Selective maternal seeding and environment shape the human gut microbiome

Abstract

Vertical transmission of bacteria from mother to infant at birth is postulated to initiate a life-long host-microbe symbiosis, playing an important role in early infant development. However, only the tracking of strictly defined unique microbial strains can clarify where the intestinal bacteria come from, how long the initial colonizers persist, and whether colonization by other strains from the environment can replace existing ones. Using rare single nucleotide variants in fecal metagenomes of infants and their family members, we show strong evidence of selective and persistent transmission of maternal strain populations to the vaginally born infant and their occasional replacement by strains from the environment, including those from family members, in later childhood. Only strains from the classes Actinobacteria and Bacteroidia, which are essential components of the infant microbiome, are transmitted from the mother and persist for at least 1 yr. In contrast, maternal strains of Clostridia, a dominant class in the mother's gut microbiome, are not observed in the infant. Caesarean-born infants show a striking lack of maternal transmission at birth. After the first year, strain influx from the family environment occurs and continues even in adulthood. Fathers appear to be more frequently donors of novel strains to other family members than receivers. Thus, the infant gut is seeded by selected maternal bacteria, which expand to form a stable community, with a rare but stable continuing strain influx over time.

Faecal microbiota and functional capacity associated with weaning weight in meat rabbits

“…Earlier studies indicated that the cage rearing effect may be caused by differences in early life gut microbial colonization process, including exposure to the maternal microbiome (e.g. breast-milk feeding and ingest the soft faeces of dams) and indigenous environment microbiome (Hufeldt, et al, 2010;Rogers, et al, 2014;Ericsson, et al, 2015;Yang, et al, 2017;Korpela, et al, 2018;Martinez, et al, 2018). Previous studies investigated the role of sex in adult animals' gut microbiota suggested that the significant difference of gut microbial composition between sexes was caused by sex hormones (Org, et al, 2016;Miyoshi, et al, 2018).…”

Developmental responses to early‐life adversity: Evolutionary and mechanistic perspectives

“…Although we are unaware of any research suggesting that infants can counteract these measures, competitive exclusion (i.e., microbial competition for available niches and resources) can, in theory, also be driven by offspring gut motility and the biochemical makeup of the mucosal lining of the offspring gut . Further, offspring intestinal immune responses to maternal microbes can result in the selective seeding of certain maternal microbial strains over others . Thus, despite the magnitude of maternal microbiota and oligosaccharide transmission, offspring physiology ultimately shapes the maternal microbes that successfully colonize and proliferate within the infant gut.…”

“…153,154 Further, offspring intestinal immune responses to maternal microbes can result in the selective seeding of certain maternal microbial strains over others. 155,156 Thus, despite the magnitude of maternal microbiota and oligosaccharide transmission, offspring physiology ultimately shapes the maternal microbes that successfully colonize and proliferate within the infant gut. Whether microbial strains might have similar mechanisms to counter offspring or maternal interests is fodder for future studies.…”

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

“…These microbes have important roles in a variety of processes benefiting their host, ranging from nutrient metabolism to immunity (Albenberg & Wu, ; Chung et al, ; Dimmitt et al, ; Douglas, ; Jašarević, Rodgers, & Bale, ; Michalkova, Benoit, Weiss, Attardo, & Aksoy, ; Pais, Lohs, Wu, Wang, & Aksoy, ; Snyder & Rio, ; Wang, Weiss, & Aksoy, ; Weiss, Wang, & Aksoy, ). 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, ).…”

“…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, ).…”