Escherichia coli Pathotypes Occupy Distinct Niches in the Mouse Intestine

Meador, Jessica P.; Caldwell, Matthew E.; Cohen, Paul S.; Conway, Tyrrell

doi:10.1128/iai.01435-13

Cited by 38 publications

(37 citation statements)

References 33 publications

(55 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…coli within the gut comes from studies showing that different E. coli strains can simultaneously colonize the mouse intestinal tract if they can utilize distinct nutrients (42, 43). The extent to which two E.…”

Section: Discussionmentioning

confidence: 99%

The Rhomboid Protease GlpG Promotes the Persistence of Extraintestinal Pathogenic Escherichia coli within the Gut

et al. 2017

View full text Add to dashboard Cite

Extraintestinal pathogenic Escherichia coli (ExPEC) strains are typically benign within the mammalian gut but can disperse to extraintestinal sites to cause diseases like urinary tract infections and sepsis. As occupation of the intestinal tract is often a prerequisite for ExPEC-mediated pathogenesis, we set out to understand how ExPEC colonizes this niche. A screen using transposon sequencing (Tn-seq) was performed to search for genes within ExPEC isolate F11 that are important for growth in intestinal mucus, which is thought to be a major source of nutrients for E. coli in the gut. Multiple genes that contribute to ExPEC fitness in mucus broth were identified, with genes that are directly or indirectly associated with fatty acid beta-oxidation pathways being especially important. One of the identified mucus-specific fitness genes encodes the rhomboid protease GlpG. In vitro, we found that the disruption of glpG had polar effects on the downstream gene glpR, which encodes a transcriptional repressor of factors that catalyze glycerol degradation. Mutation of either glpG or glpR impaired ExPEC growth in mucus and on plates containing the long-chain fatty acid oleate as the sole carbon source. In contrast, in a mouse gut colonization model in which the natural microbiota is unperturbed, the disruption of glpG but not glpR significantly reduced ExPEC survival. This work reveals a novel biological role for a rhomboid protease and highlights new avenues for defining mechanisms by which ExPEC strains colonize the mammalian gastrointestinal tract.

show abstract

Section: Discussionmentioning

confidence: 99%

The Rhomboid Protease GlpG Promotes the Persistence of Extraintestinal Pathogenic Escherichia coli within the Gut

et al. 2017

View full text Add to dashboard Cite

show abstract

“…For instance, colonization by the enterohemorrhagic Escherichia coli strain EDL933 was blocked by a complementary mixture of commensal strains that effectively occupy the various intestinal niches that serve as colonization sites for EDL933 (41). Subsequent work revealed that other E. coli pathotypes target other intestinal sites for colonization (42), indicating that further investigation of the link between strain diversity and niche specificity is necessary to develop broad-spectrum probiotics. Interestingly, in some cases, strain diversity of pathogens within a mixed infection may augment the corresponding disease.…”

Section: Discussionmentioning

confidence: 99%

Intraspecific Competition Impacts Vibrio fischeri Strain Diversity during Initial Colonization of the Squid Light Organ

