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

Abstract

BackgroundThe 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.ResultsThe 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.ConclusionsThis 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.Electronic supplementary materialThe online version of this article (doi:10.1186/s40168-017-0282-6) contains supplementary material, which is available to authorized users.

Exploring the role of the microbiota member Bifidobacterium in modulating immune-linked diseases

“…Current studies indicate that bifidobacteria are transmitted vertically from the mother's vagina, GI tract, or breast milk. This is supported by findings by Duranti et al [22], who used a novel internal transcribed spacer (ITS) approach trialled previously [23]. Duranti et al found genomically identical bifidobacteria strains in faecal and milk samples from 24 mother-infant pairs.…”

“…These findings provide initial insights as to why vaginal delivery provides a higher abundance of Bifidobacterium in infants, over a caesarean section (C-section) delivery [24,25]. Following birth, breast milk may provide a secondary delivery route for further bifidobacteria [22,26] and additionally drives proliferation of bifidobacteria due to its unique nutritional milieu of human milk oligosaccharides (HMOs), proteins, and lipids [27][28][29]. Notably, a reduced abundance of Bifidobacterium in infants is highly correlated to chronic diseases, including asthma and obesity [30].…”

Matrotrophic viviparity constrains microbiome acquisition during gestation in a live‐bearing cockroach, Diploptera punctata

“…For most animals, their microbial community is established over development through interactions with the environment, through diet, as well as interactions with other organisms (Abdul Rahman et al, ; Blaser & Dominguez‐Bello, ; Carrasco et al, ; da Costa & Poulsen, ; Estes et al, ; Funkhouser & Bordenstein, ; Gilbert, ; Korpela et al, ; Kostic et al, ; Morse et al, ; Mueller, Bakacs, Combellick, Grigoryan, & Dominguez‐Bello, ; Perez‐Muñoz, Arrieta, Ramer‐Tait, & Walter, ; Schwab, Riggs, Newton, & Moczek, ; Shukla, Vogel, Heckel, Vilcinskas, & Kaltenpoth, ; Torrazza & Neu, ; Wang & Rozen, ). Of interest is the role that parent–offspring interactions play in the microbial acquisition during early development, specifically from mother to her offspring (Adair & Douglas, ; Dimmitt et al, ; Duranti et al, ; Fox & Eichelberger, ; Funkhouser & Bordenstein, ; Gilbert, ; Jašarević, Rodgers, et al, ; Korpela et al, ; Kostic et al, ; Perez‐Muñoz et al, ; Schwab et al, ; Torrazza & Neu, ; Wade, ; Walker, Clemente, Peter, & Loos, ).…”

“…This forces vertical symbiont transmission to occur through incorporation during oogenesis or by inoculating the external egg surface for consumption immediately upon juvenile emergence (Abdul Rahman et al, ; Estes et al, ; Funkhouser & Bordenstein, ; Schwab et al, ; Shukla et al, ). Viviparous (live‐bearing) animals can have extensive and complex interactions between mother and offspring during gestation and birth, the impacts of which can last for a few days to years (Cao‐Lei et al, , ; Duranti et al, ; Funkhouser & Bordenstein, ; Jašarević, Rodgers, et al, ; Jiménez‐Chillarón et al, ; Ma et al, ; Ogawa & Miura, ; Poulin & Thomas, ; Stein & Lumey, ; Torrazza & Neu, ; Weiss et al, ). These prolonged interactions provide means for multiple routes of vertical transmission of microbes from mother to her progeny (Funkhouser & Bordenstein, ; Ma et al, ; Mueller et al, ).…”

“…These prolonged interactions provide means for multiple routes of vertical transmission of microbes from mother to her progeny (Funkhouser & Bordenstein, ; Ma et al, ; Mueller et al, ). In humans, while placental transmission of microbes is debated (Aagaard et al, ; Blaser & Dominguez‐Bello, ; Fardini, Chung, Dumm, Joshi, & Han, ; Perez‐Muñoz et al, ; Walker et al, ), mother to newborn transfer can occur during passage through the birth canal, breast feeding, and throughout early postnatal development (Ballard & Morrow, ; Dahlen, Downe, Kennedy, & Foureur, ; Duranti et al, ; Funkhouser & Bordenstein, ; Jašarević, Howerton, Howard, & Bale, ; Jašarević, Rodgers, et al, ; Korpela et al, ; Ma et al, ; Mueller et al, ). Other live‐bearing animals and their symbionts have evolved to utilize the extended gestation as a time to inoculate progeny with bacteria (Denlinger & Ma, ; Funkhouser & Bordenstein, ; Ma et al, ; Morse et al, ; Mueller et al, ; Wang et al, ).…”