Skip to main content
SpringerLink
Log in

Effects of Age and Strain on the Microbiota Colonization in an Infant Human Flora-Associated Mouse Model

  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

The establishment of human flora-associated animal models allows the in vivo manipulation of host, microbial, and environmental parameters to influence the gut microbial community. However, it is difficult to simulate infant gut microbiota in germ-free animals because of the variation and dynamic state of infant microbial communities. In this study, the effects of age and strain on intestinal microbiota were observed in an infant human flora-associated (IHFA) mouse model. To establish an IHFA model, postnatal day (PND) 1 germ-free mice (Kunming, n = 10; BALB/c, n = 10) were infected with feces from a breast-fed infant. Microbiota in the feces of BALB/c mice (at PND 7, 14, and 21), and Kunming mice (at PND 14) were analyzed by PCR-denaturing gradient gel electrophoresis. Bifidobacteria and lactobacilli levels in the feces of BALB/c and Kunming mice (PND 7/14/21) were detected by quantitative real-time PCR. The Dice similarity coefficient (Cs) for the fecal microbiota of IHFA mice in comparison with the HD donor sample was higher for BALB/c mice than for Kunming mice (P < 0.05). In addition, the DCs at PND 7 were lower than those at PND 14 and PND 21 in both mouse strains (P < 0.05). The Bifidobacteria and Lactobacillus species colonizing the BALB/c mice were similar to those in the Kunming mice (at PND 7/14/21). The bifidobacteria counts increased with age in both mouse strains, whereas the lactobacilli counts decreased with age in both strains. These results suggest that both age and strain influence microbiota patterns in the IHFA mouse model.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  1. Stark PL, Lee A (1982) The microbial ecology of the large bowel of breast-fed and formula-fed infants during the first year of life. J Med Microbiol 15:189–203

    Article  PubMed  CAS  Google Scholar 

  2. Favier CF, Vaughan EE, De Vos WM, Akkermans AD (2002) Molecular monitoring of succession of bacterial communities in human neonates. Appl Environ Microbiol 68:219–226

    Article  PubMed  CAS  Google Scholar 

  3. Penders J, Thijs C, Vink C, Stelma FF, Snijders B, Kummeling I, van den Brandt PA, Stobberingh EE (2006) Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics 118:511–521

    Article  PubMed  Google Scholar 

  4. Dimmitt RA, Staley EM, Chuang G, Tanner SM, Soltau TD, Lorenz RG (2010) Role of postnatal acquisition of the intestinal microbiome in the early development of immune function. J Pediatr Gastroenterol Nutr 51:262–273

    PubMed  CAS  Google Scholar 

  5. Hill DA, Artis D (2010) Intestinal bacteria and the regulation of immune cell homeostasis. Annu Rev Immunol 28:623–667

    Article  PubMed  CAS  Google Scholar 

  6. Sjogren YM, Tomicic S, Lundberg A, Bottcher MF, Bjorksten B, Sverremark-Ekstrom E, Jenmalm MC (2009) Influence of early gut microbiota on the maturation of childhood mucosal and systemic immune responses. Clin Exp Allergy 39:1842–1851

    Article  PubMed  CAS  Google Scholar 

  7. Edwards CA, Rumney C, Davies M, Parrett AM, Dore J, Martin F, Schmitt J, Stahl B, Norin E, Midtvedt T, Rowland IR, Heavey P, Kohler H, Stocks B, Schroten H (2003) A human flora-associated rat model of the breast-fed infant gut. J Pediatr Gastroenterol Nutr 37:168–177

    Article  PubMed  Google Scholar 

  8. Szajewska H, Mrukowicz JZ (2001) Probiotics in the treatment and prevention of acute infectious diarrhea in infants and children: a systematic review of published randomized, double-blind, placebo-controlled trials. J Pediatr Gastroenterol Nutr 33(Suppl 2):17–25

