotics; their hallmark antibiotic tolerance is attributable to their metabolic inactivity, which is triggered by several redundant pathways, including those that govern stress response (Shah et al., 2006; Lewis, 2010; Amato et al., 2013; Amato and Brynildsen, 2014). Persistence therefore appears to be a general adaptation that permits small numbers of dormant cells to survive a variety of environmental fluctuations. E. coli has been, as with so many other phenomena, a model in which to study bacterial persistence, and it seems likely that this capacity to enter a dormant state plays a significant role in surviving the considerable fluctuations it encounters in its external environment.

The external world was long thought to be so harsh as to preclude E. coli's growth outside of its host. While a tiny minority might eventually reach a new host, most cells were expected to eventually die. This is the basal assumption behind using the presence of E. coli as an indicator of fecal contamination. However, recent studies have shown that E. coli can, in fact, establish itself as a member of microbial soil, water, and plant-associated communities (Lopez-Torres et al., 1987; Ishii and Sadowsky, 2008; Texier et al., 2008; Brennan et al., 2010; Berthe et al., 2013; Dublan et al., 2014). Moreover, genomic and phylogenetic analyses of collections of E. coli strains have identified divergent lineages that appear to be adapted to a primarily non-host lifestyle (Walk et al., 2009). What adaptations are required for E. coli to make such radical ecological shifts, what niches it fills in its new communities, how stable its presence in those communities might be, and what impact its adaptation to these new niches might have on its capacity to return to a host remain outstanding questions that must be addressed (see Box 3).

It is possible that these environmental E. coli populations will help resolve the interesting problem of swarming motility. It has long been observed that groups of E. coli cells on water-restricted surfaces will congregate and engage in social, coordinated movement over the surface, a behavior also seen in other bacteria (Harshey and Matsuyama, 1994; Harshey, 2003; Partridge and Harshey, 2013a,b). However, swarming has principally been observed and studied on agar plates in the lab (Partridge and Harshey, 2013a). What function it might serve for E. coli in nature has been unclear. The gut generally lacks the sorts of surfaces on which swarming works. Given that ∼216 E. coli genes are specifically involved in swarming motility, it is a costly trait that would not be maintained if it did not confer some selective benefit (Inoue et al., 2007). It is as yet unclear if swarming plays any role in the initial colonization of the gut, but it is associated with pathogenesis, likely due to its improved colonization of tissue surfaces that facilitate opportunistic infection (see the next section) (Zhang et al., 2010; Partridge and Harshey, 2013a). Given that surfaces, and interfaces between surfaces, are regularly encountered by environmental bacteria, swarming may well prove to be an adaptation that enables the exploration and colonization of viable habitats by E. coli upon their excretion into the external environment.

E. coli's presence in the environment is a cause for concern because its relationship with humans is not entirely benign. Indeed, E. coli is a major cause of diarrheal diseases, peritonitis, colitis, bacteremia, infant mortality, and urinary tract infections that world-wide cost billions of dollars to treat and kill roughly 2 million humans each year (Russo and Johnson, 2003; Kaper et al., 2004). Some strains may even cause cancer (Arthur et al., 2012). Some opportunistic E.coli infections are caused by normally harmless or beneficial strains when introduced to sick hosts or to parts of a host's body outside of the gut (Kaper et al., 2004). However, there are also pathogenic strains that produce virulence factors and can cause illness in even the healthiest host. These strains are classified by where and how they cause disease into groups called pathotypes (see ‘Glossary’), which include enteroaggregative, enterohemorrhagic, enteropathogenic, enterotoxigenic, uropathogenic, meningitis-associated, and septicemic-associated E. coli (Kaper et al., 2004; Leimbach et al., 2013) (see ‘Glossary’).

The most notorious of these is E. coli O157:H7, an enterohemorrhagic strain that produces a shiga-like toxin (Griffin and Tauxe, 1991; Robinson et al., 2006). This toxin (see ‘Glossary’) attacks small blood vessels, killing intestinal cells, and causing bloody diarrhea and severe abdominal pain, as well as hemolytic uremic syndrome (HUS), a potentially deadly condition that can involve widespread clots in capillaries and hemolytic anemia, thrombocytopenia, and renal failure (see ‘Glossary’; Griffin et al., 1988; Kaper et al., 2004). Treatment can be difficult because antibiotics increase the risk of HUS. As a result, treatment is generally limited to the provision of fluids, adequate nutrition, medication for pain and fever, and blood transfusions when necessary (Bitzan, 2009; Smith et al., 2012).

O157:H7 is particularly dangerous because it can easily contaminate human food supplies. It resides asymptomatically in cattle and in other livestock, and can be transferred to humans via the fecal contamination of meat during its butchering and packaging (Ferens and Hovde, 2011). It can also contaminate vegetables via fertilizers and water, and through contact with live-stock-associated birds (Callaway et al., 2009, 2014). Through these points of entry into the human food chain, O157 has caused numerous outbreaks of illness (Frenzen et al., 2005; Rangel et al., 2005). In the US alone, such outbreaks have annually affected ∼63,000 individuals, killing 20, and costing around $405 million in healthcare and in lost productivity (Mead et al., 1999; Scallan et al., 2011). When E. coli gets bad press, O157:H7 is almost always the culprit, and rightfully so.

The many pathogenic strains of E. coli testify to the diversity of this single microbial ‘species’, the full extent of which was only revealed by the advent of whole-genome sequencing. For example, genome sequences have firmly placed all Shigella strains within the broader E. coli clade (Pupo et al., 2000; Lukjancenko et al., 2010; Kaas et al., 2012).

More importantly, sequencing has uncovered the remarkable plasticity and dynamism of the E. coli genome that contribute to its genetic and phenotypic diversity. In 2002, Welch et al. (2002) reported that three strains of E. coli, the popular lab strain K-12, O157:H7, and the uropathogenic strain CFT073, share only 39.2% of their genes. Subsequent sequencing of more strains has reduced this core genome to less than 20% of the more than 16,000 genes in the E. coli pan-genome (see ‘Glossary’; Lukjancenko et al., 2010; Kaas et al., 2012).

The remaining genes constitute the flexible genome (see ‘Glossary’), a vast pool of ‘plug and play’ genetic variation that can be acquired via horizontal gene transfer (Lukjancenko et al., 2010; Mira et al., 2010; Leimbach et al., 2013). This variation includes prophages, transposable elements, and accessory genes (see ‘Glossary’). These genes encode functions that can: improve fitness in particular niches; increase metabolic flexibility; and affect pathogenicity (Schmidt and Hensel, 2004; Touchon et al., 2009). Flexible genomic elements are often large and integrate into the genome at select insertion hotspots (Touchon et al., 2009). This capacity to mix and match accessory genetic elements means that new E.coli strains with novel combinations of traits can arise very quickly. Another consequence is that the size of the E. coli genome can vary greatly between strains. While standard lab strains have genomes of ∼4.5 million base pairs and 4000 genes, pathogenic strains can have genomes of over 5.9 million base pairs and 5500 genes (Blattner et al., 1997; Lukjancenko et al., 2010; de Muinck et al., 2013).

