You're using an outdated browser. Please upgrade to a modern browser for the best experience.
Submitted Successfully!
Thank you for your contribution! You can also upload a video entry or images related to this topic. For video creation, please contact our Academic Video Service.
Version Summary Created by Modification Content Size Created at Operation
1
Michiel Van de Vliet
 -- 1176 2022-09-26 15:48:06 |
2 format correction
Dean Liu
 -2 word(s) 1174 2022-09-28 04:18:54 |

Video Upload Options

We provide professional Academic Video Service to translate complex research into visually appealing presentations. Would you like to try it?
No, upload directly Yes

Confirm

Are you sure to Delete?
Yes No
Cite
If you have any further questions, please contact Encyclopedia Editorial Office.
Vliet, M.V.D.;  Joossens, M. Human Bacterial Gut Colonization. Encyclopedia. Available online: https://encyclopedia.pub/entry/27601 (accessed on 14 July 2025).
Vliet MVD,  Joossens M. Human Bacterial Gut Colonization. Encyclopedia. Available at: https://encyclopedia.pub/entry/27601. Accessed July 14, 2025.
Vliet, Michiel Van De, Marie Joossens. "Human Bacterial Gut Colonization" Encyclopedia, https://encyclopedia.pub/entry/27601 (accessed July 14, 2025).
Vliet, M.V.D., & Joossens, M. (2022, September 26). Human Bacterial Gut Colonization. In Encyclopedia. https://encyclopedia.pub/entry/27601
Vliet, Michiel Van De and Marie Joossens. "Human Bacterial Gut Colonization." Encyclopedia. Web. 26 September, 2022.
Human Bacterial Gut Colonization
Edit
This entry is adapted from the peer-reviewed paper 10.3390/microorganisms10091831

Thorough understanding of the initial colonization process of human intestines is important to optimize the prevention of microbiota-associated diseases, and also to further improve the current microbial therapies. In recent years, therefore, colonization of the human gut has gained renewed interest.

gut microbiota intestinal colonization human

1. Introduction

The human gut community is a complex, dynamic microbial network comprising of bacteria, yeast, and viruses. Due to its relevance to the host’s health and the multiple physiological functions it performs, it is sometimes referred to as the hidden organ of the body. The intestinal microbiota assists in digestion of insoluble fibers, thereby providing nutrients (short-chain fatty acids, SCFAs) for the colonic epithelial cells [1]. Besides its digestive function, it also protects the host from pathogens by occupying the available niches (space and nutrients) and plays a crucial role in the development of the host’s immune system [2][3]. The latter function is thought to be heavily impacted by the developing gut microbiota during the first years of life. The adult human colon is densely populated by bacteria with estimated numbers being as high as 1014 bacterial cells per gram in the luminal content [1]. The massive colonization of the intestines is assumed to start gradually from birth onwards until the dynamically more stable adult state is reached. Interestingly, disruptions in this colonization process have been shown to coincide with increased incidences of allergic diseases during childhood [4][5].
Regardless of the continuing research, the knowledge on intestinal colonization in humans is far from complete. Major knowledge gaps appear to result from the lack of datapoints per infant, which necessitates deduction-based conclusions and hampers in-depth insight in succession and colonization of specific bacteria in the intestinal microbial network. As dense sampling and high-quality collection of fecal samples of newborns is not straightforward for humans and key factors affecting the microbiota development (major dietary and environmental changes) are not standardized, resesarchers here summarize the colonization of the porcine gut, in comparison with what is known in infants. After all, anatomically and physiologically speaking, pigs closely resemble humans [6]. In addition, early development of the porcine gut microbiota community is more standardized, given the more consistent duration of lactation and co-habitation, for instance. For piglets, four subsequent growth phases are described, which are each well-defined, namely lactation, nursery, growing, and the final phase of weight increase named finishing. During the lactation stage, the piglet is co-housed with littermates and the mother sow. The piglets are then separated from the sow (weaning) and are co-housed with piglets of a similar age throughout the subsequent growth phases until they have reached their adult market weight. Due to these more standardized circumstances, projecting the knowledge of the porcine gut colonization on the human gut colonization might assist in a better understanding of the latter.

