A holobiont birth narrative: the epigenetic transmission of the human microbiome

Gilbert, Scott F.

doi:10.3389/fgene.2014.00282

Cited by 127 publications

(77 citation statements)

References 82 publications

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“…Transmission of bacteria is even suggested to represent a form of epigenetic inheritance (Gilbert 2014). The infant's immune system develops in tight interaction with the intestinal microbiome, which guides its maturation and may significantly influence the risk of immune-related diseases (Houghteling and Walker 2015).…”

Section: [Supplemental Materials Is Available For This Article]mentioning

confidence: 99%

Selective maternal seeding and environment shape the human gut microbiome

et al. 2018

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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.

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Section: [Supplemental Materials Is Available For This Article]mentioning

confidence: 99%

Selective maternal seeding and environment shape the human gut microbiome

et al. 2018

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“…First, the provision of nutrients such as host-derived glycans contributes to the microbial community structure and is a source of microbederived metabolites such as short-chained fatty acids (SCFA) that promote the maturation of local and systemic immune functions (6)(7)(8)(9). Second, the nutritional and environmental changes that mark the developmental trajectory of an organism from its juvenile to adult form are accompanied by distinct shifts in both the composition and functions of the maturing host's microbiota (10,11).…”

mentioning

confidence: 99%

The chemistry of negotiation: Rhythmic, glycan-driven acidification in a symbiotic conversation

Schwartzman

Koch

Heath‐Heckman

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

113

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Glycans have emerged as critical determinants of immune maturation, microbial nutrition, and host health in diverse symbioses. In this study, we asked how cyclic delivery of a single host-derived glycan contributes to the dynamic stability of the mutualism between the squid Euprymna scolopes and its specific, bioluminescent symbiont, Vibrio fischeri. V. fischeri colonizes the crypts of a host organ that is used for behavioral light production. E. scolopes synthesizes the polymeric glycan chitin in macrophage-like immune cells called hemocytes. We show here that, just before dusk, hemocytes migrate from the vasculature into the symbiotic crypts, where they lyse and release particulate chitin, a behavior that is established only in the mature symbiosis. Diel transcriptional rhythms in both partners further indicate that the chitin is provided and metabolized only at night. A V. fischeri mutant defective in chitin catabolism was able to maintain a normal symbiont population level, but only until the symbiotic organ reached maturity (∼4 wk after colonization); this result provided a direct link between chitin utilization and symbiont persistence. Finally, catabolism of chitin by the symbionts was also specifically required for a periodic acidification of the adult crypts each night. This acidification, which increases the level of oxygen available to the symbionts, enhances their capacity to produce bioluminescence at night. We propose that other animal hosts may similarly regulate the activities of epithelium-associated microbial communities through the strategic provision of specific nutrients, whose catabolism modulates conditions like pH or anoxia in their symbionts' habitat.symbiosis | squid-vibrio | metabolism | chitin

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“…For this, it is important to note that maternal transmission of microbes to the offspring's microbiota has been demonstrated repeatedly (Funkhouser and Bordenstein 2013;Gilbert 2014;Moon et al 2015).…”

Section: Microorganisms As Part Of the Epigenetic Toolkitmentioning

confidence: 98%

“…Thereby, the host-associated microbiome interacts with the host genome and thus acts as an epigenetic modifier that can be transmitted intergenerationally and will therefore not only influence individuals on short time scales but also evolution of the host species in the long run (Gilbert et al 2010;Fitzpatrick 2014;Gilbert 2014).…”

Section: Microorganisms As Part Of the Epigenetic Toolkitmentioning

confidence: 99%

The brain’s Geppetto—microbes as puppeteers of neural function and behaviour?

2015

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Research on the microbiome and its interaction with various host organs, including the brain, is increasingly gaining momentum. With more evidence establishing a comprehensive microbiota-gut-brain axis, questions have been raised as to the extent to which microbes influence brain physiology and behaviour. In parallel, there is a growing literature showing active behavioural manipulation in favour of the microbe for certain parasites. However, it seems unclear where the hidden majority of microbes are localised on the parasitism-mutualism spectrum. A long evolutionary history intimately connects host and microbiota, which complicates this classification. In this conceptual minireview, we discuss current hypotheses on host-microbe interaction and argue that novel experimental approaches and theoretical concepts, such as the hologenome theory, are necessary to incorporate transgenerational epigenetic inheritance of the microbiome into evolutionary theories.

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A holobiont birth narrative: the epigenetic transmission of the human microbiome

Cited by 127 publications

References 82 publications

Selective maternal seeding and environment shape the human gut microbiome

Selective maternal seeding and environment shape the human gut microbiome

The chemistry of negotiation: Rhythmic, glycan-driven acidification in a symbiotic conversation

The brain’s Geppetto—microbes as puppeteers of neural function and behaviour?

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