This extensive genetic plasticity poses major questions for understanding how E. coli evolves in the wild over the long-term. For instance, how does the rate of genomic evolution in a given E. coli lineage by mutation compare to that by horizontal gene transfer (Guttman and Dykhuizen, 1994; Dolbrindt et al., 2010; Paul et al., 2013)? Moreover, how much of the E. coli flexible genome ultimately derives from other organisms?

E. coli has been tremendously valuable as a de-contextualized, abstracted model organism, but it could be of even greater value were we to gain a better understanding of its ecology and natural history. As I have discussed, it is a highly diverse and broadly distributed species that occupies an expansive, generalized niche in which it experiences a vast range of environmental and ecological conditions. This breadth presents two unique and synergistic opportunities. First, the tools and techniques developed for, and the knowledge derived from, the study of E. coli's lab strains can be applied to studying its wild relatives in far greater detail than is possible for any other microbe. This capacity promises to yield new and profound insights into the biology of other microbes that experience similar conditions, as well as the discovery and identification of new microbiological phenomena. Second, any increase in our knowledge of E. coli's natural history expands the range of biological phenomena for which its strains can be used as models to study. In other words, the study of E. coli's natural history can reveal more than is possible with most organisms, and an increased understanding of its natural history in turn expands its potential as a model organism.

An example of this dynamic can be seen in studies of E. coli biofilms, which have revealed much about how harmless and pathogenic strains colonize the gut and persist in the environment (Wang et al., 2006; Beloin et al., 2008; Nesse et al., 2014; Vogeleer et al., 2014). These studies have, in turn, led to the development of E. coli as a model for studying the formation, genetics, physiology, and consequences of biofilms, generating important findings on this most common of microbial lifestyles (Beloin et al., 2008). Experimental evolutionary studies of E. coli biofilms have also led to findings of far-reaching consequence, such as how biofilms impact microbial evolution and how they facilitate the evolution of antibiotic resistance even when antibiotics are not present (Ponciano et al., 2009; Tyerman et al., 2013).

There are many unanswered questions about E. coli's natural history (see Box 3). How does E. coli adapt to non-host environments? What role does it play in non-host communities? How does it adapt to life in the soil? Just how fluid is the E. coli genome? How do environmental and ecological conditions affect this fluidity? How does the pan-genome evolve? How much interaction is there between E. coli's pan-genome and that of other microbes? How tightly adapted are hosts to their E. coli populations? How is E. coli adapting to changes in the human diet and lifestyle? Each unanswered question presents opportunities for novel research into unexplored corners of E. coli's natural history, and the subsequent expansion of its potential as a model. Improved appreciation and interest in E. coli's natural history can only uncover more questions, and increase its potential even more. If kept in mind by researchers, this dynamic will guarantee that the most important model organism of the 20^th century will continue to be one of the most important model organisms of the 21^st century and beyond.

1. 1. Adlerberth I
   2. Lindberg E
   3. Aberg N
   4. Hesselmar SR
   5. Strannegård IL
   6. Wold A

   (2006) Reduced enterobacterial and increased staphylococcal colonization of the infantile bowel: an effect of hygienic lifestyle?

   Pediatric Research 59:96–101.

   https://doi.org/10.1203/01.pdr.0000191137.12774.b2

   • Google Scholar
2. 1. Amato SM
   2. Brynildsen MP

   (2014) Nutrient transitions are a source of persisters in Escherichia coli biofilms

   PLOS ONE 9:e93110.

   https://doi.org/10.1371/journal.pone.0093110

   • Google Scholar
3. 1. Amato SM
   2. Orman MA
   3. Brynildsen MP

   (2013) Metabolic control of persister formation in Escherichia coli

   Molecular Cell 50:475–487.

   https://doi.org/10.1016/j/molcel.2013.04.002

   • Google Scholar
4. 1. Arthur JC
   2. Perez-Chanona E
   3. Mühlbauer M
   4. Tomkovich S
   5. Uronis JM
   6. Ting-Jia Fan
   7. Bampbell BJ
   8. Abujamel T
   9. Dogan B
   10. Rogers AB
   11. Rhodes JM
   12. Stintzi A
   13. Simpson KW
   14. Hansen JJ
   15. Keku TO
   16. Fodor AA
   17. Jobin C

   (2012) Intestinal inflammation targets cancer-inducing activity of the microbiota

   Science 338:120–123.

   https://doi.org/10.1126/science.1224820

   • Google Scholar
5. 1. Azad MB
   2. Konya T
   3. Maughan H
   4. Guttman DS
   5. Field CJ
   6. Chari RS
   7. Sears MR
   8. Becker AB
   9. Scott JA
   10. Kozyrkyi AL
   11. CHILD study Investigators

   (2013) Gut microbiota of healthy Canadian infants: profiles by mode of delivery and infant diet at 4 months

   Canadian Medical Association Journal 185:385–394.

   https://doi.org/10.1503/cmaj.121189

   • Google Scholar
6. 1. Bäckhed F
   2. Ley RE
   3. Sonnenburg JL
   4. Peterson DA
   5. Gordon JI

   (2005) Host-bacterial mutualism in the human intestine

   Science 307:1915–1920.

   https://doi.org/10.1126/science.1104816

   • Google Scholar
7. 1. Balaban NQ
   2. Merrin J
   3. Chait R
   4. Kowalik L
   5. Leibler S

   (2004) Bacterial persistence as a phenotypic switch

   Science 305:1622–1625.

   https://doi.org/10.1126/science.1099390

   • Google Scholar
8. 1. Barrick JE
   2. Yu DS
   3. Yoon SH
   4. Oh TK
   5. Schneider D
   6. Lenski RE
   7. Kim JF

   (2009) Genome evolution and adaptation in a long-term experiment with Escherichia coli

   Nature 461:1243–1247.

   https://doi.org/10.1038/nature08480

   • Google Scholar
9. 1. Beloin C
   2. Roux A
   3. Ghigo JM

   (2008) Escherichia coli biofilms

   Current Topics in Microbiology and Immunology 322:249–289.

   https://doi.org/10.1007/978-3-540-75418-3_12

   • Google Scholar
10. 1. Bentley R
    2. Meganathan R

    (1982)

    Biosynthesis of vitamin K (menaquinone) in bacteria

    Microbiological Reviews 46:241–280.