2. Human Bacterial Gut Colonization

Intestinal bacterial colonization in humans has been established as a sequence of different bacterial waves that support and replace each other. As most data are available for vaginally delivered breastfed infants, researchers summarize the state of the art based on data from those children. The process of developing a complex microbial community has shown to display consistent, distinguishable colonization waves which succeed each other. In humans, subsequent waves of colonization occur over the course of the first two years of life, leading to a more stable and adult-like microbiota around the age of 2 years [3]. While it was formerly proposed that bacterial colonization already started in utero [7], this has been refuted by recent studies [8][9]. Therefore, it is now generally accepted that newborns encounter their first bacteria during birth. As such, from all bacteria that the newborn encounters at birth, the first stable colonizers (first colonization wave) in humans comprise mostly facultative anaerobes such as enterobacteria and bacilli such as Streptococcus, Enterococcus, and Staphylococcus [10][11][12][13]. These bacteria remove the oxygen from the gut and thereby set an important prerequisite for the next colonization waves, which comprise strict anaerobes [14][15][16].
Once anaerobic, the genus Bifidobacterium (second colonization wave) expands rapidly, becoming the dominant member of the gut microbiota of the newborns with an exclusive milk-based diet at that time. Bifidobacterium degrades mucin and human milk oligosaccharides (HMOs), a major constituent of breastmilk. The molecules resulting from degradation of HMOs can then be further metabolized by other bacteria that cannot or only partly metabolize HMOs, a mechanism called cross-feeding [17]. As such, Bifidobacterium in turn helps to create a favorable environment for colonizers of the third wave, which comprises of Bacteroidota and other strict anaerobic bacteria belonging to the Clostridiales. Additionally, several butyrate-producing bacteria such as Anaerostipes, Roseburia, and Faecalibacterium are described to become part of the infant gut’s bacterial community at that time [13][18][19]. The transition from second to third wave appears to co-occur with weaning (when the infant is no longer breastfed) [10]. Some publications [12][18] also describe a distinct fourth colonization wave which comprises the further increase in Clostridiales, more specifically, Lachnospiraceae and Ruminococcaceae. The latter has been related to a shift in diet enriched in plant-based products [10], which is in line with data on the impact of dietary interventions on adult microbiota composition [20].
Some factors, however, impact this colonization pattern. The delivery mode is the most important factor, the one with the most profound repercussion on the gut microbiome development [21]. During vaginal birth, a newborn encounters maternal faecal, vaginal, and skin bacteria. While not all these bacteria have the ability to establish themselves in the infant gut [10], this microbial exposure at the start is markedly different from birth via caesarean section (CS), which is performed in a sterile manner. In contrast to vaginally born infants, infants born via CS have a lower abundance of Bifidobacterium and an almost complete lack of Bacteroidota. Furthermore, CS infants often have a higher abundance of Klebsiella oxytoca, Klebsiella pneumoniae, Enterobacter cloacae, Enterococcus faecium, Staphylococcus aureus, and Clostridium perfringens, several of which are typically hospital-associated bacteria and potential pathogens [21][22][23][24]. CS-associated alterations in the gut microbiota composition are most pronounced up to 6 months after birth, but even a much more prolonged effect on the gut microbiota is suspected [10]. In a large adult population (n = 1106), compositional differences based on the delivery mode could, however, no longer be identified [25], but long-term health effects are still under investigation. Additionally, formula feeding, resulting in a decrease in Bifidobacterium, and antibiotic use, resulting in an increase in facultative anaerobes such as Escherichia and Klebsiella, largely influence the developing gut microbiota compared to the colonization process described for breastfed, vaginally delivered babies [21].
Cooperation and dependence between different waves have been comprehensively described, yet this knowledge remains insufficient as it is deduced from interval sampling. The timing and length of the different colonization waves differ between infants, even when major colonization routes are similar (delivery mode, breastfeeding, etc.) [13]. With only limited timepoints, it is very difficult to reconstruct and understand the biological grounds for these differences, as a much more detailed view on the gut microbiota transitions would be required. However, since pigs have a more standardized course of their lives during the first weeks (birth, suckling, co-habitation), they might prove an elegant solution to learn how external factors influence the development of the gut microbiota, and more specifically, which events are inextricably linked to changes in the gut microbiota composition.

