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Cited by 328Gut microbiota and healthInfant Nutrition and HealthBacteriophages and microbial interactions

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Maternal inheritance of bifidobacterial communities and bifidophages in infants through vertical transmission

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Duranti, Sabrina, Lugli, Gabriele Andrea, Mancabelli, Leonardo, Armanini, Federica, Turroni, Francesca, James, Kieran, Ferretti, Pamela, Gorfer, Valentina, Ferrario, Chiara, Milani, Christian, Mangifesta, Marta, Anzalone, Rosaria, Zolfo, Moreno, Viappiani, Alice, Pasolli, Edoardo, Bariletti, Ilaria, Canto, Rosarita, Clementi, Rosanna, Cologna, Marina, Crifò, Tiziana, Cusumano, Giuseppina, Fedi, Sabina, Gottardi, Stefania, Innamorati, Claudia, Masè, Caterina, Postai, Daniela, Savoi, Daniela, Soffiati, Massimo, Tateo, Saverio, Pedrotti, Anna, Segata, Nicola, van Sinderen, Douwe, Ventura, Marco·2017·Microbiome
DOI 10.1186/s40168-017-0282-6PMC PMC5485682
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Abstract

BACKGROUND: The correct establishment of the human gut microbiota represents a crucial development that commences at birth. Different hypotheses propose that the infant gut microbiota is derived from, among other sources, the mother's fecal/vaginal microbiota and human milk. RESULTS: The composition of bifidobacterial communities of 25 mother-infant pairs was investigated based on an internal transcribed spacer (ITS) approach, combined with cultivation-mediated and genomic analyses. We identified bifidobacterial strains/communities that are shared between mothers and their corresponding newborns. Notably, genomic analyses together with growth profiling assays revealed that bifidobacterial strains that had been isolated from human milk are genetically adapted to utilize human milk glycans. In addition, we identified particular bacteriophages specific of bifidobacterial species that are common in the viromes of mother and corresponding child. CONCLUSIONS: This study highlights the transmission of bifidobacterial communities from the mother to her child and implies human milk as a potential vehicle to facilitate this acquisition. Furthermore, these data represent the first example of maternal inheritance of bifidobacterial phages, also known as bifidophages in infants following a vertical transmission route.

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Crossref · 10.1186/s40168-017-0282-6

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Figures

Fig. 1 Profiling of the bifidobacterial communities of infant fecal samples. The heat map representation shows the relative abundance of Bifidobacterium species. On the bottom of the image, the bar plots show qPCR data regarding the proportion (in %) of bifidobacteria relative to other bacteria present in a given sample
Fig. 1 Profiling of the bifidobacterial communities of infant fecal samples. The heat map representation shows the relative abundance of Bifidobacterium species. On the bottom of the image, the bar plots show qPCR data regarding the proportion (in %) of bifidobacteria relative to other bacteria present in a given sampleCC BY · PubMed Central
Fig. 2 Profiling of the bifidobacterial communities of each CoupleID. The heat map represents the relative abundance of bifidobacterial species that were determined to be present in each sample. On the left side, all known and putative novel bifidobacterial species are reported. Sample origin and CoupleID codes are reported on the top side of the heat map
Fig. 2 Profiling of the bifidobacterial communities of each CoupleID. The heat map represents the relative abundance of bifidobacterial species that were determined to be present in each sample. On the left side, all known and putative novel bifidobacterial species are reported. Sample origin and CoupleID codes are reported on the top side of the heat mapCC BY · PubMed Central
Fig. 3 Evaluation of persistence of putative vertically transmitted strains in fecal samples of the infants and mothers as well as in milk samples by PCR assays. Marker lane is the Thermo Scientific GeneRuler 1 kb DNA Ladder. The reference strains used as positive controls for each CoupleID respectively are B. longum 1886B, B. bifidum 1887B, B. breve 1900B, B. adolescentis 1892B, B. longum 1898B, B. longum 1897B, B. dentium 1893B, B. longum subsp. infantis 1888B, B. catenulatum 1899B, B. breve 1891B, B. breve 1895B, B. pseudocatenulatum 1896B, and B. breve 1889B. Primer sequences are reported in Additional file 1: Table S3
Fig. 3 Evaluation of persistence of putative vertically transmitted strains in fecal samples of the infants and mothers as well as in milk samples by PCR assays. Marker lane is the Thermo Scientific GeneRuler 1 kb DNA Ladder. The reference strains used as positive controls for each CoupleID respectively are B. longum 1886B, B. bifidum 1887B, B. breve 1900B, B. adolescentis 1892B, B. longum 1898B, B. longum 1897B, B. dentium 1893B, B. longum subsp. infantis 1888B, B. catenulatum 1899B, B. breve 1891B, B. breve 1895B, B. pseudocatenulatum 1896B, and B. breve 1889B. Primer sequences are reported in Additional file 1: Table S3CC BY · PubMed Central
Fig. 4 Human milk oligosaccharide degradation capabilities of vertically transmitted bifidobacterial strains. a Heat map representation of the presence/absence of genes encoding enzymes for degradation of milk oligosaccharides and transporters for uptake of the released compounds. Red and black squares represent the presence and absence of genes, respectively. b Growth profile on HMO-derived carbohydrates. Black color indicates that the final OD600 nm is <0.3, yellow indicates the range of final OD600 nm from 0.3 to 0.5, light green indicates the range between >0.5 and 0.8, and green indicates the final OD600 nm >0.8
Fig. 4 Human milk oligosaccharide degradation capabilities of vertically transmitted bifidobacterial strains. a Heat map representation of the presence/absence of genes encoding enzymes for degradation of milk oligosaccharides and transporters for uptake of the released compounds. Red and black squares represent the presence and absence of genes, respectively. b Growth profile on HMO-derived carbohydrates. Black color indicates that the final OD600 nm is <0.3, yellow indicates the range of final OD600 nm from 0.3 to 0.5, light green indicates the range between >0.5 and 0.8, and green indicates the final OD600 nm >0.8CC BY · PubMed Central
Fig. 5 Vertically transmitted bifidophages from mothers to newborns. Indicated at the top of the figure are the genomic maps of the identified B. longum phage 10029 and 10035. The modular genomic structure is indicated by different patterns, which specifies their predicted function (violet, lysogeny module; blue, DNA replication; red, DNA packaging and head; green, tail and tail fiber; yellow, lysis module; black arrows, hypothetical protein; grey arrows, similar to bacterial protein). On the bottom are reported the presence of the phage within the mother’s and infant’s metagenomic samples through PCR analysis. Primer sequences are reported in Additional file 1: Table S5
Fig. 5 Vertically transmitted bifidophages from mothers to newborns. Indicated at the top of the figure are the genomic maps of the identified B. longum phage 10029 and 10035. The modular genomic structure is indicated by different patterns, which specifies their predicted function (violet, lysogeny module; blue, DNA replication; red, DNA packaging and head; green, tail and tail fiber; yellow, lysis module; black arrows, hypothetical protein; grey arrows, similar to bacterial protein). On the bottom are reported the presence of the phage within the mother’s and infant’s metagenomic samples through PCR analysis. Primer sequences are reported in Additional file 1: Table S5CC BY · PubMed Central