    • Google Scholar
11. 1. Berthe T
    2. Ratajczak M
    3. Clermont O
    4. Denamur E
    5. Petit F

    (2013) Evidence for coexistence of distinct Escherichia coli populations in various aquatic environments and their survival in estuary water

    Applied and Environmental Microbiology 79:4684–4693.

    https://doi.org/10.1128/AEM.00698-13

    • Google Scholar
12. 1. Bigger JW

    (1944) Treatment of Staphylococcal infections with penicillin

    Lancet 244:497–500.

    https://doi.org/10.1016/S0140-6736(00)74210-3

    • Google Scholar
13. 1. Bitzan M

    (2009) Treatment options for HUS secondary Escherichia coli O157:H7

    Kidney International Supplement 75:S62–S66.

    https://doi.org/10.1038/ki.2008.624

    • Google Scholar
14. 1. Blattner FR
    2. Plunkett G III
    3. Bloch CA
    4. Perna NT
    5. Burland V
    6. Riley M
    7. Collado-Vides J
    8. Glasner JD
    9. Rode CK
    10. Mayhew GF
    11. Gregor J
    12. Davis NW
    13. Kirkpatrick HA
    14. Goeden MA
    15. Rose DJ
    16. Mau B
    17. Shao Y

    (1997) The complete genome sequence of Escherichia coli K-12

    Science 277:1453–1462.

    https://doi.org/10.1126/science.277.5331.1453

    • Google Scholar
15. 1. Blount ZD
    2. Barrick JE
    3. Davidson CJ
    4. Lenski RE

    (2012) Genomic analysis of a key innovation in an experimental Escherichia coli population

    Nature 489:513–518.

    https://doi.org/10.1038/nature11514

    • Google Scholar
16. 1. Blount ZD
    2. Borland CZ
    3. Lenski RE

    (2008) Historical contingency and the evolution of a key innovation in an experimental population of Escherichia coli

    Proceedings of the National Academy of Sciences of USA 105:7899–7906.

    https://doi.org/10.1073/pnas.0803151105

    • Google Scholar
17. 1. Bollinger RR
    2. Everett ML
    3. Palestrant D
    4. Love SD
    5. Lin SS
    6. Parker W

    (2003) Human secretory immunoglobulin A may contribute to biofilm formation in the gut

    Immunology 109:580–587.

    https://doi.org/10.1046/j.1365-2567.2003.01700.x

    • Google Scholar
18. 1. Bordet J
    2. Ciuca M

    (1921)

    Remarques sur l’historique des recherches, concernant la lyse microbienne transmissible

    Comptes Rendus Biologies 84:745–747.

    • Google Scholar
19. 1. Brennan FP
    2. Abram F
    3. Chinalia FA
    4. Richards KG
    5. O'Flaherty

    (2010) Characterization of environmentally persistent Escherichia coli isolates leached from an Irish soil

    Applied and Environmental Microbiology 76:2175–2180.

    https://doi.org/10.1128/AEM.01944-09

    • Google Scholar
20. 1. Brenner DJ
    2. Farmer JJ III

    (2007)

    Bergey's Manual of Systematic Bacteriology

    587–850, Bergey's Manual of Systematic Bacteriology, Volume 2, New York, Springer, The Proteobacteria, Part B: The Gammaproteobacteria.

    • Google Scholar
21. 1. Bronfenbrenner JJ

    (1932) The heat inactivation of bacteriophages

    Proceedings of the Society for Experimental Biology and Medicine 29:802–804.

    https://doi.org/10.3181/00379727-29-6087

    • Google Scholar
22. 1. Bronfenbrenner JJ
    2. Korb C

    (1925) Studies on the bacteriophage of d’Herelle: II. effect of alcohol on the bactiophage of d’Herelle

    Journal of Experimental Medicine 42:419–429.

    https://doi.org/10.1084/jem.42.3.419

    • Google Scholar
23. 1. Bruschi F
    2. Dundar M
    3. Gahan K
    4. Gartland M
    5. Szente M
    6. Viola-Magni MP
    7. Akbarova Y

    (2011) Biotechnology worldwide and the ‘European biotechnology Thematic Network’ association (EBTNA)

    Current Opinion in Biotechnology 22:S7–S14.

    https://doi.org/10.1016/j.copbio.2011.05.506

    • Google Scholar
24. 1. Callaway TR
    2. Carr MA
    3. Edrington TS
    4. Anderson RC
    5. Nisbet DJ

    (2009)

    Diet, Escherichia coli O157:H7, and cattle: a review after 10 years

    Current Issues in Molecular Biology 11:67–79.

    • Google Scholar
25. 1. Callaway TR
    2. Edrington TS
    3. Nisbet DJ

    (2014) Isolation of Escherichia coli O157:H7 and Salmonella from migratory brown-headed cowbirds (Molothrus ater), common Grackles (Quiscalus quiscula), and cattle egrets (Bubulcus ibis)

    Foodborne Pathogens and Disease 11:791–794.

    https://doi.org/10.1089/fpd.2014.1800

    • Google Scholar
26. 1. Capaldi RA
    2. Schulenberg B
    3. Murray J
    4. Aggeler R

    (2000)

    Cross-linking and electron microscopy studies of the structure and functioning of the Escherichia coli ATP synthase

    Journal of Experimental Biology 203:29–33.

    • Google Scholar
27. 1. Chang DE
    2. Smalley DJ
    3. Tucker DL
    4. Leatham MP
    5. Norris WE
    6. Stevenson SJ
    7. Anderson AB
    8. Grissom JE
    9. Laux DC
    10. Cohen PS
    11. Conway T

    (2004) Carbon nutrition of Escherichia coli in the mouse intestine

    Proceedings of the National Academy of Sciences of USA 101:7427–7432.

    https://doi.org/10.1073/pnas.0307888101

    • Google Scholar
28. 1. Chao L
    2. Levin BR

    (1977) Complex community in a simple habitat: experimental study with bacteria and phage

    Ecology 58:369–378.

    https://doi.org/10.2307/1935611

    • Google Scholar
29. 1. Chen X
    2. Zhou L
    3. Tian K
    4. Kumar A
    5. Singh S
    6. Prior BA
    7. Wang Z

    (2013) Metabolic engineering of Escherichia coli: a sustainable industrial platform for bio-based chemical production

    Biotechnology Advances 31:1200–1223.

    https://doi.org/10.1016/j.biotechadv.2013.02.009

    • Google Scholar
30. 1. Claesson MJ
    2. O'Sullivan O
    3. Wang Q
    4. Nikkilä J
    5. Marchesi JR
    6. Smidt H
    7. de Vos WM
    8. Ross RP
    9. O'Toole PW

    (2009) Comparative analysis of pyrosequencing and a phylogenetic microarray for exploring microbial community structures in the human distal intestine

    PLOS ONE 4:e6669.

    https://doi.org/10.1371/journal.pone.0006669

    • Google Scholar
31. 1. Cohen S
    2. Chang A
    3. Boyer H
    4. Helling R

    (1973) Construction of biologically functional bacterial plasmids in vitro

    Proceedings of the National Academy of Sciences of USA 70:3240–3244.

    https://doi.org/10.1073/pnas.70.11.3240

    • Google Scholar
32. 1. Cooper TF

    (2007) Recombination speeds adaptation by reducing competition between beneficial mutations in populations of Escherichia coli

    PLOS Biology 5:1899–1905.

    https://doi.org/10.1371/journal.pbio.0050225

    • Google Scholar
33. 1. Cooper TF
    2. Rozen DE
    3. Lenski RE

    (2003) Parallel changes in gene expression after 20,000 generations of evolution in Escherichia coli

    Proceedings of the National Academy of Sciences of USA 100:1072–1077.