Sun

LaSota

Cecere

et al. 2016

Appl Environ Microbiol

View full text Add to dashboard Cite

Animal development and physiology depend on beneficial interactions with microbial symbionts. In many cases, the microbial symbionts are horizontally transmitted among hosts, thereby making the acquisition of these microbes from the environment an important event within the life history of each host. The light organ symbiosis established between the Hawaiian squid Euprymna scolopes and the bioluminescent bacterium Vibrio fischeri is a model system for examining how hosts acquire horizontally transmitted microbial symbionts. Recent studies have revealed that the light organ of wild-caught E. scolopes squid contains polyclonal populations of V. fischeri bacteria; however, the function and development of such strain diversity in the symbiosis are unknown. Here, we report our phenotypic and phylogenetic characterizations of FQ-A001, which is a V. fischeri strain isolated directly from the light organ of an E. scolopes individual. Relative to the type strain ES114, FQ-A001 exhibits similar growth in rich medium but displays increased bioluminescence and decreased motility in soft agar. FQ-A001 outcompetes ES114 in colonizing the crypt spaces of the light organs. Remarkably, we find that animals cocolonized with FQ-A001 and ES114 harbor singly colonized crypts, in contrast to the cocolonized crypts observed from competition experiments involving single genotypes. The results with our two-strain system suggest that strain diversity within the squid light organ is a consequence of diversity in the single-strain colonization of individual crypt spaces. IMPORTANCEThe developmental programs and overall physiologies of most animals depend on diverse microbial symbionts that are acquired from the environment. However, the basic principles underlying how microbes colonize their hosts remain poorly understood. Here, we report our findings of bacterial strain competition within the coevolved animal-microbe symbiosis composed of the Hawaiian squid and bioluminescent bacterium Vibrio fischeri. Using fluorescent proteins to differentially label two distinct V. fischeri strains, we find that the strains are unable to coexist in the same niche within the host. Our results suggest that strain competition for distinct colonization sites dictates the strain diversity associated with the host. Our study provides a platform for studying how strain diversity develops within a host. Microbes directly contribute to the physiology, development, and evolution of metazoans (1). Many metazoan-microbe symbioses are established through horizontal transmission, i.e., animals acquire microbial symbionts from their environment (2). Coevolution of host-microbe pairs can result in genetic factors that promote remarkably high specificity between the partners, thereby assisting in the acquisition of symbionts from typically unpredictable environments (3). An important but understudied topic in coevolved metazoan-microbe symbioses is how strain diversity impacts the establishment of these associations.A particularly powerful model system to explo...

show abstract

“…Indeed, when the ability of E. coli EDL933 to colonize mice that were pre-colonized with E. coli HS and E. coli Nissle 1917 was tested, which the data in Table 2 indicate should be equally effective without E. coli MG1655 present, E. coli EDL933, was indeed eliminated 5 days following association (35). However, the same 2 commensal E. coli strains could not prevent colonization of E. coli CFT073, a uropathogenic strain, and E. coli E2348/69, an enteropathogenic strain (95). Therefore, it is unlikely that any particular commensal strain(s) of E. coli will be generally effective as a probiotic to prevent colonization by enteric pathogens.…”

Section: Competition For Nutrients In the Intestinementioning

confidence: 99%

Commensal and Pathogenic Escherichia coli Metabolism in the Gut

2015

Self Cite

View full text Add to dashboard Cite

E. coli is a ubiquitous member of the intestinal microbiome. This organism resides in a biofilm comprised of a complex microbial community within the mucus layer where it must compete for the limiting nutrients that it needs to grow fast enough to stably colonize. In this article we discuss the nutritional basis of intestinal colonization. Beginning with basic ecological principles we describe what is known about the metabolism that makes E. coli such a remarkably successful member of the intestinal microbiota. To obtain the simple sugars and amino acids that it requires, E. coli depends on degradation of complex glycoproteins by strict anaerobes. Despite having essentially the same core genome and hence the same metabolism when grown in the laboratory, different E. coli strains display considerable catabolic diversity when colonized in mice. To explain why some E. coli mutants do not grow as well on mucus in vitro as their wild type parents yet are better colonizers, we postulate that each one resides in a distinct “Restaurant” where it is served different nutrients because it interacts physically and metabolically with different species of anaerobes. Since enteric pathogens that fail to compete successfully for nutrients cannot colonize, a basic understanding of the nutritional basis of intestinal colonization will inform efforts to develop prebiotics and probiotics to combat infection.

show abstract

Escherichia coli Pathotypes Occupy Distinct Niches in the Mouse Intestine

Cited by 38 publications

References 33 publications

The Rhomboid Protease GlpG Promotes the Persistence of Extraintestinal Pathogenic Escherichia coli within the Gut

The Rhomboid Protease GlpG Promotes the Persistence of Extraintestinal Pathogenic Escherichia coli within the Gut

Intraspecific Competition Impacts Vibrio fischeri Strain Diversity during Initial Colonization of the Squid Light Organ

Commensal and Pathogenic Escherichia coli Metabolism in the Gut

Contact Info

Product

Resources

About