Cited by 21Escherichia coli research studiesBacteriophages and microbial interactionsBacterial Genetics and Biotechnology

The Probiotic Escherichia coli Strain Nissle 1917 Combats Lambdoid Bacteriophages stx and λ

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Bury, Susanne, Soundararajan, Manonmani, Bharti, Richa, von Bünau, Rudolf, Förstner, Konrad U., Oelschlaeger, Tobias A.·2018·Frontiers in Microbiology

Abstract

Shiga toxin (Stx) producing E. coli (STEC) such as Enterohemorrhagic E. coli (EHEC) are the major cause of foodborne illness in humans. In vitro studies showed the probiotic Escherichia coli strain Nissle 1917 (EcN) to efficiently inhibit the production of Stx. Life threatening EHEC strains as for example the serotype O104:H4, responsible for the great outbreak in 2011 in Germany, evolutionary developed from certain E. coli strains which got infected by stx2-encoding lambdoid phages turning the E. coli into lysogenic and subsequently Stx producing strains. Since antibiotics induce stx genes and Stx production, EHEC infected persons are not recommended to be treated with antibiotics. Therefore, EcN might be an alternative medication. However, because even commensal E. coli strains might be converted into Stx-producers after becoming host to a stx encoding prophage, we tested EcN for stx-phage genome integration. Our experiments revealed the resistance of EcN towards not only stx-phages but also against lambda-phages. This resistance was not based on the lack of or by mutated phage receptors. Rather it involved the expression of a phage repressor (pr) gene of a defective prophage in EcN which was able to partially protect E. coli K-12 strain MG1655 against stx and lambda phage infection. Furthermore, we observed EcN to inactivate phages and thereby to protect E. coli K-12 strains against infection by stx- as well as lambda-phages. Inactivation of lambda-phages was due to binding of lambda-phages to LamB of EcN whereas inactivation of stx-phages was caused by a thermostable protein of EcN. These properties together with its ability to inhibit Stx production make EcN a good candidate for the prevention of illness caused by EHEC and probably for the treatment of already infected people.

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  • Preclinical studies have demonstrated efficacy of phages targeting colibactin-producing Escherichia coli.

    “and colibactin-producing Escherichia coli [66]”

    From Phage therapy in oncology: opportunities for cancer prevention and treatment (2026) · cites this paper as [66]

    The Results section ('EcN protects K-12 strains from phage infection'; page unavailable) reports that probiotic E. coli reduced stx-phage levels, not that phages targeted colibactin-producing E. coli. A search for colibactin and preclinical efficacy found no passage in our copy addressing that claim. (LLM, conf=0.76)