    https://doi.org/10.1073/pnas.0334340100

    • Google Scholar
34. 1. Crick FH
    2. Barnett L
    3. Brenner S
    4. Watts-Tobin RJ

    (1961) General nature of the genetic code for proteins

    Nature 192:1227–1232.

    https://doi.org/10.1038/1921227a0

    • Google Scholar
35. 1. Daegelen P
    2. Studier FW
    3. Lenski RE
    4. Cure S
    5. Kim JF

    (2009) Tracing ancestors and relatives of Escherichia coli B, and the derivation of B strains REL606 and BL21(DE3)

    Journal of Molecular Biology 394:634–643.

    https://doi.org/10.1016/j.jmb.2009.09.022

    • Google Scholar
36. 1. de Muinck EJ
    2. Lagesen K
    3. Afset JE
    4. Didelot X
    5. Rønningen KS
    6. Rudi K
    7. Stenseth NC
    8. Trosvik P

    (2013) Comparisons of infant Escherichia coli isolates link genomic profiles with adaptation to the ecological niche

    BMC Genomics 14:81.

    https://doi.org/10.1186/1471-2164-14-81

    • Google Scholar
37. 1. Dolbrindt U
    2. Chowdary MG
    3. Krumbholz G
    4. Hacker J

    (2010) Genome dynamics and its impact on evolution of Escherichia coli

    Medical Microbiology and Immunology 199:145–154.

    https://doi.org/10.1007/s00430-010-0161-2

    • Google Scholar
38. 1. Dublan MD
    2. Ortiz-Marquez JCF
    3. Lett L
    4. Curatti L

    (2014) Plant-adapted Escherichia coli show increased lettuce colonizing ability, resistance to oxidative stress and chemotactic response

    PLOS ONE 9:e110416.

    https://doi.org/10.1371/journal.pone.0110416

    • Google Scholar
39. 1. Eckburg PB
    2. Bik EM
    3. Bernstein CN
    4. Purdom E
    5. Dethlefsen L
    6. Sargen M
    7. Bill SR
    8. Nelson KE
    9. Relman DA

    (2005) Diversity of the human intestinal microbial flora

    Science 308:1635–1638.

    https://doi.org/10.1126/science.1110591

    • Google Scholar
40. 1. Ellis EL
    2. Delbrück M

    (1939) The growth of bacteriophage

    Journal of General Physiology 22:365–384.

    https://doi.org/10.1085/jgp.22.3.365

    • Google Scholar
41. 1. Englesberg E
    2. Irr J
    3. Power J
    4. Lee N

    (1965)

    Positive control of enzyme synthesis by gene C in the L-arabinose system

    Journal of Bacteriology 90:946–957.

    • Google Scholar
42. 1. Escherich T

    (1988)

    The intestinal bacteria of the neonate and breast-fed infant (1885)

    Review of Infectious Disease 10:1220–1225.

    • Google Scholar
43. 1. Feeney AR
    2. Cooke EM
    3. Shinebaum R

    (1980) A comparative study of gram-negative aerobic bacilli in the faeces of babies born in hospital and at home

    Journal of Hygiene 77:129–139.

    https://doi.org/10.1017/S0022172400026565

    • Google Scholar
44. 1. Ferens WA
    2. Hovde CJ

    (2011) Escherichia coli O157:H7: Animal reservoir and sources of human infection

    Foodborne Pathogens and Disease 8:465–487.

    https://doi.org/10.1089/fpd.2010.0673

    • Google Scholar
45. 1. Frenzen PD
    2. Drake A
    3. Angulo FJ
    4. The Emerging infections Program Foodnet working group

    (2005)

    Economic cost of illness due to Escherichia coli O157 infections in the United States

    Journal of Food Protection 68:2623–2630.

    • Google Scholar
46. 1. Griffin PM
    2. Ostroff SM
    3. Tauxe RV
    4. Greene KD
    5. Wells JG
    6. Lewis JH
    7. Blake PA

    (1988) Illnesses associated with Escherichia coli O157:H7 infections. a broad clinical spectrum

    Annals of Internal Medicine 109:705–712.

    https://doi.org/10.7326/0003-4819-109-9-705

    • Google Scholar
47. 1. Griffin PM
    2. Tauxe RV

    (1991)

    The epidemiology of infections caused by Escherichia coli O157:H7, other enterohemorrhagic E. coli, and the associated hemolytic uremic syndrome

    Epidemiologic Review 13:60–98.

    • Google Scholar
48. 1. Grönlund MM
    2. Lehtonen OP
    3. Eerola E
    4. Kero P

    (1999) Fecal microflora in healthy infants born by different methods of delivery: permanent changes in intestinal flora after cesarean delivery

    Journal of Pediatric Gastroenterology and Nutrition 28:19–25.

    https://doi.org/10.1097/00005176-199901000-00007

    • Google Scholar
49. 1. Guttman DS
    2. Dykhuizen DE

    (1994) Clonal divergence in Escherichia coli as a result of recombination, not mutation

    Science 266:1380–1383.

    https://doi.org/10.1126/science.7973728

    • Google Scholar
50. 1. Hansen S
    2. Lewis K
    3. Vulić M

    (2008) Role of global regulators and nucleotide metabolism in antibiotic tolerance in Escherichia coli

    Antimicrobial Agents and Chemotherapy 52:2718–2726.

    https://doi.org/10.1128/AAC.00144-08

    • Google Scholar
51. 1. Harshey RM

    (2003) Bacterial motility on a surface: many ways to a common goal

    Annual Reviews of Microbiology 57:249–273.

    https://doi.org/10.1146/annurev.micro.57.030502.091014

    • Google Scholar
52. 1. Harshey RM
    2. Matsuyama T

    (1994) Dimorphic transition in Escherichia coli and Salmonella typhimurium: surface-induced differentiation into hyperflagellate swarmer cells

    Proceedings of the National Academy of Sciences of USA 91:8631–8635.

    https://doi.org/10.1073/pnas.91.18.8631

    • Google Scholar
53. 1. Hartl DL
    2. Dykhuizen DE

    (1984) The population genetics of Escherichia coli

    Annual Review of Genetics 18:31–68.

    https://doi.org/10.1146/annurev.ge.18.120184.000335

    • Google Scholar
54. 1. He X
    2. Mishchuk DO
    3. Shah J
    4. Weimer BC
    5. Slupsky CM

    (2013) Cross-talk between E. coli strains and a human colorectal adenocarcinoma-derived cell line

    Scientific Reports 3:3416.

    https://doi.org/10.1038/srep03416

    • Google Scholar
55. 1. Herring CD
    2. Glasner JD
    3. Blattner FR

    (2003) Gene replacement without selection: regulated suppression of amber mutations in Escherichia coli

    Gene 5:153–163.

    https://doi.org/10.1016/S0378-1119(03)00585-7

    • Google Scholar
56. 1. Hildebrand A
    2. Schlacta T
    3. Warmack R
    4. Kasuga T
    5. Fan Z

    (2013) Engineering Escherichia coli for improved ethanol production from gluconate

    Journal of Biotechnology 168:101–106.

