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The First Microbial Colonizers of the Human Gut: Composition, Activities, and Health Implications of the Infant Gut Microbiota
Open accessAbstract
SUMMARY: The human gut microbiota is engaged in multiple interactions affecting host health during the host's entire life span. Microbes colonize the neonatal gut immediately following birth. The establishment and interactive development of this early gut microbiota are believed to be (at least partially) driven and modulated by specific compounds present in human milk. It has been shown that certain genomes of infant gut commensals, in particular those of bifidobacterial species, are genetically adapted to utilize specific glycans of this human secretory fluid, thus representing a very intriguing example of host-microbe coevolution, where both partners are believed to benefit. In recent years, various metagenomic studies have tried to dissect the composition and functionality of the infant gut microbiome and to explore the distribution across the different ecological niches of the infant gut biogeography of the corresponding microbial consortia, including those corresponding to bacteria and viruses, in healthy and ill subjects. Such analyses have linked certain features of the microbiota/microbiome, such as reduced diversity or aberrant composition, to intestinal illnesses in infants or disease states that are manifested at later stages of life, including asthma, inflammatory bowel disease, and metabolic disorders. Thus, a growing number of studies have reported on how the early human gut microbiota composition/development may affect risk factors related to adult health conditions. This concept has fueled the development of strategies to shape the infant microbiota composition based on various functional food products. In this review, we describe the infant microbiota, the mechanisms that drive its establishment and composition, and how microbial consortia may be molded by natural or artificial interventions. Finally, we discuss the relevance of key microbial players of the infant gut microbiota, in particular bifidobacteria, with respect to their role in health and disease.
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“The formation of intestinal microbiota during childhood is believed to be a key factor in the development of human diseases, such as allergies, neurological disorders and obesity (2–4)”
From Kefir and Intestinal Microbiota Modulation: Implications in Human Health (2021) · cites this paper as [3]
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“Dysbiosis and other determinants of intestinal microbiota formation in childhood, such as birth via cesarean section or formula feeding, are associated with a higher risk of developing obesity, both in child and adulthood (3, 68).”
From Kefir and Intestinal Microbiota Modulation: Implications in Human Health (2021) · cites this paper as [3]
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“The development of diabetes mellitus is associated with low-grade chronic inflammation.”
From Kefir and Intestinal Microbiota Modulation: Implications in Human Health (2021) · cites this paper as [3]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
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“Changes in intestinal permeability, which are favored by an imbalance in the intestinal microbiota, encourage the occurrence of this inflammation, which leads to resistance to systemic insulin, with consequent development of diabetes (3, 75).”
From Kefir and Intestinal Microbiota Modulation: Implications in Human Health (2021) · cites this paper as [3]
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“In addition, factors that affect the formation of the intestinal microbiota—such as maternal health during pregnancy, birth via cesarean section, the use of antibiotics during childhood, and the presence of intestinal dysbiosis in childhood—are also related to the development of diabetes (3).”
From Kefir and Intestinal Microbiota Modulation: Implications in Human Health (2021) · cites this paper as [3]
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“The correct formation of intestinal microbiota during childhood is fundamental for the complete development of the baby, since the intestinal microbiota is part of the immune system, being important especially in the first months of life, when the rest of the immune system is still forming.”
From Kefir and Intestinal Microbiota Modulation: Implications in Human Health (2021) · cites this paper as [3]
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“In this context, premature babies may have immaturity in the immune, respiratory and neurological systems, suggesting a possible relationship between them (3).”
From Kefir and Intestinal Microbiota Modulation: Implications in Human Health (2021) · cites this paper as [3]
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“these early life factors may still have long-lasting implications for the physical and mental health of the individual (Callaghan et al., 2019;Gensollen et al., 2016;Milani et al., 2017), consistent with the idea that there are sensitive periods for microbiota-gut-brain interactions.”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Milani et al., 2017
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“On the contrary, it is increasingly clear that they co-evolved with human hosts and the presence of microorganisms can be important for maintaining health (1–4).”
From Kefir and Intestinal Microbiota Modulation: Implications in Human Health (2021) · cites this paper as [3]
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“Children treated with antibiotics, specially macrolides, amoxicillin, cefdinir, vancomycin, and tetracyclines (69) had a higher incidence of obesity (3), since antibiotics can alter the composition of the intestinal microbiota, leading to a dysbiotic state (3, 70).”
From Kefir and Intestinal Microbiota Modulation: Implications in Human Health (2021) · cites this paper as [3]
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“In addition, individuals with autism have a characteristic intestinal microbiota, which strengthens the relationship between intestinal microbiota and neurological disorders (1–4).”
