Escherichia coli EDL933 requires gluconeogenic nutrients to successfully colonize the intestines of streptomycin-treated mice precolonized with E. coli Nissle 1917

Infection and Immunity

Volumn 83, Issue 5, 2015, Pages 1983-1991

  Schinner, Silvia A C ^a   Mokszycki, Matthew E ^a   Adediran, Jimmy ^a   Leatham Jensen, Mary ^a   Conway, Tyrrell ^b   Cohen, Paul S ^a  

^a UNIVERSITY OF RHODE ISLAND   (United States)

^b UNIVERSITY OF OKLAHOMA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

STREPTOMYCIN;

ANAEROBIC GLYCOLYSIS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL VIRULENCE; COMMENSAL ESCHERICHIA COLI; CONTROLLED STUDY; ENTEROPATHOGENIC ESCHERICHIA COLI; ESCHERICHIA COLI 86 24; ESCHERICHIA COLI EDL933; ESCHERICHIA COLI K 12; ESCHERICHIA COLI MG1655; ESCHERICHIA COLI NISSLE 1917; ESCHERICHIA COLI O157; GENE EXPRESSION; GLUCONEOGENESIS; INTESTINE; INTESTINE FLORA; MICROBIAL DIVERSITY; MOUSE; NONHUMAN; NUTRIENT CONTENT; NUTRIENT SUPPLY; PRIORITY JOURNAL; RAT; ANIMAL; ESCHERICHIA COLI; FOOD; GLYCOLYSIS; GROWTH, DEVELOPMENT AND AGING; MALE; METABOLISM; MICROBIOLOGY;

ANIMALS; ESCHERICHIA COLI; FOOD; GLUCONEOGENESIS; GLYCOLYSIS; INTESTINES; MALE; MICE;

EID: 84928201754     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.02943-14     Document Type: Article

References (42)