    https://doi.org/10.1016/j.jbiotec.2013.07.033

    • Google Scholar
57. 1. Hobby GL
    2. Meyer K
    3. Chaffee E

    (1942) Observations on the mechanism of action of penicillin

    Experimental Biology and Medicine 50:281–285.

    https://doi.org/10.3181/00379727-50-13773

    • Google Scholar
58. 1. Hu Y
    2. Coates AR

    (2005) Transposon mutagenesis identifies genes which control antimicrobial drug tolerance in stationary-phase Escherichia coli

    FEMS Microbiology Letters 243:117–124.

    https://doi.org/10.1016/j.femsle.2004.11.049

    • Google Scholar
59. 1. Huang C
    2. Lin H
    3. Yang X

    (2012) Industrial production of recombinant therapeutics in Escherichia coli and its recent advancements

    Journal of Industrial Microbiology & Biotechnology 39:383–399.

    https://doi.org/10.1007/s10295-011-1082-9

    • Google Scholar
60. 1. Inoue T
    2. Shingaki R
    3. Hirose S
    4. Waki K
    5. Mori H
    6. Fukui K

    (2007) Genome-wide screening of genes required for swarming motility in Escherichia coli

    Journal of Bacteriology 189:950–957.

    https://doi.org/10.1128/jb.01294-06

    • Google Scholar
61. 1. Ishii S
    2. Sadowsky MJ

    (2008) Escherichia coli in the environment: implications for water quality and human health

    Microbes and Environments 23:101–108.

    https://doi.org/10.1264/jsme2.23.101

    • Google Scholar
62. 1. Jacob F
    2. Monod J

    (1961) Genetic regulatory mechanisms in the synthesis of proteins

    Journal of Molecular Biology 3:318–356.

    https://doi.org/10.1016/S0022-2836(61)80072-7

    • Google Scholar
63. 1. Jacob F
    2. Perrin D
    3. Sanchez C
    4. Monod J

    (1960) L’opéron: groupe de génes à expression coordonnée par un opérateur (The operon: a group of genes whose expression is coordinated by an operator)

    Comptes Rendus Hebdomadaires Des Séances De l'Académie Des Sciences 250:1727–1729.

    https://doi.org/10.1016/j.crvi.2005.04.005

    • Google Scholar
64. 1. Janßen HJ
    2. Steinbüchel A

    (2014) Fatty acid synthesis in Escherichia coli and its applications towards the production of fatty acid based fiofuels

    Biotechnology for Biofuels 7:7.

    https://doi.org/10.1186/1754-6834-7-7

    • Google Scholar
65. Book

    1. Judson HF

    (1996)

    The Eighth Day of Creation

    Cold Spring Harbor: Cold Spring Harbor Press.

    • Google Scholar
66. 1. Kaas RS
    2. Friis C
    3. Ussery DW
    4. Aarestrup FM

    (2012) Estimating variation within the genes and inferring the phylogeny of 186 sequenced diverse Escherichia coli genomes

    BMC Genomics 13:577.

    https://doi.org/10.1186/1471-2164-13-577

    • Google Scholar
67. 1. Kamionka M

    (2011) Engineering of therapeutic proteins production in Escherichia coli

    Current Pharmaceutical Biotechnology 12:268–274.

    https://doi.org/10.2174/138920111794295693

    • Google Scholar
68. 1. Kaper JB
    2. Nataro JP
    3. Mobley HLT

    (2004) Pathogenic Escherichia coli

    Nature Reviews Microbiology 2:123–140.

    https://doi.org/10.1038/nrmicro818

    • Google Scholar
69. 1. Kasarjian JKA
    2. Iida M
    3. Ryu J

    (2003) New restriction enzymes discovered from Escherichia coli clinical strains using a plasmid transformation method

    Nucleic Acids Research 31:e22.

    https://doi.org/10.1093/nar/gng022

    • Google Scholar
70. 1. Kaup B
    2. Bringer-Meyer S
    3. Sahm H

    (2004) Metabolic engineering of Escherichia coli: construction of an efficient biocatalyst for D-mannitol formation in a whole-cell biotransformation

    Applied Microbiology and Biotechnology 64:333–339.

    https://doi.org/10.1007/s00253-003-1470-9

    • Google Scholar
71. 1. Kawecki TJ
    2. Lenski RE
    3. Ebert D
    4. Hollis B
    5. Olivieri I
    6. Whitlock MC

    (2013) Experimental evolution

    Trends in Ecology & Evolution 27:547–560.

    https://doi.org/10.1016/j.tree.2012.06.001

    • Google Scholar
72. 1. Kim B
    2. Park H
    3. Na D
    4. Lee SY

    (2014) Metabolic engineering of Escherichia coli for the production of phenol from glucose

    Biotechnology Journal 9:621–629.

    https://doi.org/10.1002/biot.201300263

    • Google Scholar
73. 1. Koren O
    2. Goodrich JK
    3. Cullender TC
    4. Spor A
    5. Laitinen K
    6. Cling BH
    7. Gonzalez A
    8. Werner JJ
    9. Angenent LT
    10. Knight R
    11. Bäckhed F
    12. Isolauri E
    13. Salminen S
    14. Ley RE

    (2012) Host remodeling of the gut microbiome and metabolic changes during pregnancy

    Cell 150:470–480.

    https://doi.org/10.1016/j.cell.2012.07.008

    • Google Scholar
74. 1. Lawrence JG
    2. Roth JR

    (1996)

    Evolution of coenzyme B12 synthesis among enteric bacteria: evidence for loss and acquisition of a multigene complex

    Genetics 143:11–24.

    • Google Scholar
75. 1. Lehman IR
    2. Bessman MJ
    3. Simms ES
    4. Kornberg A

    (1958)

    Enzymatic synthesis of deoxyribonucleic acid. I. Preparation of substrates and partial purification of an enzyme from Escherichia coli

    Journal of Biological Chemistry 233:163–170.

    • Google Scholar
76. 1. Leimbach A
    2. Hacker J
    3. Dobrindt U

    (2013) E. coli as an all-rounder: the thin line between commensalism and pathogenicity

    Current Topics in Microbiology and Immunology 358:3–32.

    https://doi.org/10.1007/82_2012_303

    • Google Scholar
77. 1. Lewis K

    (2010) Persister cells

    Annual Reviews of Microbiology 64:357–372.

    https://doi.org/10.1146/annurev.micro.112408.134306

    • Google Scholar
78. 1. Lindberg E
    2. Adlerberth I
    3. Hesselmar B
    4. Saalman R
    5. Strannegard IL
    6. Aberg N
    7. Wold AE

    (2004) High rate of transfer of Staphylococcus aureus from parental skin to infant gut flora

    Journal of Clinical Microbiology 42:530–534.

    https://doi.org/10.1128/JCM.42.2.530-534.2004

    • Google Scholar
79. 1. Lindberg E
    2. Nowrouzian F
    3. Adlerberth I
    4. Wold AE

    (2000) Long-time persistence of superantigen-producing Staphylococcus aureus strains in the intestinal microflora of healthy infants

    Pediatric Research 48:741–747.

    https://doi.org/10.1203/00006450-200012000-00007

    • Google Scholar
80. 1. Link AJ
    2. Phillips D
    3. Church GM

    (1997)

    Methods for generating precise deletions and insertions in the genome of wild-type Escherichia coli: applications to open reading frame characterization

    Journal of Bacteriology 179:6228–9237.

