Microbial nutrient niches in the gut

Abstract

The composition and function of the mammalian gut microbiota has been the subject of much research in recent years, but the principles underlying the assembly and structure of this complex community remain incompletely understood. Processes that shape the gut microbiota are thought to be mostly niche-driven, with environmental factors such as the composition of available nutrients largely determining whether or not an organism can establish. The concept that the nutrient landscape dictates which organisms can successfully colonize and persist in the gut was first proposed in Rolf Freter's nutrient niche theory. In a situation where nutrients are perfectly mixed and there is balanced microbial growth, Freter postulated that an organism can only survive if it is able to utilize one or a few limiting nutrients more efficiently than its competitors. Recent experimental work indicates, however, that nutrients in the gut vary in space and time. We propose that in such a scenario, Freter's nutrient niche theory must be expanded to account for the co-existence of microorganisms utilizing the same nutrients but in distinct sites or at different times, and that metabolic flexibility and mixed-substrate utilization are common strategies for survival in the face of ever-present nutrient fluctuations.

Figure 1

Niche‐space diagrams representing nutrient niche concepts related to the abiotic (A‐C) and biotic (D, E) environment. The total niche space is shown as a large ellipse and the realized niche for each species is represented as a circle. Species are represented by letters a‐k. A. Freter's concept of nutrient niches considering well‐mixed nutrients and equilibrium conditions: each species occupies a preferred nutrient niche. B. Exploitation of the same nutrient niche by different species under non‐equilibrium conditions (i.e. unbalanced growth): at different times g and h have the same nutrient niche as d and b respectively. C. Extension of Freter´s theory assuming spatial structuring (i.e. Restaurant hypothesis): the same nutrient niche can be used by different species (e.g. a and i, e and j) at distinct sites. D. Niche switching and niche partitioning due to metabolic flexibility of species. Changes in the nutrient landscape force e and c to switch their niches, and a and c partition the previous niche of a. E. The effect of obligate and facultative dependencies, as well as keystone species. Nutrient fluctuations lead to disappearance of a keystone species k. Species e is completely dependent on the activity of k and goes extinct, while a is able to switch its niche and persist in the absence of k. R = species richness.

Figure 2

Consequence of nutrient fluctuations on species abundance considering different models of nutrient niches. A. In Freter's nutrient niche model species a abundance is determined by a single limiting nutrient (n₁). B. In the mixed substrate utilization model a uses several nutrients (n_1‐n₃) simultaneously and changes in the level of single nutrients has minimal effects on its abundance. C. If there is a heterogeneous distribution of nutrients (i.e. Restaurant hypothesis) a and b use the same nutrient (n₁) at different sites and are affected by local nutrient levels. D. Niche partitioning: Species b invades and outcompetes a for nutrient n₂. E. Obligate and facultative dependencies with keystones: b is completely dependent on the nutrient k’_n1 provided by keystone species k and goes extinct when k is absent, while a is metabolically flexible and can switch to another nutrient (n₁) when k is absent.

Figure 3

Spatial heterogeneity of the gut microbiota in the gastrointestinal tract. Gradients of pH and oxygen along the longitudinal axis limit the bacterial load in the proximal regions of the small intestine, whereas the large intestine carries high bacterial loads. Simple nutrients abound in the small intestine and sustain the growth of taxa able to effectively scavenge these compounds. In contrast, the large intestine is populated by taxa that can break down recalcitrant compounds. There is also spatial heterogeneity along the cross‐sectional axis of the intestine, with the mucus layer and the lumen harboring distinct microbial communities that reflect differences on nutrient availability. Fine‐scale spatial structuring is observed in both the mucus and lumen, with a heterogeneous distribution of nutrients sustaining different bacterial communities at particular sites.