Mother-to-Infant Transmission of Intestinal Bifidobacterial Strains Has an Impact on the Early Development of Vaginally Delivered Infant's Microbiota

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Abstract

Objectives

Bifidobacterium species are one of the major components of the infant's intestine microbiota. Colonization with bifidobacteria in early infancy is suggested to be important for health in later life. However, information remains limited regarding the source of these microbes. Here, we investigated whether specific strains of bifidobacteria in the maternal intestinal flora are transmitted to their infant's intestine.

Materials and Methods

Fecal samples were collected from healthy 17 mother and infant pairs (Vaginal delivery: 12; Cesarean section delivery: 5). Mother's feces were collected twice before delivery. Infant's feces were collected at 0 (meconium), 3, 7, 30, 90 days after birth. Bifidobacteria isolated from feces were genotyped by multilocus sequencing typing, and the transitions of bifidobacteria counts in infant's feces were analyzed by quantitative real-time PCR.

Results

Stains belonging to Bifidobacterium adolescentis, Bifidobacterium bifidum, Bifidobacterium catenulatum, Bifidobacterium longum subsp. longum, and Bifidobacterium pseudocatenulatum, were identified to be monophyletic between mother's and infant's intestine. Eleven out of 12 vaginal delivered infants carried at least one monophyletic strain. The bifidobacterial counts of the species to which the monophyletic strains belong, increased predominantly in the infant's intestine within 3 days after birth. Among infants delivered by C-section, monophyletic strains were not observed. Moreover, the bifidobacterial counts were significantly lower than the vaginal delivered infants until 7 days of age.

Conclusions

Among infants born vaginally, several Bifidobacterium strains transmit from the mother and colonize the infant's intestine shortly after birth. Our data suggest that the mother's intestine is an important source for the vaginal delivered infant's intestinal microbiota.

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Most cited references 35

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The genome sequence of Bifidobacterium longum subsp. infantis reveals adaptations for milk utilization within the infant microbiome.

D. A. Sela, J. Chapman, A Adeuya … (2008)

Following birth, the breast-fed infant gastrointestinal tract is rapidly colonized by a microbial consortium often dominated by bifidobacteria. Accordingly, the complete genome sequence of Bifidobacterium longum subsp. infantis ATCC15697 reflects a competitive nutrient-utilization strategy targeting milk-borne molecules which lack a nutritive value to the neonate. Several chromosomal loci reflect potential adaptation to the infant host including a 43 kbp cluster encoding catabolic genes, extracellular solute binding proteins and permeases predicted to be active on milk oligosaccharides. An examination of in vivo metabolism has detected the hallmarks of milk oligosaccharide utilization via the central fermentative pathway using metabolomic and proteomic approaches. Finally, conservation of gene clusters in multiple isolates corroborates the genomic mechanism underlying milk utilization for this infant-associated phylotype.

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Human milk glycobiome and its impact on the infant gastrointestinal microbiota.

Angela M. Zivkovic, J German, Carlito Lebrilla … (2011)

Human milk contains an unexpected abundance and diversity of complex oligosaccharides apparently indigestible by the developing infant and instead targeted to its cognate gastrointestinal microbiota. Recent advances in mass spectrometry-based tools have provided a view of the oligosaccharide structures produced in milk across stages of lactation and among human mothers. One postulated function for these oligosaccharides is to enrich a specific "healthy" microbiota containing bifidobacteria, a genus commonly observed in the feces of breast-fed infants. Isolated culture studies indeed show selective growth of infant-borne bifidobacteria on milk oligosaccharides or core components therein. Parallel glycoprofiling documented that numerous Bifidobacterium longum subsp. infantis strains preferentially consume small mass oligosaccharides that are abundant early in the lactation cycle. Genome sequencing of numerous B. longum subsp. infantis strains shows a bias toward genes required to use mammalian-derived carbohydrates by comparison with adult-borne bifidobacteria. This intriguing strategy of mammalian lactation to selectively nourish genetically compatible bacteria in infants with a complex array of free oligosaccharides serves as a model of how to influence the human supraorganismal system, which includes the gastrointestinal microbiota.

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Small subunit rRNA sequence data were generated for 27 strains of cyanobacteria and incorporated into a phylogenetic analysis of 1,377 aligned sequence positions from a diverse sampling of 53 cyanobacteria and 10 photosynthetic plastids. Tree inference was carried out using a maximum likelihood method with correction for site-to-site variation in evolutionary rate. Confidence in the inferred phylogenetic relationships was determined by construction of a majority-rule consensus tree based on alternative topologies not considered to be statistically significantly different from the optimal tree. The results are in agreement with earlier studies in the assignment of individual taxa to specific sequence groups. Several relationships not previously noted among sequence groups are indicated, whereas other relationships previously supported are contradicted. All plastids cluster as a strongly supported monophyletic group arising near the root of the cyanobacterial line of descent.

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Author and article information

Contributors

Yolanda Sanz: Role: Editor

Journal

Journal ID (nlm-ta): PLoS One

Journal ID (iso-abbrev): PLoS ONE

Journal ID (publisher-id): plos

Journal ID (pmc): plosone

Title: PLoS ONE

Publisher: Public Library of Science (San Francisco, USA )

ISSN (Electronic): 1932-6203

Publication date Collection: 2013

Publication date (Electronic): 14 November 2013

Volume: 8

Issue: 11

Electronic Location Identifier: e78331

Affiliations

[1 ]Yakult Central Institute for Microbiological Research, Tokyo, Japan

[2 ]Yakult Honsha European Research Center for Microbiology, ESV, Gent-Zwijnaarde, Belgium

[3 ]Danone Research, Centre for Specialised Nutrition, Utrecht, The Netherlands

[4 ]Danone Research, Centre for Specialised Nutrition, Singapore

[5 ]Laboratory of Microbiology, Wageningen University, Wageningen, The Netherlands

Instutite of Agrochemistry and Food Technology, Spain

Author notes

* E-mail: hiroshi-makino@ 123456yakult.co.jp

Competing Interests: The authors have declared that no competing interests exist.

Conceived and designed the experiments: HM AK EI KO RM KBA JK RT. Performed the experiments: HM AK EI HK AG. Analyzed the data: HM EI HK. Contributed reagents/materials/analysis tools: HM AK EI HK AG TS KO. Wrote the paper: HM AK EI HK AG TS KO RM KBA JK RT.

Article

Publisher ID: PONE-D-13-19228

DOI: 10.1371/journal.pone.0078331

PMC ID: 3828338

PubMed ID: 24244304

SO-VID: 9d678f23-97a3-4151-8258-6e14c9ca8621

License:

This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

History

Date received : 9 May 2013

Date accepted : 11 September 2013

Page count

Pages: 10

Funding

This work was supported by Yakult Honsha European Research Center for Microbiology ESV and Danone Research (Centre for Specialised Nutrition, Wageningen, Netherlands, and Centre Daniel Carasso, Palaiseau, France). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Mother-to-Infant Transmission of Intestinal Bifidobacterial Strains Has an Impact on the Early Development of Vaginally Delivered Infant's Microbiota

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Abstract

Objectives

Materials and Methods

Results

Conclusions

Related collections

PLOS Climate

Most cited references 35

The genome sequence of Bifidobacterium longum subsp. infantis reveals adaptations for milk utilization within the infant microbiome.

Human milk glycobiome and its impact on the infant gastrointestinal microbiota.

Investigating deep phylogenetic relationships among cyanobacteria and plastids by small subunit rRNA sequence analysis.

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