1. Tchawa-Yimga M, Leatham MP, Allen JH, Laux DC, Conway T, Cohen PS. 2006. Role of gluconeogenesis and the tricarboxylic acid cycle in the virulence of Salmonella enterica serovar Typhimurium in BALB/c mice. Infect Immun 74:1130-1140. http://dx.doi.org/10.1128/IAI.74.2.1130-1140.2006.
2. Alteri CJ, Mobley HLT. 2012. Escherichia coli physiology and metabolism dictates adaptation to diverse host microenvironments. Curr Opin Microbiol 15:3-9. http://dx.doi.org/10.1016/j.mib.2011.12.004.
3. Le Bouguénec C, Schouler C. 2011. Sugar metabolism, an additional virulence factor in enterobacteria. Int J Med Microbiol 301:1-6. http://dx.doi.org/10.1016/j.ijmm.2010.04.021.
4. Rohmer L, Hocquet D, Miller SI. 2011. Are pathogenic bacteria just looking for food? Metabolism and microbial pathogenesis. Trends Microbiol 19:341-348. http://dx.doi.org/10.1016/j.tim.2011.04.003.
5. Dunn MF, Ramírez-Trujillo JA, Hernandez-Lucas I. 2009. Major roles of isocitrate lyase and malate synthase in bacterial and fungal pathogenesis. Microbiology 155:3166-3175. http://dx.doi.org/10.1099/mic.0.030858-0.
6. Bertin Y, Deval C, de la Foye A, Masson L, Gannon V, Harel J, Martin C, Desvaux M, Forano E. 2014. The gluconeogenesis pathway is involved in maintenance of enterohaemorrhagic Escherichia coli O157:H7 in bovine intestinal content. PLoS One 9:e98367. http://dx.doi.org/10.1371/journal.pone.0098367.
7. Waligora EA, Fisher CR, Hanovice NJ, Rodou A, Wyckoff EE, Payne SM. 2014. Role of intracellular carbon metabolism pathways in Shigella flexneri virulence. Infect Immun 82:2746-2755. http://dx.doi.org/10.1128/IAI.01575-13.
8. Dethlefsen L, Huse S, Sogin ML, Relman DA. 2008. The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. PLoS Biol 6:e280. http://dx.doi.org/10.1371/journal.pbio.0060280.
9. Conlan JW, Bardy SL, KuoLee R, Webb A, Perry MB. 2001. Ability of Escherichia coli O157:H7 isolates to colonize the intestinal tract of conventional adult CD1 mice is transient. Can J Microbiol 47:91-95. http://dx.doi.org/10.1139/w00-124.
10. Conway T, Krogfelt KA, Cohen PS. 2004. The life of commensal Escherichia coli in the mammalian intestine. EcoSal Plus http://dx.doi.org/10.1128/ecosalplus.8.3.1.2.
11. Laux DC, Cohen PS, Conway T. 2005. Role of the mucus layer in bacterial colonization of the intestine, p 199-212. In Nataro JP, Cohen PS, Mobley HLT, Weiser JN (ed), Colonization of mucosal surfaces. ASM Press, Washington, DC.
12. Leatham-Jensen MP, Frimodt-Møller J, Adediran J, Mokszycki ME, Banner ME, Caughron JE, Krogfelt KA, Conway T, Cohen PS. 2012. The streptomycin-treated mouse intestine selects Escherichia coli envZ missense mutants that interact with dense and diverse intestinal microbiota. Infect Immun 80:1716-1727. http://dx.doi.org/10.1128/IAI.06193-11.
13. Adediran J, Leatham-Jensen MP, Mokszycki ME, Frimodt-Møller J, Krogfelt KA, Kazmierczak K, Kenney LJ, Conway T, Cohen PS. 2014. An Escherichia coli Nissle 1917 missense mutant colonizes the streptomycin-treated mouse intestine better than the wild type but is not a better probiotic. Infect Immun 82:670-682. http://dx.doi.org/10.1128/IAI.01149-13.
14. Maltby R, Leatham-Jensen MP, Gibson T, Cohen PS, Conway T. 2013. Nutritional basis for colonization resistance by human commensal Escherichia coli strains HS and Nissle 1917 against E. coli O157:H7 in the mouse intestine. PLoS One 8:e53957. http://dx.doi.org/10.1371/journal.pone.0053957.
15. Miranda RL, Conway T, Leatham MP, Chang DE, Norris WE, Allen JH, Stevenson SJ, Laux DC, Cohen PS. 2004. Glycolytic and gluconeogenic growth of Escherichia coli O157:H7 (EDL933) and E. coli K-12 (MG1655) in the mouse intestine. Infect Immun 72:1666-1676. http://dx.doi.org/10.1128/IAI.72.3.1666-1676.2004.
