First food and gut microbes

Key message

The infant gut microbiota development is influenced by type of milk feeding and the
composition of the complementary diet, with protein and dietary fiber intake coupled
to development of increased diversity in the maturing gut microbiota of well-nourished
infants. Pioneering studies with stunted malnourished children suggest that microbiota directed complementary foods ensures adequate maturation of the gut microbiota and may improve growth and development.

Abstract

Increasing evidence suggest that the establishment and succession of the gut microbiota in early life influences current and future health. During the first few years of
life the microbial consortium within our gut develops in composition and diversity, a process that is influenced by a multitude of internal and external factors[1–4]. Among these, type of milk feeding and the complementary diet are strong determinants that defines the establishment and temporal progression of our gut microbial cosystem[1,2,5]. While breastfeeding strongly selects for a simple and rather stable community, dominated by human milk oligosaccharide degrading Bifidobacterium spp.[6], formula feeding results in a more diverse and unstable community often ominated by Enterobacteriaceae, Clostridiaceae and/or Bacteroidaceae spp.[4,7]. The introduction of solid foods and progression in complementary foods represent steps towards maturation and diversification of the gut microbiota, with expansion in prevalence and abundance of species within the Ruminococcaceae,
Bacteroidaceae and Lachnospiraceae families[8]. Although our knowledge on how specific components of the complementary diet impact the gut microbiota still remains limited, progression towards eating family like foods, with increased intake of protein
and dietary fiber seem to contribute the natural diversification of the gut microbiota[5,8]. Here, the gradual substitution of breast and/or formula milk, especially with meat and cheese products and (rye)breads appears to be the major contributors at least in
well-nourished infants of the western-societies[5,9]. Introduction of these complementary food components likely represent an incentive for more protein fermenting and fiber degrading bacteria to establish in the gut. While we remain to understand the health-related implications of different early life gut microbiota
trajectories, recent studies in undernourished stunted children are suggesting an important link between complementary feeding and gut microbiota maturation. So called microbiota directed complementary foods (rich in fiber and protein) has been rationally designed to induce adequate maturation of the gut microbiota in stunted malnourished Bangladeshi children[10,11]. These complementary foods, designed by taking basis in
locally available foods that are also rich in fibers and protein, induced the change from an immature, prolonged milk-adapted Bifidobacterium rich gut microbiota towards a more mature one characterized by various Lachnospiraceae, Ruminococcaceae
and Bacteroidaceae species. These changes also correlated with plasma markers of linear growth, bone development, neurodevelopment and immune function in both various animal models, but also in a short-term clinical study[11]. Such results suggest that complementary foods through their action on the gut microbiota can improve growth and development of undernourished children. However, in general, our
knowledge in this field still remain very limited and there is a need to further study these exciting links between complementary feeding, gut microbiota trajectories and host physiology and development in early life.

References
1. Stewart CJ, Ajami NJ, O’Brien JL, Hutchinson DS, Smith DP, Wong MC, et al.
Temporal development of the gut microbiome in early childhood from the
TEDDY study. Nature. Nature Publishing Group; 2018;562:583–8.
2. Galazzo G, van Best N, Bervoets L, Dapaah IO, Savelkoul PH, Hornef MW, et al.
Development of the Microbiota and Associations With Birth Mode, Diet, and
Atopic Disorders in a Longitudinal Analysis of Stool Samples, Collected From
Infancy Through Early Childhood. Gastroenterology. Elsevier BV; 2020;
3. Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, et al. Human gut microbiome viewed across age and geography. Nature. 2012;486:222–7.
4. Penders J, Thijs C, Vink C, Stelma FF, Snijders B, Kummeling I, et al. Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics. 2006;118:511–21.
5. Laursen MF, Andersen LBB, Michaelsen KF, Mølgaard C, Trolle E, Bahl MI, et al. Infant Gut Microbiota Development Is Driven by Transition to Family Foods Independent of Maternal Obesity. mSphere. American Society for Microbiology Journals; 2016;1:e00069-15.
6. Laursen MF, Sakanaka M, Burg N Von, Andersen D, Mörbe U, von Burg N, et al.
Breastmilk-promoted bifidobacteria produce aromatic lactic acids in the infant gut. bioRxiv. Cold Spring Harbor Laboratory; 2020;2020.01.22.914994.
7. Bäckhed F, Roswall J, Peng Y, Feng Q, Jia H, Kovatcheva-Datchary P, et al. Dynamics and Stabilization of the Human Gut Microbiome during the First Year of Life. Cell Host Microbe. 2015;17:690–703.
8. Laursen MF, Bahl MI, Michaelsen KF, Licht TR. First foods and gut microbes. Front Microbiol. 2017;8:1–8.
9. Leong C, Haszard JJ, Lawley B, Otal A, Taylor RW, Szymlek-Gay EA, et al. ediation analysis as a means of identifying dietary components that differentially affect the
fecal microbiota of infants weaned by modified baby-led and traditional approaches. Appl Environ Microbiol. American Society for Microbiology; 2018;84.
10. Raman AS, Gehrig JL, Venkatesh S, Chang HW, Hibberd MC, Subramanian S, et al. A sparse covarying unit that describes healthy and impaired human gut microbiota development. Science (80- ). American Association for the Advancement of Science; 2019;365.
11. Gehrig JL, Venkatesh S, Chang HW, Hibberd MC, Kung VL, Cheng J, et al. Effects
of microbiota-directed foods in gnotobiotic animals and undernourished children.
Science (80- ). American Association for the Advancement of Science; 2019;365.