    Article  Google Scholar 

  9. Mshvildadze M, Neu J, Mai V (2008) Intestinal microbiota development in the premature neonate: establishment of a lasting commensal relationship. Nutr Rev 66:658–663

    Article  PubMed  Google Scholar 

  10. Huffnagle GB (2010) The microbiota and allergies/asthma. PLoS Pathog 6:e1000549

    Article  PubMed  Google Scholar 

  11. Isolauri E, Kalliomaki M, Laitinen K, Salminen S (2008) Modulation of the maturing gut barrier and microbiota: a novel target in allergic disease. Curr Pharm Des 14:1368–1375

    Article  PubMed  CAS  Google Scholar 

  12. Vael C, Vanheirstraeten L, Desager KN, Goossens H (2011) Denaturing gradient gel electrophoresis of neonatal intestinal microbiota in relation to the development of asthma. BMC Microbiol 11:68

    Article  PubMed  CAS  Google Scholar 

  13. Faith JJ, Rey FE, O’Donnell D, Karlsson M, McNulty NP, Kallstrom G, Goodman AL, Gordon JI (2010) Creating and characterizing communities of human gut microbes in gnotobiotic mice. ISME J 4:1094–1098

    Article  PubMed  Google Scholar 

  14. Hirayama K, Itoh K (2005) Human flora-associated (HFA) animals as a model for studying the role of intestinal flora in human health and disease. Curr Issues Intest Microbiol 6:69–75

    PubMed  Google Scholar 

  15. Gootenberg DB, Turnbaugh PJ (2011) Companion animals symposium: humanized animal models of the microbiome. J Anim Sci 89:1531–1537

    Article  PubMed  CAS  Google Scholar 

  16. Turnbaugh PJ, Ridaura VK, Faith JJ, Rey FE, Knight R, Gordon JI (2009) The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci Transl Med 1:6ra14

    Article  PubMed  Google Scholar 

  17. Corpet D (1980) A dynamic study of drug resistance in populations of fecal Escherichia coli from axenic mice, fed chlortetracycline continuously and associated with flora from infant, calf and piglet (author’s transl). Ann Microbiol (Paris) 131B:309–318

    CAS  Google Scholar 

  18. Hentges DJ, Marsh WW, Petschow BW, Thal WR, Carter MK (1992) Influence of infant diets on the ecology of the intestinal tract of human flora-associated mice. J Pediatr Gastroenterol Nutr 14:146–152

    Article  PubMed  CAS  Google Scholar 

  19. Butel MJ, Roland N, Hibert A, Popot F, Favre A, Tessedre AC, Bensaada M, Rimbault A, Szylit O (1998) Clostridial pathogenicity in experimental necrotising enterocolitis in gnotobiotic quails and protective role of bifidobacteria. J Med Microbiol 47:391–399

    Article  PubMed  CAS  Google Scholar 

  20. Catala I, Butel MJ, Bensaada M, Popot F, Tessedre AC, Rimbault A, Szylit O (1999) Oligofructose contributes to the protective role of bifidobacteria in experimental necrotising enterocolitis in quails. J Med Microbiol 48:89–94

    Article  PubMed  CAS  Google Scholar 

  21. Butel MJ, Waligora-Dupriet AJ, Szylit O (2002) Oligofructose and experimental model of neonatal necrotising enterocolitis. Br J Nutr 87(Suppl 2):213–219

    Article  Google Scholar 

  22. Solis G, de Los Reyes-Gavilan CG, Fernandez N, Margolles A, Gueimonde M (2010) Establishment and development of lactic acid bacteria and bifidobacteria microbiota in breast-milk and the infant gut. Anaerobe 16:307–310

    Article  PubMed  CAS  Google Scholar 

  23. Hirayama K, Miyaji K, Kawamura S, Itoh K, Takahashi E, Mitsuoka T (1995) Development of intestinal flora of human-flora-associated (HFA) mice in the intestine of their offspring. Exp Anim 44:219–222