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  1. Balamurugan S. Ahmed R. Gao A. Strange P. (2017). Comparison of the fate of the top six non-O157 shiga-toxin producing Escherichia coli (STEC) and E. coli O157:H7 during the manufacture of dry fermented sausages. Int. J. Food Microbiol. 259, 14– 21. 10.1016/j.ijfoodmicro.2017.07.018 28779623 · DOI
  2. Bettelheim K. A. (2007). The non-O157 shiga-toxigenic (verocytotoxigenic) Escherichia coli; under-rated pathogens. Crit. Rev. Microbiol. 33, 67– 87. 10.1080/10408410601172172 17453930 · DOI
  3. Bielaszewska M. Mellmann A. Zhang W. Kock R. Fruth A. Bauwens A.. (2011). Characterisation of the Escherichia coli strain associated with an outbreak of haemolytic uraemic syndrome in Germany, 2011: a microbiological study. Lancet Infect. Dis. 11, 671– 676. 10.1016/S1473-3099(11)70165-7 21703928 · DOI
  4. Bondy-Denomy J. Qian J. Westra E. R. Buckling A. Guttman D. S. Davidson A. R.. (2016). Prophages mediate defense against phage infection through diverse mechanisms. ISME J. 10, 2854– 2866. 10.1038/ismej.2016.79 27258950 PMC5148200 · DOI
  5. Brussow H. Canchaya C. Hardt W. D. (2004). Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol. Mol. Biol. Rev. 68, 560– 602, table of contents. 10.1128/MMBR.68.3.560-602.2004 15353570 PMC515249 · DOI
  6. Byrne L. Jenkins C. Launders N. Elson R. Adak G. K. (2015). The epidemiology, microbiology and clinical impact of Shiga toxin-producing Escherichia coli in England, 2009-2012. Epidemiol. Infect. 143, 3475– 3487. 10.1017/S0950268815000746 25920912 PMC9150938 · DOI
  7. Casjens S. R. Hendrix R. W. (2015). Bacteriophage lambda: early pioneer and still relevant. Virology 479–480, 310– 330. 10.1016/j.virol.2015.02.010 25742714 PMC4424060 · DOI
  8. Chatterjee S. Rothenberg E. (2012). Interaction of bacteriophage l with its E. coli receptor, LamB. Viruses 4, 3162– 3178. 10.3390/v4113162 23202520 PMC3509688 · DOI
  9. Conway E. M. (2015). HUS and the case for complement. Blood 126, 2085– 2090. 10.1182/blood-2015-03-569277 26396094 · DOI
  10. Cumby N. Edwards A. M. Davidson A. R. Maxwell K. L. (2012). The bacteriophage HK97 gp15 moron element encodes a novel superinfection exclusion protein. J. Bacteriol. 194, 5012– 5019. 10.1128/JB.00843-12 22797755 PMC3430355 · DOI
  11. Darmon E. Leach D. R. (2014). Bacterial genome instability. Microbiol. Mol. Biol. Rev. 78, 1– 39. 10.1128/MMBR.00035-13 24600039 PMC3957733 · DOI
  12. Dupuis M. E. Villion M. Magadan A. H. Moineau S. (2013). CRISPR-Cas and restriction-modification systems are compatible and increase phage resistance. Nat. Commun. 4: 2087. 10.1038/ncomms3087 23820428 · DOI
  13. Edgar R. Domrachev M. Lash A. E. (2002). Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 30, 207– 210. 10.1093/nar/30.1.207 11752295 PMC99122 · DOI · Paper page
  14. Eklund M. Leino K. Siitonen A. (2002). Clinical Escherichia coli strains carrying stx genes: stx variants and stx-positive virulence profiles. J. Clin. Microbiol. 40, 4585– 4593. 10.1128/JCM.40.12.4585-4593.2002 12454157 PMC154619 · DOI
  15. Forstner K. U. Vogel J. Sharma C. M. (2014). READemption-a tool for the computational analysis of deep-sequencing-based transcriptome data. Bioinformatics 30, 3421– 3423. 10.1093/bioinformatics/btu533 25123900 · DOI
  16. Frank C. Werber D. Cramer J. P. Askar M. Faber M. An Der Heiden M.. (2011). Epidemic profile of Shiga-toxin-producing Escherichia coli O104:H4 outbreak in Germany. N. Engl. J. Med. 365, 1771– 1780. 10.1056/NEJMoa1106483 21696328 · DOI · Paper page
  17. Fraser M. E. Fujinaga M. Cherney M. M. Melton-Celsa A. R. Twiddy E. M. O'brien A. D.. (2004). Structure of shiga toxin type 2 (Stx2) from Escherichia coli O157:H7. J. Biol. Chem. 279, 27511– 27517. 10.1074/jbc.M401939200 15075327 · DOI
