Applied Microbiology and Biotechnology

, Volume 102, Issue 24, pp 10645–10663 | Cite as

Staying alive: growth and survival of Bifidobacterium animalis subsp. animalis under in vitro and in vivo conditions

  • Muireann Egan
  • Francesca Bottacini
  • Mary O’Connell Motherway
  • Patrick G. Casey
  • Ruth Morrissey
  • Silvia Melgar
  • Jean-Michel Faurie
  • Christian Chervaux
  • Tamara Smokvina
  • Douwe van SinderenEmail author
Genomics, transcriptomics, proteomics


Members of the Bifidobacterium genus are widely used as probiotics in fermented milk products. Bifidobacterium animalis subsp. animalis CNCM I-4602 grows and survives poorly in reconstituted skimmed milk (RSM). Availing of genome and transcriptome information, this poor growth and survival phenotype in milk was substantially improved by the addition of certain compounds, such as yeast extract, uric acid, glutathione, cysteine, ferrous sulfate, and a combination of magnesium sulfate and manganese sulfate. Carbohydrate utilization of CNCM I-4602 was also investigated, allowing the identification of several carbohydrate utilization gene clusters, and highlighting this strain’s inability to utilize lactose, unlike the type strain of this subspecies, B. animalis subsp. animalis ATCC25527 and the B. animalis subsp. lactis subspecies. In addition, the ability of B. animalis subsp. animalis CNCM I-4602 to colonize a murine model was investigated, which showed that this strain persists in the murine gut for a period of at least 4 weeks. Associated in vivo transcriptome analysis revealed that, among other genes, a gene cluster encoding a predicted type IVb tight adherence (Tad) pilus was upregulated, indicating that this extracellular structure plays a role in the colonization/adaptation of the murine gastrointestinal tract by this strain.


Bifidobacteria Genome sequencing Reconstituted skimmed milk Transcriptomics Probiotic Gastrointestinal tract 



The authors would like to sincerely thank Dr. Richard J. Roberts for assistance provided with the REBASE database ( We are also extremely grateful to Shandong Longlive Bio-Technology Co., Ltd. (Shandong, China) for the provision of xylo-oligosaccharides and Glycom A/S (Lyngby, Denmark) for the provision of purified Human Milk Oligosaccharides (HMOs) samples used in this study under their donation program.


This work was financially supported by Danone Research (Paris, France) and by the Science Foundation Ireland (SFI) (Wilton Place, Dublin, Ireland), through the Irish Government’s National Development Plan (grant no. SFI/12/RC/2273) and a HRB postdoctoral fellowship (Grant No. PDTM/2011/9) awarded to MOCM. FB is a recipient of a FEMS Research Grant (FEMS-RG-2016-0103) and FEMS/ESCMID Award.

Compliance with ethical standards

Experiments with mice were approved by the University College Cork Animal Experimentation Ethics Committee and experimental procedures were conducted under license from the Irish Government (license number B100/3729).

Conflict of interest

JMF, CC, and TS are employees of Danone (Paris, France). All other authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Supplementary material

253_2018_9413_MOESM1_ESM.pdf (163 kb)
ESM 1 (PDF 163 kb)


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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Muireann Egan
    • 1
  • Francesca Bottacini
    • 1
  • Mary O’Connell Motherway
    • 1
  • Patrick G. Casey
    • 1
  • Ruth Morrissey
    • 1
  • Silvia Melgar
    • 1
  • Jean-Michel Faurie
    • 2
  • Christian Chervaux
    • 2
  • Tamara Smokvina
    • 2
  • Douwe van Sinderen
    • 1
    Email author
  1. 1.APC Microbiome Ireland and School of MicrobiologyUniversity College CorkCorkIreland
  2. 2.Danone Nutricia ResearchPalaiseauFrance

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