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Administration of the Probiotic Escherichia coli Strain A0 34/86 Resulted in a Stable Colonization of the Human Intestine During the First Year of Life

Probiotics and Antimicrobial Proteins volume 12, pages 343–350 (2020)Cite this article

Abstract

Colinfant New Born (CNB) is an orally administered probiotic preparation containing the Escherichia coli strain A0 34/86, which is specially marketed for use in newborns and infants. Although the impact of different probiotics on the composition of the human gut microbiota has been previously described, the effects of E. coli probiotic consumption during infancy on the development of intestinal microbiota are not known. The effect of oral administration of CNB on the Enterobacteriaceae population was mapped using 16S rRNA gene sequencing in DNA samples isolated from the stools of one infant collected at 177 different time points during the first year of life. E. coli strains turnover was analyzed based on the detection of 26 genetic determinants, phylogroups, and pulsed-field gel electrophoresis (PFGE) analysis. Administration of CNB during the second and third month of life introduced the Escherichia genus to the infant’s intestinal tract, and Escherichia became dominant among the Enterobacteriaceae family (p < 0.01). Genetic determinants, typical for probiotic E. coli A0 34/86 strain, were detected on the first day after application of CNB and persisted all year. In addition, nine transient E. coli strains were identified; these strains harbored different genetic determinants and showed different PFGE profiles. Transient strains were detected from 2 to 24 days in the stool samples. The first Escherichia colonizer originated from the application of the CNB probiotic preparation. Probiotic E. coli A0 34/86 successfully colonized the intestinal tract of an infant and became resident during the first year of life.

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References

  1. Nowrouzian F, Hesselmar B, Saalman R, Strannegard IL, Aberg N, Wold AE, Adlerberth I (2003) Escherichia coli in infants' intestinal microflora: colonization rate, strain turnover, and virulence gene carriage. Pediatr Res 54:8–14

    CAS  Article  Google Scholar 

  2. Mukhopadhya I, Hansen R, El-Omar EM, Hold GL (2012) IBD-what role do Proteobacteria play? Nat Rev Gastroenterol Hepatol 9:219–230

    CAS  Article  Google Scholar 

  3. Alsalah D, Al-Jassim N, Timraz K, Hong PY (2015) Assessing the groundwater quality at a Saudi Arabian agricultural site and the occurrence of opportunistic pathogens on irrigated food produce. Int J Environ Res Public Health 12:12391–12411

    CAS  Article  Google Scholar 

  4. Kuang YS, Li SH, Guo Y, Lu JH, He JR, Luo BJ, Jiang FJ, Shen H, Papasian CJ, Pang H, Xia HM, Deng HW, Qiu X (2016) Composition of gut microbiota in infants in China and global comparison. Sci Rep 6:36666

    CAS  Article  Google Scholar 

  5. de Muinck EJ, Oien T, Storrø O, Johnsen R, Stenseth NC, Rønningen KS, Rudi K (2011) Diversity, transmission and persistence of Escherichia coli in a cohort of mothers and their infants. Environ Microbiol Rep 3:352–359

    Article  Google Scholar 

  6. Rudi K, Storro O, Oien T, Johnsen R (2012) Modelling bacterial transmission in human allergen-specific IgE sensitization. Lett Appl Microbiol 54:447–454

    CAS  Article  Google Scholar 

  7. Russo TA, Johnson JR (2000) Proposal for a new inclusive designation for extraintestinal pathogenic isolates of Escherichia coli: ExPEC. J Infect Dis 181:1753–1754

    CAS  Article  Google Scholar 

  8. Vila J, Sáez-López E, Johnson JR, Römling U, Dobrindt U, Cantón R, Giske CG, Naas T, Carattoli A, Martínez-Medina M, Bosch J, Retamar P, Rodríguez-Baño J, Baquero F, Soto SM (2016) Escherichia coli: an old friend with new tidings. FEMS Microbiol Rev 40:437–463

    CAS  Article  Google Scholar 

  9. Versalovic J (2013) The human microbiome and probiotics: implications for pediatrics. Ann Nutr Metab 2:42–52

    Article  Google Scholar 

  10. Wassenaar TM (2016) Insights from 100 years of research with probiotic E. coli. Eur J Microbiol Immunol (Bp) 6:147–161

    Article  Google Scholar 

  11. Lodinová-Zadniková R, Tlaskalova H, Bartakova Z (1991) The antibody response in infants after colonisation of the intestine with E. coli 083. Artificial colonisation used as prevention against nosocomial infections. Adv Exp Med Biol 310:329–333

    Article  Google Scholar 

  12. Lodinová-Zádníková R, Cukrowska B, Tlaskalova-Hogenova H (2003) Oral administration of probiotic Escherichia coli after birth reduces frequency of allergies and repeated infections later in life (after 10 and 20 years). Int Arch Allergy Immunol 131:209–211