    Article  PubMed  CAS  Google Scholar 

  24. Silley P (2009) Human flora-associated rodents: does the data support the assumptions. Microb Biotechnol 2:6–14

    Article  PubMed  Google Scholar 

  25. Yuan J, Zeng B, Niu R, Tang H, Li W, Zhang Z, Wei H (2011) The development and stability of the genus Bacteroides from human gut microbiota in HFA mice model. Curr Microbiol 62:1107–1112

    Article  PubMed  CAS  Google Scholar 

  26. Pang X, Hua X, Yang Q, Ding D, Che C, Cui L, Jia W, Bucheli P, Zhao L (2007) Inter-species transplantation of gut microbiota from human to pigs. ISME J 1:156–162

    Article  PubMed  CAS  Google Scholar 

  27. Muyzer G, de Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700

    PubMed  CAS  Google Scholar 

  28. Penders J, Vink C, Driessen C, London N, Thijs C, Stobberingh EE (2005) Quantification of Bifidobacterium spp., Escherichia coli and Clostridium difficile in faecal samples of breast-fed and formula-fed infants by real-time PCR. FEMS Microbiol Lett 243:141–147

    Article  PubMed  CAS  Google Scholar 

  29. Walter J, Hertel C, Tannock GW, Lis CM, Munro K, Hammes WP (2001) Detection of Lactobacillus, Pediococcus, Leuconostoc, and Weissella species in human feces by using group-specific PCR primers and denaturing gradient gel electrophoresis. Appl Environ Microbiol 67:2578–2585

    Article  PubMed  CAS  Google Scholar 

  30. Bartosch S, Fite A, Macfarlane GT, McMurdo ME (2004) Characterization of bacterial communities in feces from healthy elderly volunteers and hospitalized elderly patients by using real-time PCR and effects of antibiotic treatment on the fecal microbiota. Appl Environ Microbiol 70:3575–3581

    Article  PubMed  CAS  Google Scholar 

  31. Monnet C, Correia K, Sarthou AS, Irlinger F (2006) Quantitative detection of Corynebacterium casei in cheese by real-time PCR. Appl Environ Microbiol 72:6972–6979

    Article  PubMed  CAS  Google Scholar 

  32. Alpert C, Sczesny S, Gruhl B, Blaut M (2008) Long-term stability of the human gut microbiota in two different rat strains. Curr Issues Mol Biol 10:17–24

    PubMed  CAS  Google Scholar 

  33. Friswell MK, Gika H, Stratford IJ, Theodoridis G, Telfer B, Wilson ID, McBain AJ (2010) Site and strain-specific variation in gut microbiota profiles and metabolism in experimental mice. PLoS ONE 5:e8584

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank Jiong Ren and Huan Tang for the fecal sample's of their babies. This study was supported by the National Basic Research Program of China (20013CB531406), the National Department Public Benefit Research Foundation (201202023-04) and the National Basic Research Program of China (2007CB513007).

Author information

Authors and Affiliations

  1. Department of Laboratory Animal Science, College of Basic Medical Sciences, Third Military Medical University, Gaotanyan Street, Chongqing, China

    Benhua Zeng, Jing Yuan, Wenxia Li, Huan Tang & Hong Wei

  2. Institute of Immunology, Third Military Medical University, Gaotanyan Street 30, Chongqing, 400038, China

    Guiqing Li

Authors
  1. Benhua Zeng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Guiqing Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jing Yuan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Wenxia Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Huan Tang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hong Wei
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hong Wei.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zeng, B., Li, G., Yuan, J. et al. Effects of Age and Strain on the Microbiota Colonization in an Infant Human Flora-Associated Mouse Model. Curr Microbiol 67, 313–321 (2013). https://doi.org/10.1007/s00284-013-0360-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00284-013-0360-3

Keywords

Search

Navigation