The Gluconeogenesis Pathway Is Involved in Maintenance of Enterohaemorrhagic Escherichia coli O157:H7 in Bovine Intestinal Content

Bertin, Yolande; Deval, Christiane; Foye, Anne de la; Masson, Luke; Gannon, Victor P. J.; Harel, Josée; Martin, Christine; Desvaux, Mickaël; Forano, Evelyne

doi:10.1371/journal.pone.0098367

Cited by 40 publications

(61 citation statements)

References 56 publications

(76 reference statements)

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…Therefore, it is important to determine whether pathogens require glycolytic nutrients, gluconeogenic nutrients, or both for success in invading and subsequently colonizing the host. Indeed, recent studies have suggested that some pathogens use glycolytic nutrients, some use gluconeogenic nutrients, and some use both to adapt to diverse host habitats (1)(2)(3)(4)(5)(6)(7).…”

mentioning

confidence: 99%

Escherichia coli EDL933 Requires Gluconeogenic Nutrients To Successfully Colonize the Intestines of Streptomycin-Treated Mice Precolonized with E. coli Nissle 1917

et al. 2015

View full text Add to dashboard Cite

bEscherichia coli MG1655, a K-12 strain, uses glycolytic nutrients exclusively to colonize the intestines of streptomycin-treated mice when it is the only E. coli strain present or when it is confronted with E. coli EDL933, an O157:H7 strain. In contrast, E. coli EDL933 uses glycolytic nutrients exclusively when it is the only E. coli strain in the intestine but switches in part to gluconeogenic nutrients when it colonizes mice precolonized with E. -12) reported that E. coli 86-24, an O157:H7 strain, activates the expression of virulence genes under gluconeogenic conditions, suggesting that colonization of the intestine with a probiotic E. coli strain that outcompetes O157:H7 strains for gluconeogenic nutrients could render them nonpathogenic. Here we report that E. coli Nissle 1917, a probiotic strain, uses both glycolytic and gluconeogenic nutrients to colonize the mouse intestine between 1 and 5 days postfeeding, appears to stop using gluconeogenic nutrients thereafter in a large, long-term colonization niche, but continues to use them in a smaller niche to compete with invading E. coli EDL933. Evidence is also presented suggesting that invading E. coli EDL933 uses both glycolytic and gluconeogenic nutrients and needs the ability to perform gluconeogenesis in order to colonize mice precolonized with E. coli Nissle 1917. The data presented here therefore rule out the possibility that E. coli Nissle 1917 can starve the O157:H7 E. coli strain EDL933 of gluconeogenic nutrients, even though E. coli Nissle 1917 uses such nutrients to compete with E. coli EDL933 in the mouse intestine. While much attention has been paid to the role of specific virulence factors in bacterial pathogenesis, until recently little attention has been paid to the roles of specific metabolic pathways in the ability of bacterial pathogens to initiate the pathogenic process. Yet clearly, if a bacterial pathogen is unable to initiate pathogenesis because nutrients essential for its growth are unavailable in the host, it will be unable to establish itself and cause disease. Therefore, it is important to determine whether pathogens require glycolytic nutrients, gluconeogenic nutrients, or both for success in invading and subsequently colonizing the host. Indeed, recent studies have suggested that some pathogens use glycolytic nutrients, some use gluconeogenic nutrients, and some use both to adapt to diverse host habitats (1-7).We are interested in the nutritional basis of Escherichia coli colonization of the intestine and particularly in whether precolonization by commensal E. coli strains can be used to prevent invading E. coli intestinal pathogens from colonizing. Commensal E. coli strains colonize the human intestine in the presence of a dense and diverse intestinal microbiota comprising at least 500 cultivable species and 10 13 to 10 14 total bacteria (8). Unfortunately, E. coli colonization cannot be studied experimentally in conventional animals due to colonization resistance, which occurs when all niches are filled by the microbiota (9)....