  18. Freese N. H. Norris D. C. Loraine A. E. (2016). Integrated genome browser: visual analytics platform for genomics. Bioinformatics 32, 2089– 2095. 10.1093/bioinformatics/btw069 27153568 PMC4937187 · DOI
  19. Fuchs S. Muhldorfer I. Donohue-Rolfe A. Kerenyi M. Emody L. Alexiev R.. (1999). Influence of RecA on in vivo virulence and Shiga toxin 2 production in Escherichia coli pathogens. Microb. Pathog. 27, 13– 23. 10.1006/mpat.1999.0279 10371706 · DOI
  20. Gamage S. D. Patton A. K. Strasser J. E. Chalk C. L. Weiss A. A. (2006). Commensal bacteria influence Escherichia coli O157:H7 persistence and Shiga toxin production in the mouse intestine. Infect. Immun. 74, 1977– 1983. 10.1128/IAI.74.3.1977-1983.2006 16495578 PMC1418637 · DOI
  21. Gamage S. D. Strasser J. E. Chalk C. L. Weiss A. A. (2003). Nonpathogenic Escherichia coli can contribute to the production of Shiga toxin. Infect. Immun. 71, 3107– 3115. 10.1128/IAI.71.6.3107-3115.2003 12761088 PMC155771 · DOI
  22. Grillo-Puertas M. Villegas J. M. Rintoul M. R. Rapisarda V. A. (2012). Polyphosphate degradation in stationary phase triggers biofilm formation via LuxS quorum sensing system in Escherichia coli. PLoS ONE 7: e50368. 10.1371/journal.pone.0050368 23226268 PMC3511525 · DOI
  23. Hancock V. Vejborg R. M. Klemm P. (2010). Functional genomics of probiotic Escherichia coli Nissle 1917 and 83972, and UPEC strain CFT073: comparison of transcriptomes, growth and biofilm formation. Mol. Genet. Genomics 284, 437– 454. 10.1007/s00438-010-0578-8 20886356 · DOI
  24. Herold S. Siebert J. Huber A. Schmidt H. (2005). Global expression of prophage genes in Escherichia coli O157:H7 strain EDL933 in response to norfloxacin. Antimicrob. Agents Chemother. 49, 931– 944. 10.1128/AAC.49.3.931-944.2005 15728886 PMC549229 · DOI
  25. Hofer B. Ruge M. Dreiseikelmann B. (1995). The superinfection exclusion gene (sieA) of bacteriophage P22: identification and overexpression of the gene and localization of the gene product. J. Bacteriol. 177, 3080– 3086. 10.1128/jb.177.11.3080-3086.1995 7768804 PMC176996 · DOI
  26. Hoffmann S. Otto C. Kurtz S. Sharma C. M. Khaitovich P. Vogel J.. (2009). Fast mapping of short sequences with mismatches, insertions and deletions using index structures. PLoS Comput. Biol. 5: e1000502. 10.1371/journal.pcbi.1000502 19750212 PMC2730575 · DOI
  27. Hoyland-Kroghsbo N. M. Maerkedahl R. B. Svenningsen S. L. (2013). A quorum-sensing-induced bacteriophage defense mechanism. MBio 4: e00362– 12. 10.1128/mBio.00362-12 23422409 PMC3624510 · DOI
  28. Islam M. R. Ogura Y. Asadulghani M. Ooka T. Murase K. Gotoh Y. (2012). A sensitive and simple plaque formation method for the Stx2 phage of Escherichia coli O157:H7, which does not form plaques in the standard plating procedure. Plasmid 67, 227– 235. 10.1016/j.plasmid.2011.12.001 22186359 · DOI
  29. Islam S. U. (2016). Clinical uses of probiotics. Medicine (Baltimore) 95, e2658. 10.1097/MD.0000000000002658 26844491 PMC4748908 · DOI
  30. Jandhyala S. M. Talukdar R. Subramanyam C. Vuyyuru H. Sasikala M. Nageshwar Reddy D. (2015). Role of the normal gut microbiota. World J. Gastroenterol. 21, 8787– 8803. 10.3748/wjg.v21.i29.8787 26269668 PMC4528021 · DOI · Paper page
  31. Karch H. Bielaszewska M. Bitzan M. Schmidt H. (1999). Epidemiology and diagnosis of Shiga toxin-producing Escherichia coli infections. Diagn. Microbiol. Infect. Dis. 34, 229– 243. 10.1016/S0732-8893(99)00031-0 10403103 · DOI