References

  1. Gentile, C.L.; Weir, T.L. The gut microbiota at the intersection of diet and human health. Science 2018, 362, 776–780.
  2. Flint, H.J.; Scott, K.P.; Louis, P.; Duncan, S.H. The role of the gut microbiota in nutrition and health. Nat. Rev. Gastroenterol. Hepatol. 2012, 9, 577–589.
  3. Tamburini, S.; Shen, N.; Wu, H.C.; Clemente, J.C. The microbiome in early life: Implications for health outcomes. Nat. Med. 2016, 22, 713–722.
  4. Abrahamsson, T.R.; Jakobsson, H.E.; Andersson, A.F.; Björkstén, B.; Engstrand, L.; Jenmalm, M.C. Low gut microbiota diversity in early infancy precedes asthma at school age. Clin. Exp. Allergy 2014, 44, 842–850.
  5. Depner, M.; Taft, D.H.; Kirjavainen, P.V.; Kalanetra, K.M.; Karvonen, A.M.; Peschel, S.; Ege, M.J. Maturation of the gut microbiome during the first year of life contributes to the protective farm effect on childhood asthma. Nat. Med. 2020, 26, 1766–1775.
  6. Bendixen, E.; Danielsen, M.; Larsen, K.; Bendixen, C. Advances in porcine genomics and proteomics—a toolbox for developing the pig as a model organism for molecular biomedical research. Brief. Funct. Genom. 2010, 9, 208–219.
  7. Aagaard, K.; Ma, J.; Antony, K.M.; Ganu, R.; Petrosino, J.; Versalovic, J. The placenta harbors a unique microbiome. Sci. Transl. Med. 2014, 6, 237ra65.
  8. Olomu, I.N.; Pena-Cortes, L.C.; Long, R.A.; Vyas, A.; Krichevskiy, O.; Luellwitz, R.; Mulks, M.H. Elimination of “kitome” and “splashome” contamination results in lack of detection of a unique placental microbiome. BMC Microbiol. 2020, 20, 1–19.
  9. Sterpu, I.; Fransson, E.; Hugerth, L.W.; Du, J.; Pereira, M.; Cheng, L.; Schuppe-Koistinen, I. No evidence for a placental microbiome in human pregnancies at term. Am. J. Obstet. Gynecol. 2021, 224, 296-e1.
  10. Korpela, K. Impact of delivery mode on infant gut microbiota. Ann. Nutr. Metab. 2021, 77, 11–19.
  11. Bittinger, K.; Zhao, C.; Li, Y.; Ford, E.; Friedman, E.S.; Ni, J.; Wu, G.D. Bacterial colonization reprograms the neonatal gut metabolome. Nat. Microbiol. 2020, 5, 838–847.
  12. Korpela, K.; de Vos, W.M. Early life colonization of the human gut: Microbes matter everywhere. Curr. Opin. Microbiol. 2018, 44, 70–78.
  13. Beller, L.; Deboutte, W.; Falony, G.; Vieira-Silva, S.; Tito, R.Y.; Valles-Colomer, M.; Matthijnssens, J. Successional stages in infant gut microbiota maturation. Mbio 2021, 12, e01857-21.
  14. Bäckhed, F.; Roswall, J.; Peng, Y.; Feng, Q.; Jia, H.; Kovatcheva-Datchary, P.; Wang, J. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe 2015, 17, 690–703.
  15. Houghteling, P.D.; Walker, W.A. Why is initial bacterial colonization of the intestine important to the infant’s and child’s health? J. Pediatric Gastroenterol. Nutr. 2015, 60, 294.
  16. Rodríguez, J.M.; Murphy, K.; Stanton, C.; Ross, R.P.; Kober, O.I.; Juge, N.; Collado, M.C. The composition of the gut microbiota throughout life, with an emphasis on early life. Microb. Ecol. Health Dis. 2015, 26, 26050.
  17. Turroni, F.; Milani, C.; Ventura, M.; van Sinderen, D. The human gut microbiota during the initial stages of life: Insights from bifidobacteria. Curr. Opin. Biotechnol. 2022, 73, 81–87.
  18. Milani, C.; Duranti, S.; Bottacini, F.; Casey, E.; Turroni, F.; Mahony, J.; Ventura, M. The first microbial colonizers of the human gut: Composition, activities, and health implications of the infant gut microbiota. Microbiol. Mol. Biol. Rev. 2017, 81, e00036-17.
  19. Moore, R.E.; Townsend, S.D. Temporal development of the infant gut microbiome. Open Biol. 2019, 9, 190128.
  20. David, L.A.; Maurice, C.F.; Carmody, R.N.; Gootenberg, D.B.; Button, J.E.; Wolfe, B.E.; Turnbaugh, P.J. Diet rapidly and reproducibly alters the human gut microbiome. Nature 2014, 505, 559–563.
  21. Shao, Y.; Forster, S.C.; Tsaliki, E.; Vervier, K.; Strang, A.; Simpson, N.; Lawley, T.D. Stunted microbiota and opportunistic pathogen colonization in caesarean-section birth. Nature 2019, 574, 117–121.
  22. Thomson, P.; Medina, D.A.; Garrido, D. Human milk oligosaccharides and infant gut bifidobacterial: Molecular strategies for their utilization. Food Microbiol. 2018, 75, 37–46.
  23. Penders, J.; Thijs, C.; Vink, C.; Stelma, F.F.; Snijders, B.; Kummeling, I.; Stobberingh, E.E. Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics 2006, 118, 511–521.
  24. Stokholm, J.; Thorsen, J.; Chawes, B.L.; Schjørring, S.; Krogfelt, K.A.; Bønnelykke, K.; Bisgaard, H. Cesarean section changes neonatal gut colonization. J. Allergy Clin. Immunol. 2016, 138, 881–889.
  25. Falony, G.; Joossens, M.; Vieira-Silva, S.; Wang, J.; Darzi, Y.; Faust, K.; Raes, J. Population-level analysis of gut microbiome variation. Science 2016, 352, 560–564.
More
© Text is available under the terms and conditions of the Creative Commons Attribution (CC BY) license; additional terms may apply. By using this site, you agree to the Terms and Conditions and Privacy Policy.
Upload a video for this entry
Information
Subjects: Microbiology
Contributors MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to https://encyclopedia.pub/register :
Michiel Van de Vliet
,
Marie Joossens
View Times: 512
Revisions: 2 times (View History)
Update Date: 28 Sep 2022
Table of Contents
    1000/1000
    Hot Most Recent
    Academic Video Service
    Feedback