show abstract

mentioning

confidence: 99%

Escherichia coli EDL933 Requires Gluconeogenic Nutrients To Successfully Colonize the Intestines of Streptomycin-Treated Mice Precolonized with E. coli Nissle 1917

et al. 2015

View full text Add to dashboard Cite

show abstract

“…) while the genes encoding uptake or assimilation of this amino acid were not found differentially expressed in microarrays experiments when the bacteria reached the stationary growth phase (Bertin et al . ). Asparagine was poorly detected in BSIC‐LEM while the transcription of ansB that encodes asparaginase (deamination of asparagine to aspartate) was significantly induced in EHEC EDL933 during incubation in f‐BSIC (Table ).…”

Section: Resultsmentioning

confidence: 99%

“…Genes involved in the assimilation or transport of a limited number of amino acids are up-regulated in EHEC EDL933 during incubation in f-BSIC Whole transcriptomic profiling of the reference EHEC strain EDL933 incubated in bovine small intestinal content (BSIC) previously deposited in NCBI's GEO database (accession number GSE49468) (Bertin et al, 2014) revealed the induction of genes associated with amino acids transport and catabolism. In the current report, we performed an in depth analysis of the assimilation of free amino acids present in BSIC by EHEC EDL933.…”

Section: Resultsmentioning

confidence: 99%

“…It is well documented that gluconeogenesis (GNG) pathway is required by pathogenic Enterobacteriaceae during host infection and contributes to bacterial fitness in vivo (Miranda et al 2004;Alteri et al, 2009;Dougherty et al, 2006). Analysis of the transcriptome profiling of EHEC grown in BSIC pinpointed the central role of GNG pathway in survival and maintenance of EHEC in the GIT of cattle (Bertin et al, 2014). Amino acids, identified as gluconeogenic substrates for EHEC in BSIC (Bertin et al, 2014), are potentially present in the bovine gut since in addition to amino acid provided from the animal diet, aspartate and serine are abundant components of the bovine intestinal mucus layer and can be released into luminal content during cells renewal (Montagne et al, 2000;Bertin et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Aspartate metabolism is involved in the maintenance of enterohaemorrhagic Escherichia coli O157:H7 in bovine intestinal content

Bertin

Segura

Jubelin

et al. 2018

Environmental Microbiology

Self Cite

View full text Add to dashboard Cite

The gastrointestinal tract (GIT) of healthy cattle is the main reservoir of enterohaemorrhagic Escherichia coli (EHEC). Therefore, it is crucial to better understand the physiology of EHEC in the bovine GIT. In this study, we demonstrate that aspartate present in bovine small intestine content (BSIC), was exhausted after incubation of the reference EHEC strain EDL933 but was poorly assimilated by the endogenous microbiota. Furthermore, the bovine commensal E. coli strain BG1 appeared less efficient than EDL933 in aspartate assimilation suggesting a competitive ability of EHEC to assimilate this amino acid. Our results strongly suggest that aspartate, internalized via the DcuA aspartate: succinate antiporting system, is then converted to fumarate and carbamoyl-aspartate, the precursor for UMP biosynthesis. Aspartate assimilation by these two pathways conferred a competitive growth advantage to EHEC in BSIC. In summary, supply of intracellular fumarate due to aspartate deamination and used as an electron acceptor for anaerobic fumarate respiration, as well as de novo synthesis of pyrimidine from aspartate appear to be important pathways favouring EHEC persistence in the bovine gut. Aspartate probably represents an ecological niche for EHEC in the bovine small intestine.

show abstract

“…On the other hand, among the less abundant proteins, we only detected the homologous recombination pathway, which is extremely important for the accurate repair of DNA double-strand breaks (Figure 2C). Different studies have reported that glycolysis / gluconeogenesis pathway might influence in the colonization process of EHEC in the gastrointestinal tract of both mouse and bovine (20, 21). Although glycolysis substrates inhibit the expression of genes that are localized in locus of enterocyte effacement (LEE), this pathway plays an important role in the initial colonization and maintenance of EHEC in the mouse intestine.…”