  32. Kim J. W. Dutta V. Elhanafi D. Lee S. Osborne J. A. Kathariou S. (2012). A novel restriction-modification system is responsible for temperature-dependent phage resistance in Listeria monocytogenes ECII. Appl. Environ. Microbiol. 78, 1995– 2004. 10.1128/AEM.07086-11 22247158 PMC3298167 · DOI
  33. Kuhnert P. Nicolet J. Frey J. (1995). Rapid and accurate identification of Escherichia coli K-12 strains. Appl. Environ. Microbiol. 61, 4135– 4139. 8526531 PMC167724
  34. Labrie S. J. Samson J. E. Moineau S. (2010). Bacteriophage resistance mechanisms. Nat. Rev. Microbiol. 8, 317– 327. 10.1038/nrmicro2315 20348932 · DOI
  35. Ladero V. Garcia P. Bascaran V. Herrero M. Alvarez M. A. Suarez J. E. (1998). Identification of the repressor-encoding gene of the Lactobacillus bacteriophage A2. J. Bacteriol. 180, 3474– 3476. 9642205 PMC107307
  36. Leatham M. P. Banerjee S. Autieri S. M. Mercado-Lubo R. Conway T. Cohen P. S. (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. 10.1128/IAI.00059-09 19364832 PMC2708557 · DOI
  37. Love M. I. Huber W. Anders S. (2014). Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15: 550. 10.1186/s13059-014-0550-8 25516281 PMC4302049 · DOI · Paper page
  38. Łusiak-Szelachowska M. Weber-Dąbrowska B. Jończyk-Matysiak E. Wojciechowska R. Górski A. (2017). Bacteriophages in the gastrointestinal tract and their implications. Gut Pathog. 9: 44. 10.1186/s13099-017-0196-7 28811841 PMC5553654 · DOI
  39. Martin M. (2011). Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet. J. 17, 10– 12. 10.14806/ej.17.1.200 · DOI · Paper page
  40. Matsuura Y. Takehira M. Joti Y. Ogasahara K. Tanaka T. Ono N.. (2015). Thermodynamics of protein denaturation at temperatures over 100 degrees C: CutA1 mutant proteins substituted with hydrophobic and charged residues. Sci. Rep. 5: 15545. 10.1038/srep15545 26497062 PMC4620440 · DOI
  41. Mattila-Sandholm T. Myllärinen P. Crittenden R. Mogensen G. Fondén R. Saarela M. (2002). Technological challenges for future probiotic foods. Int. Dairy J. 12, 173– 182. 10.1016/S0958-6946(01)00099-1 · DOI
  42. Mead P. S. Griffin P. M. (1998). Escherichia coli O157:H7. Lancet 352, 1207– 1212. 10.1016/S0140-6736(98)01267-7 9777854 · DOI
  43. Melton-Celsa A. R. (2014). Shiga toxin (Stx) classification, structure, and function. Microbiol Spectr 2: EHEC-0024-2013 10.1128/microbiolspec.EHEC-0024-2013 PMC4270005 25530917 · DOI
  44. Mills S. Shanahan F. Stanton C. Hill C. Coffey A. Ross R. P. (2013). Movers and shakers: influence of bacteriophages in shaping the mammalian gut microbiota. Gut Microbes 4, 4– 16. 10.4161/gmic.22371 23022738 PMC3555884 · DOI
  45. Mohsin M. Guenther S. Schierack P. Tedin K. Wieler L. H. (2015). Probiotic Escherichia coli Nissle 1917 reduces growth, Shiga toxin expression, release and thus cytotoxicity of enterohemorrhagic Escherichia coli. Int. J. Med. Microbiol. 305, 20– 26. 10.1016/j.ijmm.2014.10.003 25465158 · DOI
  46. Neely M. N. Friedman D. I. (1998). Functional and genetic analysis of regulatory regions of coliphage H-19B: location of shiga-like toxin and lysis genes suggest a role for phage functions in toxin release. Mol. Microbiol. 28, 1255– 1267. 10.1046/j.1365-2958.1998.00890.x 9680214 · DOI
  47. Nissle A. (1925). Weiteres über Grundlagen und Praxis der Mutaflorbehandlung. Dt. Med. Wschr. 44, 1809– 1813. 10.1055/s-0028-1137292 · DOI
  48. O'brien A. D. Newland J. W. Miller S. F. Holmes R. K. Smith H. W. Formal S. B. (1984). Shiga-like toxin-converting phages from Escherichia coli strains that cause hemorrhagic colitis or infantile diarrhea. Science 226, 694– 696. 10.1126/science.6387911 6387911 · DOI
  49. Oelschlaeger T. A. (2010). Mechanisms of probiotic actions - a review. Int. J. Med. Microbiol. 300, 57– 62. 10.1016/j.ijmm.2009.08.005 19783474 · DOI
