The small intestine microbiota, nutritional modulation and relevance for health

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Highlights

  • The genera Streptococcus and Veillonella are active small intestinal commensals.

  • The streptococci of the small intestine are phylogenetically and functionally diverse.

  • The small intestine microbiota is amenable to dietary modulation.

  • Host–microbe interactions in the small intestine strongly affect immune, metabolic and endocrine functions.

  • The small intestine microbiota plays important roles in human health and disease.

The intestinal microbiota plays a profound role in human health and extensive research has been dedicated to identify microbiota aberrations that are associated with disease. Most of this work has been targeting the large intestine and fecal microbiota, while the small intestine microbiota may also have a profound impact on various aspects of the host's physiology, including immune, metabolic and endocrine functions. This review highlights the recent advances made in the study of the human small intestine microbiota. In addition, it describes recent human and animal studies that underpin the importance of this part of the intestine for health of the host organism.

Introduction

The different regions of the human intestine harbor distinct bacterial communities that vary in density and diversity [1]. The fecal microbiota composition has been associated with host health and disease, and its easy accessibility has stimulated its characterization in various human cohorts [2]. In contrast, limited information is available for the human small intestine (SI) microbiota characterized by its relatively low-density (102–107 cells/g), which is largely due to the rapid luminal flow and secretion of bactericidal substances (e.g. bile acids) in this part of the intestinal tract [3]. The SI is responsible for approximately 90% of the overall energy absorption from the diet [4] facilitated by the large surface area of its mucosa. Adequate absorptive capacity depends on maintenance of mucosal integrity that is constantly challenged by its exposure to the luminal milieu, including the microbiota. Mechanisms that contribute to this mucosal integrity, include the production of antimicrobial peptides (AMPs), a physical mucin barrier, and mucosal antibodies. Especially the terminal ileum is associated with the largest mass of lymphoid tissue in the human body, that is, the gut-associated lymphoid tissue (GALT) and Peyer's patches [5], which are essential for maintenance of a microbiota-accommodating immune homeostasis via dedicated luminal antigen-sampling (see also Box 1).

As a consequence of the fundamental role of the SI in the host's nutritional- (metabolic) and immune- status, it is highly plausible that this region of the intestine, and its endogenous microbiota, have profound influence on host physiology [6, 7]. This review describes the state of our knowledge of the SI microbiota and the role of this region of the intestine in host health.

Section snippets

Sampling of the small intestine

The SI is poorly accessible in healthy individuals and collection of luminal samples during routine gastroduodenoscopy and colonoscopy practices is challenging [8, 9, 10••]. As an alternative, intraluminal naso-ileal catheters facilitate the collection of such samples [1, 11••]. However, volunteers are fasted before placing such catheters and sampling may require luminal flushing, which may interfere with the accurate determination of the ‘normal’ SI microbiota in human individuals. Moreover,

The human small intestinal microbiota

Microbiota composition analysis of ileostoma effluent revealed that individual subjects harbor a distinct microbiota. Contrary to the more stable fecal microbiota [15, 16], the SI microbiota displays pronounced compositional fluctuations during the course of several days and even within a day, which most likely reflect the subject's dietary variation [13]. The microbiota can encompass subject-specific genera like Clostridium, Escherichia, and Turicibacter in variable amounts, but Streptococcus

Microbiota-driven SI immune development in health and disease

Throughout the host lifespan, complex-signaling and dynamic-signaling interactions shape the interplay between host and microbiota [19], including spatial and temporal variations within the different regions of the intestine [20, 21]. Exposure of the newborn to the maternal microbiota initiates the intestinal colonization by the microbiota of which the composition varies dramatically during the first year of life, after which it stabilizes to establish a complex and host-specific microbial

Microbiota impacts on SI metabolism and gut-brain signaling

The gut microbiota affects host metabolism through various physiological processes, including the production of short-chain fatty acids (SCFAs). Emerging evidence shows that SCFAs produced by the microbiota interact with host enteroendocrine cells (e.g. L cells) by modulating G protein coupled receptor (GPR41, GPR43) signaling [45], impacting on the production of glucose homeostasis modulators like peptide YY (PYY) and glucagon-like peptide (GLP)-1 [46]. SCFAs may further control intestinal

Targeting the SI ecosystem to improve consumer health

Diet is a major driver of population dynamics of the SI microbiota, which may strongly influence the interactions between the microbiota and the mucosa in the SI, which can impact on the host health [50, 57]. This notion is supported by recent in vitro studies that highlighted the considerable variation in immunomodulatory capacities of streptococcal isolates from the SI (unpublished data) and the proposed role of SI butyrate-producing microbes in T2D control [10••]. These diet-induced effects

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

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    These authors have contributed equally to this manuscript and share first authorship.

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