Section: Resultsmentioning

confidence: 99%

Quantification of EnterohemorrhagicEscherichia coliO157:H7 proteome using TMT-Based Analysis

Bei

Amigo

et al. 2018

Preprint

View full text Add to dashboard Cite

25Enterohemorrhagic Escherichia coli (EHEC) O157:H7 is a human pathogen responsible for 26 diarrhea, hemorrhagic colitis and hemolytic uremic syndrome (HUS). EHEC infection is 27 distributed worldwide and numerous outbreaks of diseases caused by enterohemorrhagic 28 have been reported. To promote a comprehensive insight into the molecular basis of EHEC 29 O157:H7 physiology and pathogenesis, the combined proteome of EHEC O157:H7 strains, 30 Clade 8 and Clade 6 isolated from cattle in Argentina, and the standard EDL933 (clade 3) 31 strain has been analyzed. TMT (Tandem Mass Tags)-based quantitative proteomic and 32 emPAI analyses were performed to estimate the protein abundance in EHEC proteome. 33 2,234 non-redundant proteins of EHEC O157:H7 were identified. A comparison of this 34 result with in silico data of EHEC O157:H7 genome showed that approximately 40% of the 35 predicted proteome of this pathogen were covered. According to the emPAI analysis, 85 36 proteins were among the most abundant (e.g. GAPDH, FliC H-antigen, Enolase, and 37 GroEL). Tellurite resistance proteins were also highly abundant. COG analysis showed that 38 although most of the identified proteins are related to cellular metabolism, the majority of 39 the most abundant proteins are associated with translation processes. A KEGG enrichment 40 analysis revealed that Glycolysis / Gluconeogenesis was the most significant pathway. On 41 the other hand, the less abundant detected proteins are those related to DNA processes, cell 42 respiration and prophage. Among the proteins that composed the Type III Secretion 43 System, the most abundant protein was EspA. Altogether, the results show a subset of 44 important proteins that contribute to physiology and pathogenicity of EHEC O157:H7. 45 IMPORTANCE 46 3 The study of the abundance of proteins present within a complex mixture of proteins in a 47 cell, under different conditions, can provide important information about the activities of 48 individual protein components and protein networks that are cornerstones for the 49 comprehension of physiological adaptations in response to biological demands promoted 50 by environmental changes. We generated a comprehensive and accurate quantitative list of 51 EHEC O157:H7 proteome, which provides a description of the most abundant proteins 52 produced by this pathogen that were related to physiology and pathogenesis of EHEC. This 53 study provides information and extends the understanding on functional genomics and the 54 biology of this pathogen.55 Keywords: EHEC, Tandem mass tags (TMT), protein quantitation, bacterial proteomic 56 57 58 Enterohemorrhagic Escherichia coli (EHEC) O157:H7 is a zoonotic pathogen belonging to 59 Shiga toxin-producing E. coli (STEC) and responsible for different diseases as diarrhea, 60 hemorrhagic colitis and hemolytic uremic syndrome (HUS). HUS is distributed worldwide 61 and considered to be a public health problem in several countries (1,2). Unfortunately, 62 Argentina is the country with the highest incidence of HUS i...

show abstract

The Gluconeogenesis Pathway Is Involved in Maintenance of Enterohaemorrhagic Escherichia coli O157:H7 in Bovine Intestinal Content

Cited by 40 publications

References 56 publications

Escherichia coli EDL933 Requires Gluconeogenic Nutrients To Successfully Colonize the Intestines of Streptomycin-Treated Mice Precolonized with E. coli Nissle 1917

Escherichia coli EDL933 Requires Gluconeogenic Nutrients To Successfully Colonize the Intestines of Streptomycin-Treated Mice Precolonized with E. coli Nissle 1917

Aspartate metabolism is involved in the maintenance of enterohaemorrhagic Escherichia coli O157:H7 in bovine intestinal content

Quantification of EnterohemorrhagicEscherichia coliO157:H7 proteome using TMT-Based Analysis

Contact Info

Product

Resources

About