    • Google Scholar
81. 1. Linn S
    2. Arber W

    (1968) Host specificity of DNA produced by Escherichia coli. X. In vitro restriction of phage fd replicative form

    Proceedings of the National Academy of Sciences of USA 59:1300–1306.

    https://doi.org/10.1073/pnas.59.4.1300

    • Google Scholar
82. 1. Liu T
    2. Khosla C

    (2010) Genetic engineering of Escherichia coli for biofuel production

    Annual Review of Genetics 44:53–69.

    https://doi.org/10.1146/annurev-genet-102209-163440

    • Google Scholar
83. 1. Lopez-Torres AJ
    2. Hazen TC
    3. Toranzos GA

    (1987) Distribution and in situ survival and activity of Klebsiella pneumonia and Escherichia coli in a tropical rain forest watershed

    Current Microbiology 15:213–218.

    https://doi.org/10.1007/BF01577533

    • Google Scholar
84. 1. Lukjancenko O
    2. Wassenaar TM
    3. Ussery DW

    (2010) Comparison of 61 sequenced Escherichia coli genomes

    Microbial Ecology 60:708–720.

    https://doi.org/10.1007/s00248-010-9717-3

    • Google Scholar
85. 1. Lederberg J
    2. Lederberg E

    (1952)

    Replica plating and indirect selection of bacterial mutants

    Journal of Bacteriology 63:399–406.

    • Google Scholar
86. 1. Lenski RE

    (1988) Experimental studies of pleiotropy and epistasis in Escherichia coli. I. variation in competitive fitness among mutants resistant to virus T4

    Evolution 42:425–432.

    https://doi.org/10.2307/2409028

    • Google Scholar
87. 1. Lenski RE

    (2004) Phenotypic and genomic evolution during a 20,000 generation experiment with the bacterium Escherichia coli

    Plant Breeding Reviews 24:225–265.

    https://doi.org/10.1002/9780470650288.ch8

    • Google Scholar
88. 1. Luria SE
    2. Delbrück M

    (1943)

    Mutations of bacteria from virus sensitivity to virus resistance

    Genetics 28:491–511.

    • Google Scholar
89. 1. Lwoff A

    (1953)

    Lysogeny

    Bacteriology Reviews 17:269–337.

    • Google Scholar
90. 1. Mead PS
    2. Slutsker L
    3. Dietz V
    4. McCraig LF
    5. Bresee JS
    6. Shapiro C
    7. Griffin PM
    8. Tauxe RV

    (1999) Food-related illness and death in the United States

    Emerging Infectious Diseases 5:607–625.

    https://doi.org/10.3201/eid0505.990502

    • Google Scholar
91. 1. Meselson M
    2. Yuan R

    (1968) DNA restriction enzyme from E. coli

    Nature 217:1110–1114.

    https://doi.org/10.1038/2171110a0

    • Google Scholar
92. 1. Meyer JR
    2. Agrawal AA
    3. Quick RT
    4. Dobias DT
    5. Schneider D
    6. Lenski RE

    (2010) Parallel changes in host resistance to viral infection during 45,000 generations of relaxed selection

    Evolution 60:3024–3034.

    https://doi.org/10.1111/j.1558-5646.2010.01049.x

    • Google Scholar
93. 1. Meyer JR
    2. Dobias DT
    3. Weitz JS
    4. Barrick JE
    5. Quick RT
    6. Lenski RE

    (2012) Repeatability and contingency in the evolution of a key innovation in phage lambda

    Science 335:428–432.

    https://doi.org/10.1126/science.1214449

    • Google Scholar
94. 1. Minot S
    2. Sinha R
    3. Chen J
    4. Li H
    5. Keilbaugh SA
    6. Wu GD
    7. Lewis JD
    8. Bushman FD

    (2011) The human gut virome: inter-individual variation and dynamic response to diet

    Genome Research 21:1616–1625.

    https://doi.org/10.1101/gr.122705.111

    • Google Scholar
95. 1. Mira A
    2. Martin-Cuadrado AB
    3. D'Auria G
    4. Rodríguez-Valera F

    (2010) The bacterial pan-genome: a new paradigm in microbiology

    International Microbiology 12:45–57.

    https://doi.org/10.2436/20.1501.01.110

    • Google Scholar
96. 1. Moeller AH
    2. Li Y
    3. Ngole EM
    4. Ahuka-Mundeke S
    5. Lonsdorf EV
    6. Pusey AE
    7. Peeters M
    8. Hahn BH
    9. Ochman H

    (2014) Rapid changes in the gut microbiome during human evolution

    Proceedings of the National Academy of Sciences of USA 111:16431–16435.

    https://doi.org/10.1073/pnas.1419136111

    • Google Scholar
97. 1. Nascimento HH
    2. Silva LE
    3. Souza RT
    4. Silva NP
    5. Scaletsky IC

    (2014) Phenotypic and genotypic characteristics associated with biofilm formation in clinical isolates of atypical enteropathogenic Escherichia coli (aEPEC) strains

    BMC Microbiology 14:184.

    https://doi.org/10.1186/1471-2180-14-184

    • Google Scholar
98. 1. Nesse LL
    2. Sekse C
    3. Berg K
    4. Johannesen KC
    5. Solheim H
    6. Vestby LK
    7. Urdahl AM

    (2014) Potentially pathogenic Escherichia coli can form a biofilm under conditions relevant to the food production chain

    Applied and Environmental Microbiology 80:2042–2049.

    https://doi.org/10.1128/AEM.03331-13

    • Google Scholar
99. 1. Nowrouzian F
    2. Hesselmar B
    3. Saalman R
    4. Strannegard I
    5. Aberg N
    6. Wold AE
    7. Adlerberth I

    (2003) Escherichia coli in infants' intestinal microflora: colonization rate, strain turnover, and virulence gene carriage

    Pediatric Research 54:8–14.

    https://doi.org/10.1203/01.PDR.0000069843.20655.EE

    • Google Scholar
100. 1. Neu J
     2. Rushing J

     (2011) Cesarean versus vaginal delivery: long-term infant outcomes and the hygiene hypothesis

     Clinics in Perinatology 38:321–331.

     https://doi.org/10.1016/j.clp.2011.03.008

     • Google Scholar
101. 1. Nirenberg M
     2. Leder P
     3. Bernfield M
     4. Brimacombe R
     5. Trupin J
     6. Rottman F
     7. O'Neal C

     (1965) RNA codewords and protein synthesis, VII. On the general nature of the RNA code

     Biochemistry 53:1161–1168.

     https://doi.org/10.1073/pnas.53.5.1161

     • Google Scholar
102. 1. Partridge JD
     2. Harshey RM

     (2013a) More than motility: Salmonella flagella contribute to overriding friction and facilitating colony hydration during swarming

     Journal of Bacteriology 195:919–929.