    Article  Google Scholar 

  13. Hejnova J, Dobrindt U, Nemcova R, Rusniok C, Bomba A, Frangeul L, Hacker J, Glaser P, Sebo P, Buchrieser C (2005) Characterization of the flexible genome complement of the commensal Escherichia coli strain A0 34/86 (O83 : K24 : H31). Microbiology 151:385–398

    CAS  Article  Google Scholar 

  14. Apperloo-Renkema HZ, van der Waaij D (1991) Study of colonization resistance for Enterobacteriaceae in man by experimental contamination and biotyping as well as the possible role of antibodies in the clearance of these bacteria from the intestines. Epidemiol Infect 107:619–626

    CAS  Article  Google Scholar 

  15. Souza V, Castillo A, Eguiarte LE (2002) The evolutionary ecology of Escherichia coli. Am Sci 90:332–341

    Article  Google Scholar 

  16. Lasaro M, Liu Z, Bishar R, Kelly K, Chattopadhyay S, Paul S, Sokurenko E, Zhu J, Goulian M (2014) Escherichia coli isolate for studying colonization of the mouse intestine and its application to two-component signaling knockouts. J Bacteriol 196:1723–1732

    Article  Google Scholar 

  17. Hentges DJ, Que JU, Casey SW (1985) The influence of streptomycin on the ecology of the intestine and resistance to infection. In: Adam D, Hahn H, Opferkuch W (eds) The influence of antibiotics on the host-parasite relationship II. Springer, Berlin

    Google Scholar 

  18. Hudault S, Guignot J, Servin AL (2001) Escherichia coli strains colonising the gastrointestinal tract protect germfree mice against Salmonella typhimurium infection. Gut 49:47–55

    CAS  Article  Google Scholar 

  19. Derrien M, van Hylckama Vlieg JE (2015) Fate, activity, and impact of ingested bacteria within the human gut microbiota. Trends Microbiol 23:354–366

    CAS  Article  Google Scholar 

  20. Šmajs D, Micenková L, Šmarda J, Vrba M, Sevčíková A, Vališová Z, Woznicová V (2010) Bacteriocin synthesis in uropathogenic and commensal Escherichia coli: colicin E1 is a potential virulence factor. BMC Microbiol 10:288

    Article  Google Scholar 

  21. Micenková L, Štaudová B, Bosák J, Mikalová L, Littnerová S, Vrba M, Ševčíková A, Woznicová V, Šmajs D (2014) Bacteriocin-encoding genes and ExPEC virulence determinants are associated in human fecal Escherichia coli strains. BMC Microbiol 14:109

    Article  Google Scholar 

  22. Micenková L, Beňová A, Frankovičová L, Bosák J, Vrba M, Ševčíková A, Kmeťová M, Šmajs D (2017) Human Escherichia coli isolates from hemocultures: septicemia linked to urogenital tract infections is caused by isolates harboring more virulence genes than bacteraemia linked to other conditions. Int J Med Microbiol 307:182–189

    Article  Google Scholar 

  23. Micenková L, Bosák J, Vrba M, Ševčíková A, Šmajs D (2016) Human extraintestinal pathogenic Escherichia coli strains differ in prevalence of virulence factors, phylogroups, and bacteriocin determinants. BMC Microbiol 16:218

    Article  Google Scholar 

  24. Yamamoto S, Terai A, Yuri K, Kurazono H, Takeda Y, Yoshida O (1995) Detection of urovirulence factors in Escherichia coli by multiplex polymerase chain reaction. FEMS Immunol Med Microbiol 12:85–90

    CAS  Article  Google Scholar 

  25. Bírošová E, Siegfried L, Kmeťová M, Makara A, Ostró A, Gresová A, Urdzík P, Liptáková A, Molokácová M, Bártl R, Valanský L (2004) Detection of virulence factors in alpha-haemolytic Escherichia coli strains isolated from various clinical materials. Clin Microbiol Infect 10:569–573

    Article  Google Scholar 

  26. Gómez-Moreno R, Robledo IE, Baerga-Ortiz A (2014) Direct detection and quantification of bacterial genes associated with inflammation in DNA isolated from stool. Adv Microbiol 4:1065–1075

    Article  Google Scholar 

  27. Janda JM, Abbott SL (2007) 16S rRNA gene sequencing for bacterial identification in the diagnostic laboratory: pluses, perils, and pitfalls. J Clin Microbiol 45:2761–2764