From Kefir and Intestinal Microbiota Modulation: Implications in Human Health (2021) · cites this paper as [3]
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“breast-fed infants have consistently greater levels of bifidobacteria and an overall lower diversity compared to formula-fed infants (Milani et al., 2017).”
From Viral Infections, the Microbiome, and Probiotics (2021) · cites this paper as Milani et al., 2017
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1 retracted
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- Tissier H . 1900. Recherches sur la flore intestinale normale et pathologique du nourisson. Thesis. University of Paris, Paris, France.
Cited by
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Human gut microbiome: Hopes, threats and promises
Cani, P. D. (2018) · Gut · doi:10.1136/gutjnl-2018-316723 · Cited by 1,386
Inflammatory bowel diseases (IBD) and the microbiome-searching the crime scene for clues
Lee, M., & Chang, E. B. (2021) · Gastroenterology · doi:10.1053/j.gastro.2020.09.056 · Cited by 645
Emerging issues in probiotic safety: 2023 perspectives
Merenstein, D., Pot, B., Leyer, G., Ouwehand, A. C., Preidis, G. A., Elkins, C. A., Hill, C., Lewis, Z. T., Shane, A. L., Zmora, N., et al. (2023) · Gut Microbes · doi:10.1080/19490976.2023.2185034 · Cited by 481
Bifidobacterium adolescentis as a key member of the human gut microbiota in the production of GABA
Duranti, S., Ruiz, L., Lugli, G. A., Tames, H., Milani, C., Mancabelli, L., Mancino, W., Longhi, G., Carnevali, L., Sgoifo, A., et al. (2020) · Scientific Reports · doi:10.1038/s41598-020-70986-z · Cited by 341
Self-citation
Metadata
- Authors
- Milani, C., Duranti, S., Bottacini, F., Casey, E., Turroni, F., Mahony, J., Belzer, C., Delgado Palacio, S., Arboleya Montes, S., Mancabelli, L., Lugli, G. A., Rodriguez, J. M., Bode, L., de Vos, W., Gueimonde, M., Margolles, A., van Sinderen, D., & Ventura, M.
- Affiliations
- University of Parma (IT)
- National University of Ireland (IE)
- Wageningen University & Research (NL)
- Departamento de Microbiologia y Bioquimica de Productos Lacteos, IPLA-CSIC, Villaviciosa, Asturias, Spain
- Department of Nutrition, Food Science and Food Technology, Complutense University of Madrid, Madrid, Spain
- University of California San Diego (US)
- Laboratory of Microbiology, Wageningen University, Wageningen, The Netherlands
- Consejo Superior de Investigaciones Científicas (ES)
- APC Microbiome Institute and School of Microbiology, National University of Ireland, Cork, Ireland
- ORCID
- Venue
- Microbiology and Molecular Biology Reviews
- Publisher
- American Society for Microbiology
- Published
- 2017-12
- Volume
- 81
- Issue
- 4
- ISSN
- 1092-2172 (ISSN-L)
- 1098-5557
- PMC
- PMC5706746
- OpenAlex
- W2767360135
- Semantic Scholar
- 632e13fa6d1709c03f031492eea621c2167514f5
- Cited by
- 1,950
- References
- 552
- Citations by year
- 2026: 165 · 2025: 247 · 2024: 285 · 2023: 268 · 2022: 288 · 2021: 290 · 2020: 246 · 2019: 107 · 2018: 47 · 2017: 4
- FWCI
- 10.41
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Microbiology and Molecular Biology Reviews (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Socio-Environmental Systems Modeling (acceptedVersion)
- Arrow@dit (Dublin Institute of Technology) (submittedVersion)
- Cork Open Research Archive (University College Cork, Ireland) (submittedVersion)
- DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Funders
- Science Foundation Ireland (SFI/12/RC/2273, 15/SIRG/3430)
- Ministero dell'Istruzione, dell'Università e della Ricerca
- Ministerio de Economía y Competitividad (PCIN-2015-233, AGL2016-75476-R)
- Danone
- EU Joint Programming Initiative “A Healthy Diet for a Healthy Life”
- Spanish Plan Estatal de I+D+I (AGL2016-78311-R)
- 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 › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Keywords
- infant gut microbiota, neonatal gut colonization, breast milk, Bifidobacterium, host-microbe coevolution, asthma, inflammatory bowel disease, metabolic disorders, functional foods, microbiota modulation
- MeSH terms
- Infant Health, Gastrointestinal Microbiome, Whole Genome Sequencing, Breast Feeding, Female, Humans, Immune System, Infant, Intestinal Diseases, Maternal-Fetal Exchange, Milk, Human, Pregnancy, Symbiosis, Biomarkers, Probiotics, Gastrointestinal Tract
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