16. Njoroge JW, Nguyen Y, Curtis MM, Moreira CG, Sperandio V. 2012. Virulence meets metabolism: Cra and KdpE gene regulation in enterohemorrhagic Escherichia coli. mBio 3:e00280-12. http://dx.doi.org/10.1128/mBio.00280-12.
17. Njoroge JW, Gruber C, Sperandio V. 2013. The interacting Cra and KdpE regulators are involved in the expression of multiple virulence factors in enterohemorrhagic Escherichia coli. J Bacteriol 195:2499-2508. http://dx.doi.org/10.1128/JB.02252-12.
18. Schulze J, Sonnenborn U. 1995. Oral administration of a certain strain of live Escherichia coli for intestinal disorders? Infection 23:184-188. http://dx.doi.org/10.1007/BF01793863.
19. Patzer SI, Baquero MR, Bravo D, Moreno F, Hantke K. 2003. The colicin G, H and X determinants encode microcinsMand H47, which might utilize the catecholate siderophore receptors FepA, Cir, Fiu and IroN. Microbiology 149:2557-2570. http://dx.doi.org/10.1099/mic.0.26396-0.
20. Blum G, Marre R, Hacker J. 1995. Properties of Escherichia coli strains of serotype O6. Infection 23:234-236. http://dx.doi.org/10.1007/BF01781204.
21. Grozdanov L, Zähringer U, Blum-Oehler G, Brade L, Henne A, Knirel YA, Schombel U, Schulze J, Sonnenborn U, Gottschalk G, Hacker J, Rietschel ET, Dobrindt U. 2002. A single nucleotide exchange in the wzy gene is responsible for the semirough O6 lipopolysaccharide phenotype and serum sensitivity of Escherichia coli strain Nissle 1917. J Bacteriol 184:5912-5925. http://dx.doi.org/10.1128/JB.184.21.5912-5925.2002.
22. Grozdanov L, Raasch C, Schulze J, Sonnenborn U, Gottschalk G, Hacker J, Dobrindt U. 2004. Analysis of the genome structure of the nonpathogenic probiotic Escherichia coli strain Nissle 1917. J Bacteriol 186:5432-5441. http://dx.doi.org/10.1128/JB.186.16.5432-5441.2004.
23. Rund SA, Rohde H, Sonnenborn U, Oelschlaeger TA. 2013. Antagonistic effects of probiotic Escherichia coli Nissle 1917 on EHEC strains of serotype O104:H4 and O157:H7. Int J Med Microbiol 303:1-8. http://dx.doi.org/10.1016/j.ijmm.2012.11.006.
24. Bachmann BJ. 1996. Derivations and genotypes of some mutant derivatives of Escherichia coli K-12, p 2460-2488. In Neidhardt FC, Curtiss R, III, Ingraham JI, Lin ECC, Low KB, Magasanik B, Reznikoff WS, Riley M, Schaechter M, Umbarger HE (ed), Escherichia coli and Salmonella: cellular and molecular biology, 2nd ed, vol 2. American Society for Microbiology, Washington, DC.
25. Blattner FR, Plunkett G, III, Bloch CA, Perna NT, Burland V, Riley M, Collado-Vides J, Glasner JD, Rode CK, Mayhew GF, Gregor J, Davis NW, Kirkpatrick HA, Goeden MA, Rose DJ, Mau B, Shao Y. 1997. The complete genome sequence of Escherichia coli K-12. Science 277:1453-1474. http://dx.doi.org/10.1126/science.277.5331.1453.
26. Perna NT, Plunkett G, III, Burland V, Mau B, Glasner JD, Rose DJ, Mayhew GF, Evans PS, Gregor J, Kirkpatrick HA, Posfai G, Hackett J, Klink S, Boutin A, Shao Y, Miller L, Grotbeck E, Davis NW, Lim A, Dimalanta ET, Potamousis KD, Apodaca J, Anantharaman TS, Lin J, Yen G, Schwartz DC, Welch RA, Blattner FR. 2001. Genome sequence of enterohaemorrhagic Escherichia coli O157:H7. Nature 409:529-533. http://dx.doi.org/10.1038/35054089.
27. Datsenko KA, Wanner BL. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97:6640-6645. http://dx.doi.org/10.1073/pnas.120163297.
28. Miller JH. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
29. Banwell JG, Gorbach SL, Pierce NF, Mitra R, Mondal A. 1971. Acute undifferentiated human diarrhea in the tropics. II. Alterations in intestinal fluid and electrolyte movements. J Clin Invest 50:890-900.