  50. Pacheco A. R. Sperandio V. (2012). Shiga toxin in enterohemorrhagic E.coli: regulation and novel anti-virulence strategies. Front. Cell. Infect. Microbiol. 2: 81. 10.3389/fcimb.2012.00081 22919672 PMC3417539 · DOI
  51. Paton J. C. Paton A. W. (1998). Pathogenesis and diagnosis of Shiga toxin-producing Escherichia coli infections. Clin. Microbiol. Rev. 11, 450– 479. 9665978 PMC88891
  52. Pedersen M. G. Hansen C. Riise E. Persson S. Olsen K. E. (2008). Subtype-specific suppression of Shiga toxin 2 released from Escherichia coli upon exposure to protein synthesis inhibitors. J. Clin. Microbiol. 46, 2987– 2991. 10.1128/JCM.00871-08 18650349 PMC2546733 · DOI
  53. Pennington H. (2010). Escherichia coli O157. Lancet 376, 1428– 1435. 10.1016/S0140-6736(10)60963-4 20971366 · DOI
  54. Ranade K. Poteete A. R. (1993). Superinfection exclusion (sieB) genes of bacteriophages P22 and lambda. J. Bacteriol. 175, 4712– 4718. 10.1128/jb.175.15.4712-4718.1993 8335629 PMC204922 · DOI
  55. Randall-Hazelbauer L. Schwartz M. (1973). Isolation of the bacteriophage lambda receptor from Escherichia coli. J. Bacteriol. 116, 1436– 1446. 4201774 PMC246503
  56. Reissbrodt R. Hammes W. P. Dal Bello F. Prager R. Fruth A. Hantke K.. (2009). Inhibition of growth of Shiga toxin-producing Escherichia coli by nonpathogenic Escherichia coli. FEMS Microbiol. Lett. 290, 62– 69. 10.1111/j.1574-6968.2008.01405.x 19016876 · DOI
  57. Rund S. A. Rohde H. Sonnenborn U. Oelschlaeger T. A. (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. 10.1016/j.ijmm.2012.11.006 23312798 · DOI
  58. Samson J. E. Magadan A. H. Sabri M. Moineau S. (2013). Revenge of the phages: defeating bacterial defences. Nat. Rev. Microbiol. 11, 675– 687. 10.1038/nrmicro3096 23979432 · DOI
  59. Schmidt H. (2001). Shiga-toxin-converting bacteriophages. Res. Microbiol. 152, 687– 695. 10.1016/S0923-2508(01)01249-9 11686382 · DOI
  60. Schmidt H. Bielaszewska M. Karch H. (1999). Transduction of enteric Escherichia coli isolates with a derivative of Shiga toxin 2-encoding bacteriophage phi3538 isolated from Escherichia coli O157:H7. Appl. Environ. Microbiol. 65, 3855– 3861. 10473386 PMC99711
  61. Schultz M. (2008). Clinical use of E. coli Nissle 1917 in inflammatory bowel disease. Inflamm. Bowel. Dis. 14, 1012– 1018. 10.1002/ibd.20377 18240278 · DOI · Paper page
  62. Schwartz M. (1976). The adsorption of coliphage lambda to its host: effect of variations in the surface density of receptor and in phage-receptor affinity. J. Mol. Biol. 103, 521– 536. 10.1016/0022-2836(76)90215-1 181582 · DOI
  63. Serra-Moreno R1 Jofre J. Muniesa M. (2008). The CI repressors of Shiga toxin-converting prophages are involved in coinfection of Escherichia coli strains, which causes a down regulation in the production of Shiga toxin 2. J. Bacteriol. 190, 4722– 4735. 10.1128/JB.00069-08 18469095 PMC2446792 · DOI
  64. Smith D. L. James C. E. Sergeant M. J. Yaxian Y. Saunders J. R. McCarthy A. J.. (2007). Short-tailed stx phages exploit the conserved YaeT protein to disseminate Shiga toxin genes among enterobacteria. J. Bacteriol. 189, 7223– 7233. 10.1128/JB.00824-07 17693515 PMC2168440 · DOI
  65. Sonnenborn U. (2016). Escherichia coli strain Nissle 1917-from bench to bedside and back: history of a special Escherichia coli strain with probiotic properties. FEMS Microbiol. Lett. 363: fnw212. 10.1093/femsle/fnw212 27619890 · DOI · Paper page
  66. Tesh V. L. (2012). The induction of apoptosis by Shiga toxins and ricin. Curr. Top. Microbiol. Immunol. 357, 137– 178. 10.1007/82_2011_155 22130961 · DOI