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Authors
Duranti, S., Lugli, G. A., Mancabelli, L., Armanini, F., Turroni, F., James, K., Ferretti, P., Gorfer, V., Ferrario, C., Milani, C., Mangifesta, M., Anzalone, R., Zolfo, M., Viappiani, A., Pasolli, E., Bariletti, I., Canto, R., Clementi, R., Cologna, M., Crifò, T., Cusumano, G., Fedi, S., Gottardi, S., Innamorati, C., Masè, C., Postai, D., Savoi, D., Soffiati, M., Tateo, S., Pedrotti, A., Segata, N., van Sinderen, D., & Ventura, M.
Affiliations
  • University of Parma (IT)
  • University of Trento (IT)
  • National University of Ireland (IE)
  • Provincia Autonoma di Trento (IT)
Corresponding author
Ventura, Marco
ORCID
Venue
Microbiome
Publisher
Springer Science and Business Media LLC
Published
2017-06-26
Volume
5
Issue
1
Pages
66-66
ISSN
2049-2618 (ISSN-L)
DOI
10.1186/s40168-017-0282-6
PMC
PMC5485682
OpenAlex
W2717530497
Cited by
327
References
65
Citations by year
2026: 21 · 2025: 40 · 2024: 31 · 2023: 33 · 2022: 41 · 2021: 62 · 2020: 37 · 2019: 28 · 2018: 26 · 2017: 8
FWCI
11.16
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Microbiome (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Institutional Research Information System (Università degli Studi di Trento) (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • Fondazione Caritro, Trento, Italy
  • EU Joint Programming Initiative – A Healthy Diet for a Healthy Life
  • Ministero dell’Istruzione, dell’Università e della Ricerca
  • Fondazione Cariparma
  • Science Foundation Ireland (SFI/12/RC/2273)
  • GenProbio srl
  • EU Joint Programming Initiative - A Healthy Diet for a Healthy Life
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
  • Health Sciences › Nursing › Nutrition and Dietetics › Infant Nutrition and Health
  • Life Sciences › Immunology and Microbiology › Virology › Bacteriophages and microbial interactions
Keywords
maternal inheritance, vertical transmission, Bifidobacterium, infant gut microbiota, breast milk, mother-infant dyads
MeSH terms
Gastrointestinal Microbiome, Bacteriophages, Bifidobacterium, Breast Feeding, Feces, Humans, Infant, Infant, Newborn, Milk, Human, Mothers, Polysaccharides, Sequence Analysis, DNA

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