30. Welch RA, Burland V, Plunkett G, III, Redford P, Roesch P, Rasko D, Buckles EL, Liou SR, Boutin A, Hackett J, Stroud D, Mayhew GF, Rose DJ, Zhou S, Schwartz DC, Perna NT, Mobley HL, Donnenberg MS, Blattner FR. 2002. Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli. Proc Natl Acad Sci U S A 99:17020-17024. http://dx.doi.org/10.1073/pnas.252529799.
31. Miller CP, Bohnhoff M. 1963. Changes in the mouse's enteric microbiota associated with enhanced susceptibility to Salmonella infection following streptomycin-treatment. J Infect Dis 113:59-66. http://dx.doi.org/10.1093/infdis/113.1.59.
32. Møller AK, Leatham MP, Conway T, Nuijten PJM, de Haan LAM, Krogfelt KA, Cohen PS. 2003. An Escherichia coli MG1655 lipopolysaccharide deep-rough core mutant grows and survives in mouse cecal mucus but fails to colonize the mouse large intestine. Infect Immun 71:2142-2152. http://dx.doi.org/10.1128/IAI.71.4.2142-2152.2003.
33. Medina V, Pontarollo R, Glaeske D, Tabel H, Goldie H. 1990. Sequence of the pckA gene of Escherichia coli K-12: relevance to genetic and allosteric regulation and homology of E. coli phosphoenolpyruvate carboxykinase with the enzymes from Trypanosoma brucei and Saccharomyces cerevisiae. J Bacteriol 172:7151-7156.
34. Niersbach M, Kreuzaler F, Geerse RH, Postma PW, Hirsch HJ. 1992. Cloning and nucleotide sequence of the Escherichia coli K-12 ppsA gene, encoding PEP synthase. Mol Gen Genet 231:332-336.
35. Goldie AH, Sanwal BD. 1980. Genetic and physiological characterization of Escherichia coli mutants deficient in phosphoenolpyruvate carboxykinase activity. J Bacteriol 141:1115-1121.
36. Leatham MP, Banerjee S, Autieri SM, Mercado-Lubo R, Conway T, Cohen PS. 2009. Precolonized human commensal Escherichia coli strains serve as a barrier to E. coli O157:H7 growth in the streptomycin-treated mouse intestine. Infect Immun 77:2876-2886. http://dx.doi.org/10.1128/IAI.00059-09.
37. Fabich AJ, Jones SA, Chowdhury FZ, Cernosek A, Anderson A, Smalley D, McHargue DWJ, Hightower GA, Smith JT, Autieri SM, Leatham MP, Lins JJ, Allen JH, Laux DC, Cohen PS, Conway T. 2008. Comparison of carbon nutrition for pathogenic and commensal Escherichia coli strains in the mouse intestine. Infect Immun 76:1143-1152. http://dx.doi.org/10.1128/IAI.01386-07.
38. Hoskins L. 1984. Mucin degradation by enteric bacteria: ecological aspects and implications for bacterial attachment to gut mucosa, p 51-65. In Boedecker EC (ed), Attachment of organisms to the gut mucosa, vol II. CRC Press, Inc, Boca Raton, FL.
39. Henrissat B, Davies G. 1997. Structural and sequence-based classification of glycoside hydrolases. Curr Opin Struct Biol 7:637-644. http://dx.doi.org/10.1016/S0959-440X(97)80072-3.
40. Hoskins LC, Agustines M, McKee WB, Boulding ET, Kriaris M, Niedermeyer G. 1985. Mucin degradation in human colon ecosystems. Isolation and properties of fecal strains that degrade ABH blood group antigens and oligosaccharides from mucin glycoproteins. J Clin Invest 75:944-953.
41. Ng KM, Ferreyra JA, Higginbottom SK, Lynch JB, Kashyap PC, Gopinath S, Naidu N, Choudhury B, Weimer BC, Monack DM, Sonnenburg JL. 2013. Microbiota-liberated host sugars facilitate post-antibiotic expansion of enteric pathogens. Nature 502:96-99. http://dx.doi.org/10.1038/nature12503.
42. Autieri SM, Lins JJ, Leatham MP, Laux DC, Conway T, Cohen PS. 2007. L-Fucose stimulates utilization of D-ribose by Escherichia coli MG1655ΔfucAO and E. coli Nissle 1917 ΔfucAO mutants in the mouse intestine and in M9 minimal medium. Infect Immun 75:5465-5475. http://dx.doi.org/10.1128/IAI.00822-07.