    CAS  Article  Google Scholar 

  28. Clermont O, Bonacorsi S, Bingen E (2000) Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol 66:4555–4558

    CAS  Article  Google Scholar 

  29. Tenover FC, Arbeit RD, Goering RV, Mickelsen PA, Murray BE, Persing DH, Swaminathan B (1995) Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J Clin Microbiol 33:2233–2239

    CAS  Article  Google Scholar 

  30. Tenaillon O, Skurnik D, Picard B, Denamur E (2010) The population genetics of commensal Escherichia coli. Nat Rev Microbiol 8:207–217

    CAS  Article  Google Scholar 

  31. Azad MB, Konya T, Maughan H, Guttman DS, Field CJ, Chari RS, Sears MR, Becker AB, Scott JA, Kozyrskyj AL, CHILD Study Investigators (2013) Gut microbiota of healthy Canadian infants: profiles by mode of delivery and infant diet at 4 months. Can Med Assoc J 185:385–394

    Article  Google Scholar 

  32. Taddei CR, Oliveira FF, Duarte RT, Talarico ST, Takagi EH, Ramos Carvalho II, Gomes FM, Brandt K, Martinez MB (2014) High abundance of Escherichia during the establishment of fecal microbiota in Brazilian children. Microb Ecol 67:624–634

    Article  Google Scholar 

  33. Adlerberth I, Carlsson B, de Man P, Jalil F, Khan SR, Larsson P, Mellander L, Svanborg C, Wold AE, Hanson LA (1991) Intestinal colonization with Enterobacteriaceae in Pakistani and Swedish hospital-delivered infants. Acta Paediatr Scand 80:602–610

    CAS  Article  Google Scholar 

  34. Zollner-Schwetz I, Högenauer C, Joainig M, Weberhofer P, Gorkiewicz G, Valentin T, Hinterleitner TA, Krause R (2008) Role of Klebsiella oxytoca in antibiotic-associated diarrhea. Clin Infect Dis 47:e74–e78

    Article  Google Scholar 

  35. Quin C, Estaki M, Vollman DM, Barnett JA, Gill SK, Gibson DL (2018) Probiotic supplementation and associated infant gut microbiome and health: a cautionary retrospective clinical comparison. Sci Rep 29:8283

    Article  Google Scholar 

  36. Adlerberth I, Jalil F, Carlsson B, Mellander L, Hanson LA, Larsson P, Khalil K, Wold AE (1998) High turnover rate of Escherichia coli strains in the intestinal flora of infants in Pakistan. Epidemiol Infect 121:587–598

    CAS  Article  Google Scholar 

  37. Conway T, Cohen PS (2015) Commensal and pathogenic Escherichia coli metabolism in the gut. Microbiol Spectr 3

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Acknowledgment

We thank Thomas Secrest (Secrest Editing, Ltd.) for his assistance with the English revision of the manuscript.

Funding

This study was funded by the Ministry of Education, Youth, and Sports of the Czech Republic; the European Structural and Investment Funds (CETOCOEN PLUS project: CZ.02.1.01/0.0/0.0/15_003/0000469; the RECETOX research infrastructure: LM2015051 and CZ.02.1.01/0.0/0.0/16_013/0001761); the Ministry of Health, the Czech Republic (FNBr, 65269705); and by the Grant Agency of the Czech Republic (project No. 17-24592Y). Computational resources were supplied by the Ministry of Education, Youth, and Sports of the Czech Republic under the Projects CESNET (Project No. LM2015042) and CERIT-Scientific Cloud (Project No. LM2015085) provided within the Projects Large Research, Development, and Innovations Infrastructures. Additional funding to SS was provided by the Advanced parallel project and embedded computer systems, Brno University of Technology (FIT-S-17-3994). This work was partly supported by the GAMU grant (MUNI/M/1322/2015) and the GACR grant (GA16-21649S) to DŠ.

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Authors and Affiliations

  1. Research Centre for Toxic Compounds in the Environment, Faculty of Science, Masaryk University, Kamenice 5, 625 00, Brno, Czech Republic

    Lenka Micenková, Stanislav Smatana, Adam Novotný & Eva Budinská

  2. Department of Biology, Faculty of Medicine, Masaryk University, Kamenice 5, Building A6, 625 00, Brno, Czech Republic

    Juraj Bosák & David Šmajs

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  1. Lenka Micenková
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  2. Juraj Bosák
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Correspondence to David Šmajs.

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Micenková, L., Bosák, J., Smatana, S. et al. Administration of the Probiotic Escherichia coli Strain A0 34/86 Resulted in a Stable Colonization of the Human Intestine During the First Year of Life. Probiotics & Antimicro. Prot. 12, 343–350 (2020). https://doi.org/10.1007/s12602-019-09548-3

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Keywords

  • E. coli
  • Enterobacteriaceae
  • Probiotic
  • Colinfant
  • Sequencing