  67. Toh H. Oshima K. Toyoda A. Ogura Y. Ooka T. Sasamoto H.. (2010). Complete genome sequence of the wild-type commensal Escherichia coli strain SE15, belonging to phylogenetic group B2. J. Bacteriol. 192, 1165– 1166. 10.1128/JB.01543-09 20008064 PMC2812965 · DOI
  68. Touchon M. Hoede C. Tenaillon O. Barbe V. Baeriswyl S. Bidet P.. (2009). Organised genome dynamics in the Escherichia coli species results in highly diverse adaptive paths. PLoS Genet. 5: e1000344. 10.1371/journal.pgen.1000344 19165319 PMC2617782 · DOI
  69. Troge A. Scheppach W. Schroeder B. O. Rund S. A. Heuner K. Wehkamp J.. (2012). More than a marine propeller–the flagellum of the probiotic Escherichia coli strain Nissle 1917 is the major adhesin mediating binding to human mucus. Int. J. Med. Microbiol. 302, 304– 314. 10.1016/j.ijmm.2012.09.004 23131416 · DOI
  70. Vally H. Hall G. Dyda A. Raupach J. Knope K. Combs B.. (2012). Epidemiology of Shiga toxin producing Escherichia coli in Australia, 2000-2010. BMC Public Health 12: 63. 10.1186/1471-2458-12-63 22264221 PMC3398300 · DOI
  71. Vidakovic L. Singh P. K. Hartmann R. Nadell C. D. Drescher K. (2018). Dynamic biofilm architecture confers individual and collective mechanisms of viral protection. Nat. Microbiol. 3, 26– 31. 10.1038/s41564-017-0050-1 29085075 PMC5739289 · DOI
  72. Wagner P. L. Livny J. Neely M. N. Acheson D. W. Friedman D. I. Waldor M. K. (2002). Bacteriophage control of Shiga toxin 1 production and release by Escherichia coli. Mol. Microbiol. 44, 957– 970. 10.1046/j.1365-2958.2002.02950.x 12010491 · DOI
  73. Weiss G. (2013). Intestinal irony: how probiotic bacteria outcompete bad bugs. Cell Host Microbe 14, 3– 4. 10.1016/j.chom.2013.07.003 23870306 · DOI
  74. Zhang X. Mcdaniel A. D. Wolf L. E. Keusch G. T. Waldor M. K. Acheson D. W. (2000). Quinolone antibiotics induce Shiga toxin-encoding bacteriophages, toxin production, and death in mice. J. Infect. Dis. 181, 664– 670. 10.1086/315239 10669353 · DOI
  75. Zhou K. Zhou L. Lim Q. Zou R. Stephanopoulos G. Too H. P. (2011). Novel reference genes for quantifying transcriptional responses of Escherichia coli to protein overexpression by quantitative PCR. BMC Mol. Biol. 12: 18. 10.1186/1471-2199-12-18 21513543 PMC3110127 · DOI
  76. Zhou Y. Liang Y. Lynch K. H. Dennis J. J. Wishart D. S. (2011). PHAST: a fast phage search tool. Nucleic Acids Res. 39, W347– W352. 10.1093/nar/gkr485 21672955 PMC3125810 · DOI

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Authors
Bury, S., Soundararajan, M., Bharti, R., von Bünau, R., Förstner, K. U., & Oelschlaeger, T. A.
Affiliations
University of Würzburg (DE)
Corresponding author
Oelschlaeger, Tobias A.
Venue
Frontiers in Microbiology
Published
2018-05-29
Volume
9
Pages
929-929
ISSN
1664-302X (ISSN-L)
OpenAlex
W2807130658
Cited by
21
References
6
Citations by year
2026: 2 · 2025: 1 · 2024: 2 · 2023: 4 · 2022: 5 · 2021: 3 · 2020: 3 · 2019: 1
FWCI
1.20
Type
journal article
Language
en
Open access
Locations
  • Frontiers in Microbiology (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Online Publication Service of Würzburg University (Würzburg University) (submittedVersion, cc-by)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Escherichia coli research studies
  • Physical Sciences › Environmental Science › Ecology › Bacteriophages and microbial interactions
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Keywords
Escherichia coli Nissle 1917, probiotics, Shiga toxin-producing Escherichia coli, enterohemorrhagic Escherichia coli, bacteriophage lambda, prophage integration, phage resistance, phage inactivation, thermostable proteins, foodborne illness prevention

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