     https://doi.org/10.1128/jb.02064-12

     • Google Scholar
103. 1. Partridge JD
     2. Harshey RM

     (2013b) Swarming: flexible roaming plans

     Journal of Bacteriology 195:909–918.

     https://doi.org/10.1128/jb.02063-12

     • Google Scholar
104. 1. Paul S
     2. Linardopoulou EV
     3. Billig M
     4. Tchesnokova V
     5. Price LB
     6. Johnson JR
     7. Chattopadhyay S
     8. Sokurenko EV

     (2013) Role of homologous recombination of extraintestinal Escherichia coli

     Journal of Bacteriology 195:231–242.

     https://doi.org/10.1128/JB.01524-12

     • Google Scholar
105. 1. Ponciano JM
     2. La HJ
     3. Joyce P
     4. Forney LJ

     (2009) Evolution of diversity in spatially structured Escherichia coli populations

     Applied and Environmental Microbiology 75:6047–6054.

     https://doi.org/10.1128/AEM.00063-09

     • Google Scholar
106. 1. Pupo GM
     2. Lan R
     3. Reeves PR

     (2000) Multiple independent origins of Shigella clones of Escherichia coli and convergent evolution of many of their characteristics

     Proceedings of the National Academy of Sciences of USA 97:10567–10572.

     https://doi.org/10.1073/pnas.180094797

     • Google Scholar
107. 1. Rangel JM
     2. Sparling PH
     3. Crowe C
     4. Griffin PM
     5. Swerdlow DL

     (2005) Epidemiology of Escherichia coli O157:H7, 1982–2002

     Emerging Infectious Diseases 11:603–609.

     https://doi.org/10.3201/eid1104.040739

     • Google Scholar
108. 1. Roberts RJ

     (2005) How restriction enzymes became the workhorses of molecular biology

     Proceedings of the National Academy of Sciences of USA 102:5902–5908.

     https://doi.org/10.1073/pnas.0500923102

     • Google Scholar
109. 1. Robinson CM
     2. Sinclair JF
     3. Smith MJ
     4. O'Brien AD

     (2006) Shiga toxin of enterohemorrhagic Escherichia coli type O157:H7 promotes intestinal colonization

     Proceedings of the National Academy of Sciences of USA 103:9667–9672.

     https://doi.org/10.1073/pnas.0602359103

     • Google Scholar
110. 1. Rudi K
     2. Storrø O
     3. Øien T
     4. Johnsen R

     (2012) Modelling bacterial transmission in human allergen-specific IgE sensitization

     Letters in Applied Microbiology 54:447–454.

     https://doi.org/10.1111/j.1472-765X.2012.03229.x

     • Google Scholar
111. 1. Russo TA
     2. Johnson JR

     (2003) Medical and economic impact of extraintestinal infections due to Escherichia coli: focus on an increasingly endemic problem

     Microbes and Infection 5:449–456.

     https://doi.org/10.1016/S1286-4579(03)00049-2

     • Google Scholar
112. 1. Sannasiddappa TH
     2. Costabile A
     3. Gibson GR
     4. Clarke SR

     (2011) The influence of Staphylococcus aureus on gut microbial ecology in an in vitro continuous culture human colonic model system

     PLOS ONE 6:e23227.

     https://doi.org/10.1371/journal.pone.0023227

     • Google Scholar
113. 1. Savageau MA

     (1983) Escherichia coli habitats, cell types, and molecular mechanisms of gene control

     The American Naturalist 122:732–744.

     https://doi.org/10.1086/284168

     • Google Scholar
114. 1. Scallan E
     2. Hoekstra RM
     3. Angulo FJ
     4. Tauxe RV
     5. Widdowson M
     6. Roy SL
     7. Jones JL
     8. Griffin PM

     (2011) Foodborne illness acquired in the United States – major pathogens

     Emerging Infectious Diseases 17:7–15.

     https://doi.org/10.3201/eid1701.091101p1

     • Google Scholar
115. Book

     1. Schaechter M
     2. Neidhardt FC

     (1987)

     Indroduction

     In: Neidhardt FC, editors. Escherichia coli and Salmonella typhimurium. Washington: American Society for Microbiology Press. pp. 1–2.

     • Google Scholar
116. 1. Schluter J
     2. Foster KR

     (2012) The evolution of mutualism in gut microbiota via host epithelial selection

     PLOS Biology 10:e1001424.

     https://doi.org/10.1371/journal.pbio.1001424

     • Google Scholar
117. 1. Schmidt H
     2. Hensel M

     (2004) Pathogenicity islands in bacterial pathogens

     Clinical Microbiology Reviews 17:14–56.

     https://doi.org/10.1128/CMR.17.1.14-56.2004

     • Google Scholar
118. 1. Sears HI
     2. Brownlee I
     3. Uchiyama JK

     (1950)

     Persistence of individual strains of E. coli in the intestinal tract of man

     Journal of Bacteriology 59:293–301.

     • Google Scholar
119. 1. Shah D
     2. Zhang Z
     3. Khodursky AB
     4. Kaldalu N
     5. Kurg K
     6. Lewis K

     (2006) Persisters: a distinct physiological state of E. coli

     BMC Microbiology 6:53.

     https://doi.org/10.1186/1471-2180-6-53

     • Google Scholar
120. 1. Shoaie S
     2. Kalrsson F
     3. Mardinoglu A
     4. Nookaew I
     5. Bordel S
     6. Nielsen J

     (2013) Understanding the interactions between bacteria and the human gut through metabolic modeling

     Scientific Reports 3:2532.

     https://doi.org/10.1038/srep02532

     • Google Scholar
121. 1. Shulman ST
     2. Friedmann HC
     3. Sims RH

     (2007) Theodor Escherich: the first pediatric infectious diseases physician?

     Clinical Infectious Diseases 45:1025–1029.

     https://doi.org/10.1086/521946

     • Google Scholar
122. 1. Smith KE
     2. Wilker PR
     3. Reiter PL
     4. Hedican EB
     5. Bender JB
     6. Hedberg CW

     (2012) Antibiotic treatment of Escherichia coli O157 infection and the risk of hemolytic uremic syndrome, Minnesota

     Pediatric Infectious Disease Journal 31:37–41.

     https://doi.org/10.1097/INF.0b013e31823096a8

     • Google Scholar
123. 1. Stevens A

     (1960) Incorporation of the adenine ribonucleotide into RNA by cell fractions from E. coli

     Biochemical and Biophysical Research Communications 3:92–96.

     https://doi.org/10.1016/0006-291X(60)90110-8

     • Google Scholar
124. 1. Tenaillon O
     2. Skurnik D
     3. Picard B
     4. Denamur E

     (2010) The population genetics of commensal Escherichia coli

     Natures Reviews Microbiology 8:207–217.

     https://doi.org/10.1038/nrmicro2298

     • Google Scholar
125. 1. Texier S
     2. Prigent-Combaret C
     3. Gourdon MH
     4. Poirier MA
     5. Faivre P
     6. Dorioz JM
     7. Poulenard J
     8. Jocteur-Monrozier L
     9. Moenne-Loccoz Y
     10. Trevisan D

     (2008) Persistence of culturable Escherichia coli fecal contaminants in dairy Alpine grassland soils

     Journal of Environmental Quality 37:2299–2310.

     https://doi.org/10.2134/jeq2008.0028

     • Google Scholar
126. 1. Tomas J
     2. Reygner J
     3. Mayeur C
     4. Ducroc R
     5. Bouet S
     6. Bridonneau C
     7. Cavin J
     8. Thomas M
     9. Langella P
     10. Cherbuy C

     (2015) Early colonizing Escherichia coli elicits remodeling of rat colonic epithelium shifty toward a new homeostatic state

     The ISME Journal 9:46–58.

     https://doi.org/10.1038/ismej.2014.111

     • Google Scholar
127. 1. Touchon M
     2. Hoede C
     3. Tenaillon O
     4. Barbe V
     5. Baeriswyl S
     6. Bidet P
     7. Bingen E
     8. Bonascorsi S
     9. Bouchier C
     10. Bouvet O
     11. Calteau A
     12. Chiapello H
     13. Clermont O
     14. Cruveiller S
     15. Danchin A
     16. Diard M
     17. Dossat C
     18. Karoui ME
     19. Frapy E
     20. Garry L
     21. Ghigo JM
     22. Gilles AM
     23. Johnson J
     24. Le Bouguénec C
     25. Lescat M
     26. Mangenot S
     27. Martinez-Jéhanne V
     28. Matic I
     29. Nassif X
     30. Oztas S
     31. Petit MA
     32. Pichon C
     33. Rouy Z
     34. Ruf CS
     35. Schneider D
     36. Tourret J
     37. Vacherie B
     38. Vallenet D
     39. Médigue C
     40. Rocha EP
     41. Denamur E

     (2009) Organised genome dynamics in the Escherichia coli species results in high diverse adaptive paths

     PLOS Genetics 5:e1000344.

     https://doi.org/10.1371/journal.pgen.1000344

     • Google Scholar
128. 1. Travisano M
     2. Mongold JA
     3. Bennet AF
     4. Lenski RE

     (1995) Experimental tests of the roles of adaptation, chance and history in evolution

     Science 267:87–90.

     https://doi.org/10.1126/science.7809610

     • Google Scholar
129. 1. Tyerman JG
     2. Ponciano JM
     3. Joyce P
     4. Forney LJ
     5. Harmon LJ

     (2013) The evolution of antibiotic susceptibility and resistance during the formation of Escherichia coli biofilms in the absence of antibiotics

     BMC Evolutionary Biology 13:22.

     https://doi.org/10.1186/1471-2148-13-22

     • Google Scholar
130. 1. van Elsas JD
     2. Semenov AV
     3. Costa R
     4. Trevors JT

     (2011) Survival of Escherichia coli in the environment: fundamental and public health aspects

     The ISME Journal 5:173–183.

     https://doi.org/10.1038/ismej.2010.80

     • Google Scholar
131. 1. Virgin HW

     (2014) The virome in mammalian physiology and disease

     Cell 157:142–150.

     https://doi.org/10.1016/j.cell.2014.02.032

     • Google Scholar
132. 1. Vogeleer P
     2. Tremblay YD
     3. Mafu AA
     4. Jacques M
     5. Harel J

     (2014) Life on the outside: role of biofilms in environmental persistence of Shiga-toxin producing Escherichia coli

     Frontiers in Microbiology 5:317.

     https://doi.org/10.3389/fmicb.2014.00317

     • Google Scholar
133. 1. Walk ST
     2. Alm EW
     3. Gordon DM
     4. Ram JL
     5. Toranzos GA
     6. Tiedje JM
     7. Whittam TS

     (2009) Cryptic lineages of the genus Escherichia

     Applied and Environmental Microbiology 75:6534–6544.

     https://doi.org/10.1128/AEM.01262-09

     • Google Scholar
134. 1. Wang X
     2. Rochon M
     3. Lamprokostopoulou H
     4. Lünsdorf H
     5. Nimitz M
     6. Römling U

     (2006) Impact of biofilm matrix components of commensal Escherichia coli with the gastrointestinal cell line HT-29

     Cellular and Molecular Life Sciences 63:2352–2363.

     https://doi.org/10.1007/s00018-006-6222-4t

     • Google Scholar
135. 1. Welch RA
     2. Burland V
     3. Plunkett G III
     4. Redford P
     5. Roesch P
     6. Rasko D
     7. Buckles EL
     8. Liou SR
     9. Boutin A
     10. Hackett J
     11. Stroud D
     12. Mayhew GF
     13. Rose DJ
     14. Zhou S
     15. Schwartz DC
     16. Perna NT
     17. Mobley HL
     18. Donnenberg MS
     19. Blattner FR

     (2002) Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli

     Proceedings of the National Academy of Sciences of USA 99:17020–17024.

     https://doi.org/10.1073/pnas.252529799

     • Google Scholar
136. 1. Werkman CH

     (1927)

     Vitamin effects in the physiology of microorganisms

     Journal of Bacteriology 14:335–347.

     • Google Scholar
137. 1. Winfield MD
     2. Groisman EA

     (2003) Role of nonhost environments in the lifestyles of Salmonella and Escherichia coli

     Applied and Environmental Microbiology 69:3687–3694.

     https://doi.org/10.1128/AEM.69.7.3687-3694.2003

     • Google Scholar
138. 1. Wiser MJ
     2. Ribeck N
     3. Lenski RE

     (2013) Long-term dynamics of adaptation in asexual populations

     Science 342:1364–1367.

     https://doi.org/10.1126/science.1243357

     • Google Scholar
139. 1. Wollman E

     (1925)

     Recherches sur la bacteriophagie (phenomene de twort-d’Herelle)

     Annales de l’Institut Pasteur 56:137–164.

     • Google Scholar
140. 1. Wollman E
     2. Wollman E

     (1937)

     The phases of bacteriophages

     Comptes Rendus Hebdomadaires Des Séances Et Mémoires De La Société De Biologie (Proceedings of the Academy of Sciences and Minutes of the Society of Biology) 124:931–934.

     • Google Scholar
141. 1. Zhang R
     2. Turner L
     3. Berg HC

     (2010) The upper surface of an Escherichia coli swarm is stationary

     Proceedings of the National Academy of Sciences of USA 107:288–290.

     https://doi.org/10.1073/pnas.0912804107

     • Google Scholar
142. 1. Zhang Y

     (2014) Persisters, persistent infections and the Yin-Yang model

     Emerging Microbes and Infections 3:e3.

     https://doi.org/10.1038/emi.2014.3

     • Google Scholar
143. Book

     1. Zimmer C

     (2008)

     Microcosm

     New York: Pantheon Books.

     • Google Scholar

Author details

1. Zachary D Blount

   Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, United States

   Contribution

   ZDB, Drafting or revising the article

   For correspondence

   blountza@msu.edu

   Competing interests

   The author declares that no competing interests exist.

• 34,322

  views

• 4,063

  downloads

• 268

  citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.